24

Proprioception and
Neuromuscular Control
Todd S. Ellenbecker, DPT, MS, OCS, SCS, CSCS, George J. Davies, DPT, MEd, SCS,
ATC, CSCS, and Jake Bleacher, PT, MS, CSCS

Chapter ObjeCtIves

l Define proprioception, kinesthesia, and other related asp­ l Identify factors associated with diminished proprioception
ects by using terminology consistent with the expanded and the effects of injury, disuse, and aging on neuromuscular
classic definitions contained in this chapter. control and joint stability in the upper and lower extremities.
l Identify the different types and functions of mechanore­ l Design and implement progressive proprioception training
ceptors in the upper and lower extremities. programs that meet the functional demands of the patient
l List and describe clinical measurements of proprioception and are appropriate for the patient's level of skill and recov­
and kinesthesia in the upper and lower extremities. ery when returning from an upper or lower extremity injury.

Human beings are unique in their capacity to propel themselves the CNS (spinal cord, brainstem and cerebellum, and cerebral
through their environment in an upright posture. This ability cortex), with the end result being coordinated muscle activity
is achieved through a complex interaction of lower limb mus- during movement to maintain joint stability.1 The motor
cle activity coordinated by the central nervous system (CNS). response varies depending on joint position, type of force,
To maintain balance and postural control we rely on sensory direction of force, and which higher center predominates in
information from the periphery from our visual, vestibular, and processing the information.
somatosensory systems. The nervous system integrates this Segmental spinal reflexes involve the processing of afferent
peripheral afferent information to maintain postural control input between peripheral receptors in the muscle spindle and
during stance. Golgi tendon organs at the musculotendinous junction with
Control of locomotion, including walking or running, occurs the efferent output of motor neurons in the ventral horn of the
through complex neural pathways in the spinal cord called spinal cord. On the most basic level, monosynaptic reflexes pro-
central pattern generators or limb controllers. These motor duce an excitatory or inhibitory efferent motor response to the
programs for locomotion are automatic but are modulated by stimulus received from the periphery. Along with the physiologic
the CNS through feedback and feedforward mechanisms. The properties of the muscle itself (length-tension curve), these
feedforward mechanism operates on the premise of initiating peripheral receptors potentially assist in modulating muscle
a motor response in anticipation of a load or activity that will stiffness, with muscle tension varying according to the amount
disrupt the integrity of a joint and gauges the response from of afferent input.1
previous experiences. In contrast, the feedback system operates The afferent information received in the cortical area of the
directly in response to a potentially destabilizing event by using brain from peripheral mechanoreceptors produces a voluntary
a normal reference point to monitor the muscle activity neces- motor response to potential disturbances in functional joint
sary to restore homeostasis.1 stability. The latency of the response is usually greater than
Both feedback and feedforward systems rely on processing 120 msec and sometimes longer, depending on the amount of
of afferent information from the periphery at different levels of information in the environment being processed. In addition to

524

C H A P T E R 2 4    Pro p r i o c e p t i o n a n d N e u ro m u s c u l a r C o n t ro l 525

the response to an environmental stimulus, the potential exists be a product of sensations induced by external forces that result
for a theorized motor program operating under the assump- in a change in limb position with noncontracting muscles. The
tion that the individual components of performing skilled sensation of active movement (or kinesthesia as it is now better
­movements, such as swinging a bat, that require sequential steps known) encompasses the appreciation of change in position of a
would be difficult to enact successfully without having a prepro- limb with contracting muscles. Appreciation of the position of a
grammed set of instructions to optimize efficiency, speed, and limb in space has been termed stagnosia, and finally, in the pres-
coordinated muscle activity.2 ence of tension, appreciation of force applied during a voluntary
The function of the cerebellum and brainstem is to ­integrate contraction has been termed dynamaesthesia .8 Although these
peripheral feedback from the environment with the motor expanded definitions found in the classic ­literature provide addi-
­commands from the cerebral cortex to enable humans to ­perform tional information about human proprioception, adaptations of
skilled and coordinated movement. The action of these neural these classic ­definitions have been suggested and are used for the
centers allows the adjustments needed to carry out an intended purposes of this ­chapter (Box 24-1).
motor skill with precision and efficiency.2
A PubMed search of the terms proprioception and neuro- Afferent neurobiology
muscular control was performed in October 2010. The results
identified 305 references, the majority (260) of which have been of the joint
published during the last decade. However, when the search Early work on afferent proprioceptive function of the human
is limited to higher levels of evidence, including randomized joint included investigations into the role of joint- and muscle-
controlled trials (RCTs), systematic reviews, and metaanalysis based afferent receptors in human active and passive movement
studies, the actual number is 37 high-quality studies. In one and detection of joint position.8 In 1898 Goldsheider proposed
such study, Riemann et  al3 performed a literature review to that the sensation of passive movements was solely the product
­identify sensorimotor assessment techniques, many of which of joint-based receptors. This view is still widely accepted today
are described throughout this chapter. Their conclusions indi- for passive movements.7,8
cate that the complex ­interactions and relationships among The view up until the 1970s about the sensory feedback of
the ­individual ­components of the sensorimotor system make active human movements was that when voluntary movement
­measuring and analyzing specific characteristics and functions was initiated by the cerebral cortex, only low-level control was
difficult. Additionally, the specific assessment techniques used to presented by the receptors in muscles and tendons. This sensory
measure a variable can influence the results obtained. Optimizing information from the muscles and tendons yielded information
the application of sensorimotor research to clinical settings can to the spinal cord and some subcortical extrapyramidal parts of
best be accomplished through the use of common nomenclature the brain such as the cerebellum but played no contributing role
to describe the underlying physiologic ­mechanisms and specific in conscious sensation, which remained in the province of the
measurement techniques. joint receptors.8 In the early 1970s, however, important research
by Goodwin et  al9 and Eklund10 independently demonstrated
the important role that muscular receptors play in contributing
Definitions to sensations of active movement qualitatively. This section of
Review of the orthopedic and musculoskeletal rehabilitation the chapter focuses on both joint- and muscle-based afferent
­literature identifies many different versions of definitions for ­receptors to allow the clinician a more complete understanding of
the terms associated with joint proprioception and neuromus- the sources of afferent information in the human body. This will
cular control. In Goetz's Textbook of Clinical Neurology, pro- later lead to a greater understanding of how specific ­treatment
prioception is defined as any postural, positional, or kinetic strategies can be used clinically to improve ­proprioceptive and
information provided to the CNS by sensory receptors in neuromuscular function in both upper and lower extremity
muscles, tendons, joints, or skin.4 Other texts define proprio- rehabilitation (Box 24-2).
ception as “awareness of the position and movements of our
limbs, fingers, and toes derived from receptors in the muscles,
tendons and joints.”5 Sherrington's classic definition of prop-
rioception is “afferent information arising from the proprio-
ceptive field,” and mechanoreceptors or proprioceptors were Box 24-1
identified as being the source of the origination of this afferent
information.6 Definitions of Proprioception and Associated
These original definitions of the term proprioception continue Functions in Humans
to be used today; however, a more advanced definition of the Proprioception: Afferent information, including joint position
sensory functions that encompass human proprioceptive func- sense, kinesthesia, and sensation of resistance
tion is clearly needed. In a classic monograph titled Physiologie Joint position sense: The ability to recognize joint position in space
des Muskelsinnes, Goldsheider7 proposed that muscle sense be Kinesthesia: The ability to appreciate and recognize joint
divided into four distinct and separate sensory functions. These movement or motion
functions were described as sensation of passive movements, Sensation of resistance: The ability to appreciate
sensation of active movements, sensation of position, and appre- and recognize force generated within a joint
ciation or sensation of heaviness and resistance. These original Neuromuscular control: Appropriate efferent responses
classifications or definitions have been expanded to decrease to afferent proprioceptive input
confusion. The sensation of passive movements is considered to

and are represented by plexuses Factors Affecting Joint Proprioception of small unmyelinated nerve fibers or free nerve endings. The type II present in noncontractile capsular and ligamentous structures in receptor is considered to be a dynamic mechanoreceptor whose human joints (Table 24-1). and skin. They are numerous in the The type I and type II mechanoreceptors described in the pre- capsular tissues of all the limb joints. and velocity of joint movements. Type III receptors are adapting mechanoreceptors. When considerable stress is ­generated in the joint Type II mechanoreceptors are elongated. particularly at Mechanoreceptors are sensory neurons or peripheral afferents the ­border between the fibrous capsule and the subsynovial located within joint capsular tissues. The Injury type IV receptor represents the pain receptor system of articu- Surgery lar tissues and is entirely inactive in normal circumstances. changes in intraarticular pressure. with thick multilaminated connective tissue capsules. The type I receptor is categorized as both a tendon organ. Wyke12 reported that the popula. as well as the apophyseal ceding paragraphs are the primary receptors located in the joint joints of the vertebral column. joints. and III receptors. These type III receptors are found in both joints than in distal joints. Type I receptors are typically located intrinsic and extrinsic ligamentous structures12 and are similar in the superficial layers of the joint capsule. the receptors remain acti- joints but are reported to be present in greater number in distal vated centripetally at a high velocity only if extreme joint displace- ment or joint traction is maintained. Research delineating the type of type I receptors allows the body to know where the limb is III mechanoreceptor classifies this receptor as a high-threshold. placed and receive constant input on limb position in virtually slowly adapting structure. the type III receptor will become actively stimulated. The final joint receptor to be discussed in this section is the Box 24-2 type IV receptor. adjacent periosteum.526 Physical Rehabilitation of the Injured Athlete Classification of Afferent joints than in proximal joints. ­fibroadipose tissue and often alongside articular blood vessels. ligaments. muscle. receptors and are reported to be entirely inactive in ­immobile which elicits an action potential. become taut. Type Fatigue IV receptors are typically distributed throughout the fibrous Immobility joint capsule.14. in nature to the Golgi tendon organs found in tendons. slowly cussed in later sections of this chapter. capsule. Aging ­bradykinin. near their bony attachments.12 These receptors become activated for very brief moments ent mechanoreceptors have been classified and are commonly (1 ­second or less) at the onset of joint movement. and other inflammatory exudates produced by Arthritis damaged or necrosing tissues can stimulate activation of the type IV receptor.12 Deformation or stimulation of the tissues in which Type II ­mechanoreceptors are low-threshold. II.12 The resting discharge ments.13 Four primary types of affer. rapidly ­adapting the mechanoreceptors lie produces gated release of sodium. unlike type I. conical corpuscles ligaments. again similar in nature to the Golgi any joint position.11. Disuse Marked mechanical deformation or chemical irritation such Ligamentous laxity as exposure of the nerve endings to agents such as histamine.1 Type II corpuscles are located Mechanoreceptor in the deeper layers of the fibrous joint capsule. extreme ranges of joint motion where the ligamentous structures and the direction. These type III receptors are completely inactive in static and dynamic mechanoreceptor12 whose discharge pattern immobile joints and become active or stimulated only toward the signals static joint position. type I receptors are low-threshold. and articular fat pads. These receptors are noncorpuscular. A proportion of type I receptors found predominantly in the superficial surfaces of the joint liga- are always active in every joint position. brief.15 Table 24-1 Classification of Mechanoreceptors in the Human Body Type Location Threshold Response Active I Superficial joint capsule Low Slow adapting Always Limbs and vertebrae Static/dynamic Greater density proximal joints II Deeper layers of the joint capsule Low Rapidly adapting Dynamic only Greater density distal joints III Superficial surface of the joint High Slowly adapting Dynamic end-range movements Ligament Joint traction IV Joint capsule. tendons. Type III receptors are primarily confined to the joint liga- tion of type I receptors appears to be more dense in proximal mentous structures. amplitude. These Wyke14 also reported that type III receptors become activated type II corpuscles are present in the fibrous capsules of all with longitudinal traction on the limbs. as dis- Physiologically. adjacent periosteum — — Not active in normal Articular fat pads circumstances . corpuscles with a very thin capsule. ­high-velocity discharges signal joint acceleration and Type I articular receptors are traditionally globular or ovoid ­deceleration during both active and passive joint movements.12.

15. The most common mechanoreceptor in the lower extremity was the classic Ruffini end-organ in the capsular ligaments of The distribution of afferent articular nerves in synovial joints the glenohumeral joint. III.12 These receptors have also been identified in the menisci of may play a role in regulation of shoulder movement. Two types of slowly adapting Ruffini ing rapid stretch of a muscle during an eccentric contraction or end-organs and rapidly adapting pacinian corpuscles were ­passive stretch. They function as rapidly adapting. show how the capsular ligaments of the glenohumeral joint aid ceptors. In the limbs. consist of nuclear bag and nuclear chain fibers. labrum. Further the knee. These pacinian receptors are more prevalent in distal ous free nerve endings. significant ­contributions to the regulation of human movement and prop- Afferent joint receptors rioceptive feedback are obtained from receptors located in con- tractile structures. subacro- stimuli resulting from an inflammatory response. mechanoreceptors.21 Nuclear bag fibers are ­ligaments. most of which were present on the roof side tion. They found two types innervated by γ1 (dynamic) motor neurons and are more sensitive of mechanoreceptors and free nerve endings in the ­glenohumeral to the rate of change in muscle length. In addition. Pacinian corpuscles were less abundant consists of medium and large myelinated fibers innervating overall.2 mial bursa. however.16 Ide et al19 did find Type III or Golgi tendon organ–like endings are found pre. and collateral receptors was found in the glenoid labrum. such as that occurring dur- joint capsular ligaments. function of the shoulder.20. which is exposed to impingement-type and joint movement at constant velocity. The subacromial bursa was found to have diffuse. free nerve ligaments of the knee. cruciate. evidence of both Ruffini and pacinian ­mechanoreceptors in the dominantly in intraarticular and extraarticular joint ligaments. tendon organ. and inferior portions of the glenohumeral ligaments. These receptors respond to changing mechanical stress in the provision of afferent proprioceptive input by their inher- and are always active because of the gradient pressure difference ent distribution of both type I Ruffini mechanoreceptors and in the joint capsule. middle. in the upper extremity Two of the primary mechanisms for afferent feedback from The classification system mentioned earlier for the four primary the muscle-tendon unit are the muscle spindle and the Golgi types of mechanoreceptors found in human noncontractile cap. bursa. subacromial bursa. Their findings suggest that the ­subacromial including the collateral ligaments and cruciate ligaments in the bursa receives both nociceptive and proprioceptive stimuli and knee. high-threshold receptors with a function similar information and enhance the understanding of proprioceptive to that of the Golgi tendon organs found in tendons. Kikuchi17 and Shimoda18 reported that type II the small end-organs or mechanoreceptors throughout joint pacinian corpuscles were more commonly found in the capsular tissue. slowly adapting mechanore.2 stress.16 In this way the type are not as prevalent in the distal joints of the ankle. the meniscofemoral. type II receptors are located endings were noted in the fibrocartilage tissue in the peripheral in the intraarticular and extraarticular fat pads of all synovial half.2 Type III Golgi tendon organ–like endings are structur. and IV mech- Type I or Ruffini receptors located in the superficial layers of anoreceptors in human coracoacromial ligaments. and found a copious supply of low-threshold receptors and respond to acceleration. and passive joint movement but are silent during inactivity of the subacromial arch.20 Intrafusal nuclear chain fibers are innervated by . and subacromial bursa. Ide et  al19 also studied the subacromial mal joints such as the hip. and collateral ligaments of the knee. more ­complex joints such as the ankle and are less densely distributed in proxi.20. These reviews the joint capsule are low-threshold. research into the exact distribution of these important ­structures ally identical to the Golgi tendon organ receptors and ­function as in the human shoulder is indicated to give clinicians further slowly adapting. They are completely inactive in normal situations and In addition to the afferent structures found in noncontrac- are activated by marked mechanical deformation or ­chemical tile ­tissues of the human shoulder (joint capsule. cruciate. These type IV receptor Afferent receptors nerve endings are found throughout the joints of the extremities of contractile structures in the fibrous capsule and adjacent periosteum and in the articu- lar fat pads and are the most prevalent receptor type in the knee in the upper extremity menisci. yet copi- joints. and intrinsic and extrinsic ligaments). II. Vangsness et al16 studied the neural histol. A rapidly adapting movement because of their location in the superficial portion of receptor such as the pacinian receptor can identify changes in the joint capsule.2 Several authors have also studied the labrum and subacromial Type II or pacinian receptors are located in the deep layers bursa. type I receptors are found to be tension in the joint capsular ligaments but quickly decreases its more densely distributed in the proximal joints of the hip and input once the ­tension becomes constant. however.21 These two groups in the human body. with no evidence of larger. They undergo deformation with natural the more rapidly adapting pacinian receptors. including the glenohumeral fibers ­project from large afferent axons. taken from three cadavers. free nerve endings. with the remaining 45% consisting knee. Type IV free nerve endings function as the pain receptor or nociception system in synovial joints.14 provides ditionally grouped intrafusal muscle fibers into two groups generalized information about the location of these receptors based on the type of afferent projections. Vangsness et al16 reported that no evidence of mechano- of the joint capsule.12 receptors. Analysis of the coracoclavicular and acromioclavicular of small unmyelinated fibers that transmit nociception or pain ligaments showed equal distribution of type I and II mechano- sensation. Unlike the study by Vangsness et al. Morisawa et al13 identified type I. tion of the ­tension on a ligament. decelera. Nuclear chain ogy of the human shoulder joint. These nerves represent approximately 55% of the total ligaments of the human glenohumeral joint than in the human ­quantity of articular nerves. C H A P T E R 2 4    Pro p r i o c e p t i o n a n d N e u ro m u s c u l a r C o n t ro l 527 Afferent mechanoreceptors i­dentified in the superior.12 Ruffini II receptor has the ability to monitor acceleration and decelera- receptors have also been found in the meniscofemoral.20 Research classifying muscle spindles has tra- sular and ligamentous tissues described by Wyke12.

control tion. These tendinous mechanoreceptors actively move the extremity to the specified angle without visual are present in the human shoulder and respond to the tension input. When subjects initially detect movement to occur. The patient is then asked to ity is the Golgi tendon organ. Lower spindle densities have been reported for has been more standardized in the literature. visual. Muscles that cross the [1992]: Proprioception following anterior cruciate ligament reconstruction. (From Lephart.20 Muscle spindles do not occur in h.5°/sec. however. with simultaneous stimulation of antagonis. that occurs with predictable or programmed movement pat. activation and whether the subject overestimates or underestimates knee of the tension-sensitive Golgi tendon organ produces a protective position is not considered. Spindle density device.24 This kinetic link activation concept control switch to indicate that the test leg has been moved. with the subscapularis and described by Barrack et al27 and Skinner et al28 involves placing infraspinatus having greater densities than the supraspinatus and the subject in a seated position with the leg hanging freely over teres minor.22 Muscles with attachment to the coracoid. Muscle spindles provide much of the primary information F i g u re  2 4 . con- mechanism that causes relaxation of the agonist muscle that is sider both the magnitude and direction of the error and can be undergoing tension. pectoralis minor. with greater densities of by measuring angular displacement until the subject senses muscle spindles being reported in muscles that initiate and con- motion in the knee. Upper levels of the CNS can bias the sensitivity of muscle panel. position for several seconds. and passive return of the extremity The second major aspect of musculotendinous afferent activ.22 This lower rotator cuff spindle density probably the seat and suspended by a motorized pulley system in 90° of suggests synergistic mechanoreceptor activation with the scapu. J.23 This coupled or shared mechanoreceptor activation is ing of a blindfold.15. spindle input and sampling.26 The method the rotator cuff muscle-tendon units.. also have high of angular position for joint position sense.M. F. The combination of nuclear chain and nuclear bag fibers allows afferent communication from the muscle-tendon unit to c remain sensitive over a wide range of joint motion during both h reflex and voluntary activation (Table 24-2). they engage a terns in the human body. d. S. including muscle length and joint posi- transducer. mates the reference angle. g. starting reference angle.20. Real error calculations.2. With tendon organs relays afferent feedback about muscle ­tension and absolute error.29 Barrack et al30 ­demonstrated through studies on proprioception that extremities with no ­evidence of Clincal assessment pathologic conditions have a high degree of symmetry in joint of proprioception position sense. as a protective mechanism. stationary arm. digital microprocessor. M. b.S.1 Proprioceptive testing device. and open chain (seated) versus closed . Because essentially no standard protocols have been estab- in the lower extremity lished for measuring joint position sense or for performing joint The two primary tests measuring proprioception and ­kinesthetic replication tests. 24-1). many variations exist. Tactile.H. Additionally. Initiation of movement into either flexion or an example of the kinetic link or proximal-to-distal sequencing extension proceeds at a rate of angular deflection of 0. The threshold for detecting passive movement is assessed is probably related to muscle function. and auditory cues are elimi- lothoracic musculature during movement of the glenohumeral nated with the use of custom-fitted Jobst air splints and wear- joint.20 Activation of the Golgi be calculated as either an absolute or a real angular error. 1:188–196. motor. moving arm. the extremity to a specified angle by the clinician. Fu. Rotational for motor learning. only the magnitude of the error is determined. and coracobrachialis. pneumatic compression similar density in all muscles in the human body. used to determine whether a subject overestimates or underesti- tic musculature. holding of the nohumeral joint and is discussed later in this chapter..528 Physical Rehabilitation of the Injured Athlete Table 24-2 Characteristics of the Muscle Spindle Fiber Motor Type Length Axon Type Function Nuclear 7-8 mm Medium size Stimulation of larger f e bag long motor fibers increases tension in the bag. The difference between the actual and replicated angle can generated by muscular contraction.25. Kocher. b d γ2 (static) motor neurons and are more sensitive to static muscle i length. to the starting reference position. a. handheld disengage switch..) have a very high number of muscle spindles per unit of muscle weight. active ­passive motion (TTDPM) for movement sense and ­reproduction or passive reproduction. such as the pectoralis major and biceps. c. et al.. flexion (Fig. trol fine movements or maintain posture. pneumatic compression boot.28 is further demonstrated by the deltoid/rotator cuff force couple23 Testing for joint position sense involves passive movement of and other important biomechanical features of the human gle. e. including apparatuses awareness in the knee joint are the threshold to ­detection of used for angular measurement. such as the biceps. f. Sport Rehabil. The TTDPM test spindle densities. g a Nuclear 4-5 mm Small Stimulation of smaller chain long motor fibers reduces tension on the bag. and i. front of the shoulder. joint position.

15. the magnitude of sway is compared with that on the uninvolved side. the TTDPM test is designed to selectively with specific reference stimulate the Ruffini or Golgi-type mechanoreceptors in the articular structures being tested. . Champaign. Their results may be due to the fact that proprioceptive input is greater in the standing weight- ­bearing position. Allegrucci et al39 measured greater sensitivity to passive move- ring typically at very slow angular velocities.. Consistent with earlier research. such as an instrumented (motorized) shoul.2 Upper extremity proprioceptive testing device.38 Allegrucci et  al39 measured shoulder kinesthesia kinesthesia. ings in this study suggest that athletes in unilaterally ­dominant der wheel35 and other devices such as the one used by the upper extremity sports may have a proprioceptive deficit in University of Pittsburgh.  24-2). This ensures Assessment of proprioception that only joint kinesthesia is being assessed and not simply visual and neuromuscular control or auditory responses to perceived movement.39 This finding ­provides test has resulted in the selection and recommendation of slow a ­rationale for proprioceptive upper ­extremity ­training in angular velocities (0. as well as the resulting muscular activation patterns.H. and sensation of resistance. Single-leg hop tests are often used for assessing stability in F i g u re  2 4 . patients with pathologic knee or ankle conditions. In Lephart. F. and the timed hop test. ear- phones. Kinetics. of neuromuscular control and joint kinematics.]: Proprioception and Neuromuscular Control. dominant or preferred hand relative to the nondominant texts.34 and passive motion was found to be enhanced (smaller evaluation are reviewed. S. The results showed that the athletes had greater ­difficulty Assessment of glenohumeral joint kinesthesia has been per. in healthy athletes who performed unilateral upper extremity Separate techniques can be used to assess each of these aspects sports. Single-limb postural stability tests have also been used for measuring the amount of sway in individuals with complaints of ankle instability. whose characteristics are described the dominant arm that may interfere with optimal afferent next (Fig.5° to 2°/sec) to enhance the reliability of ­athletes from this population. such as baseball. the crossover hop test. TTDPM in the human shoulder was measured by Blaiser clinical applications. The find- on the TTDPM. and tactile realm.15. The TTDPM of proprioception.5° to 2.2° for all testing condi- function. In this range positions of glenohumeral rotation. in the upper extremity Physiologically. in which multiple joints are being loaded. and a pneumatic cuff are recommended to eliminate cues from the visual. blindfolds.2. and leg strength has been inconclusive in ­studies to date. techniques used in research investigations. and chapters2. Normative data on 40 healthy college-aged individuals and Neuromuscular Control undergoing the TTDPM test were reported by Warner et al37 for the Shoulder from both neutral rotational starting positions and 30° of Evaluation of proprioception and neuromuscular control in the humeral rotation with 90° of glenohumeral joint abduction. and Fu.35 Elaborate test. to allow the clinician to perform a detailed et al.15.36 using the TTDPM feedback regarding joint position. detecting passive motion in the dominant ­extremity than in formed with a test called the TTDPM. The relation- [eds. as well as in lier.2 Extensive research2. joint position sense. and the instantaneous center of pressure is recorded along a graph. [2000]: Role of shoulder stabilization relative to restoration of the test include single-leg or triple-leg hop tests for distance. rehabilitation on restoring proprioception and neuromuscular Testing in the literature has been done at the midrange and end- control requires the use of clinical assessment techniques. Tropp et  al33 developed such a test for measuring ankle instability that has been used with variations throughout the years. test was performed with the shoulder in 90° of abduction and both 0° and 75° of external rotation and compared bilater- Measurement of Kinesthesia ally. human shoulder encompasses both afferent and efferent neural They found an average of 1. In addition to the device used.15. with no significant difference measured between the Proprioception for the purposes of this and many other articles. amount of movement before detection) at or near the end range of external rotation versus the midrange of external rotation or Primary Measures of Proprioception internal rotation. Testing is typically performed to the human shoulder for internal and external rotation of the glenohumeral joint in Determination of which patients require particular emphasis in varying positions of elevation in the scapular and coronal planes. ment with the shoulder in 75° of external rotation bilaterally ing devices have been used in several studies that have reported than with the shoulder in a more neutral condition.34 subject's or patient's ability to detect a passive movement occur. This test assesses the the nondominant extremity. tennis. data ­acquisition. or volleyball. C H A P T E R 2 4    Pro p r i o c e p t i o n a n d N e u ro m u s c u l a r C o n t ro l 529 chain (standing). Individuals stand for 60 seconds on a force platform. Variations (From Pollack.31 Lattanzio et al25 and Marks and Quinney32 used closed chain weight-bearing joint replications and reported a high degree of accuracy.34 consists of three major submodalities: extremity.M.) ­proprioception.2. R.15 tions.36 As stated ear- section. auditory. IL: Human ship of hop tests to functional parameters such as instability.

60.40. a seated position with an electronic digital inclinometer (EDI).. physical medicine and rehabilitation literature.15. ­replication testing to quantify arm position.59 but it is not typically consid- angular reproduction. Various authors2. mates the position initially selected as closely as possible.64 have shown decreased lated manual muscle test (MMT). Closed kinetic chain (CKC) upper extremity tests are also used Voight et al41 used an isokinetic dynamometer with 90° of abduc. the reader is referred is returned to a starting position. Inc. however. Widespread tion coefficient of 0. reported in the scientific and clinical literature. Each touch of the line is counted and of the afferent pathways of the human shoulder. Researchers have used both Closed Kinetic Chain Upper Extremity active2. The subject or patient then moves both hands back position replication tests primarily involve stimulation of both and forth and touches each line alternatively as many times as joint and muscle receptors and provide a thorough assessment possible in 15 seconds. with males averaging Assessment of Neuromuscular Control 18. in an attempt to provide a means of assessing the functional out pathologic shoulder conditions showed the average of the seven ability of the upper extremity more accurately.49 with ­regular physical activity. Testing procedures to assess is measurement of muscular strength. the upper extremity are limited. with an intraclass correla- to assess neuromuscular control of the shoulder. and the modified push-up has been used Angles chosen were greater than 90° and less than 90° of flexion ­clinically as an acceptable alternative to assess CKC function in and abduction. Normative Davies developed the CKC upper extremity stability test data developed by Davies and Hoffman for 100 male subjects with. Further ­discussion is ity. active joint angular the floor.44-47 functional method.40 This represents the average ­difference is initiated in the starting position of a standard push-up for between the seven reference angles and the actual matched angles males and modified (off the knees) push-up for females.61 The test measurements to be 2. Although wide- tion and elbow flexion and standard isokinetic stabilization to per. both upper and lower extremity strength. without any visual. spread use of CKC training techniques has been reported in the form active angular joint replication testing via a fatigue paradigm. and various apparatuses have been Testing used to facilitate the accuracy of joint angular replication testing.56. which is indicative of use of electromyographic (EMG) studies to measure muscular high clinical reliability between sessions with this examination activity during shoulder rehabilitative exercise. One of the “gold standards” in physical education for gross tial tracking devices and multiple positions of active joint angular assessment of upper extremity strength has been the push-up.56.43 have used complex three-dimensional spa. Two by the subjects over the seven measurements. or tactile cues. Davies and Hoffman40 tested subjects in ered appropriate for use in patients with shoulder dysfunction. Modification of the push-up with the EDI being used to verify the position of the ­extremity. and it has to as %MMT or %MVC (maximum voluntary contraction) been suggested that this decreased capacity for movement and allows comparison and expression of the relative activity of sense results in a higher incidence of falling and joint degenera- human muscle activity during activities of daily living (ADLs) tion in this population. This is commonly referred proprioceptive acuity in older adults with testing. 3 feet apart on Regardless of the testing methodology.49 and abnormal muscular activity pat- terns during planar motions50-52 and functional activities53 is Effects of aging. The subject then reapproxi. After this period of joint positioning. has been reported. the age-related decline in prop- rioception can be lessened through dampening of the effect of *Available from Cybex. the patient then attempted to replicate the angular position.15 tallied to ­generate the CKC upper extremity stability test score.5 touches and females averaging 20. to assess neuromuscular control of the shoulder. to Chapter 25. of the Shoulder The CKC upper extremity stability test has been subjected Several methods have been used by clinicians and researchers to a test-retest reliability measure. disuse atrophy on the neuromuscular system. in ­musculoskeletal rehabilitation.7°. Medway.62 Studies63. These MMT and the use of handheld dynamometers and isokinetic tests typically place the extremity in a particular position to allow ­apparatuses have been used extensively for the documentation of the subject to appreciate the spatial orientation of the extrem.927 being generated.36.2.* The positional demands placed on the anterior capsule and Reference angles were chosen in several ranges and verified with the the increased joint loading limit the effectiveness of this test EDI. the upper extremities. This test has been used to generate sport-specific normative In the most clinically applicable research study on active joint data in normal populations. Methods such as the joint position sense are called joint angular replication tests.54-58 currently They also used the passive mode of the isokinetic dynamometer existing evaluation methods to properly assess CKC function of set at 2°/sec to perform passive joint angular replication testing. strips of tape are placed parallel to each other. MA. external rotation greater than 45° and less than 45°. However.5 touches in 15 seconds. auditory. Most of these and injury on lower extremity studies comparing muscular activity expressed the contribution proprioception or activity of the muscle in terms of the amount of muscle activ- The effects of age and injury have been correlated with dimin- ity relative to the maximal activity assessed via a maximal iso- ished proprioceptive sense. and internal rotation greater than 45° and less than 45°. it has also been found that and sport-specific movement patterns.530 Physical Rehabilitation of the Injured Athlete Measurement of Joint Position Sense Muscular Strength Testing Joint position sense is the ability of the subject to appreciate where Another important aspect of assessing neuromuscular control the extremity is oriented in space.61 movement patterns such as the throwing motion48 and tennis serve and groundstrokes.42. Normative results have been established. instability.41 and passive41 angular replication tests for assess- ment of the glenohumeral joint.48. the subject's extremity beyond the scope of this chapter.2 In addition to .

The Measuring the ACL-hamstring reflex in patients with ACL inability to achieve full voluntary muscle contraction may lead rupture. posterior. Lephart and Fu2 and Nawoczenski et  al71 confirmed this decreased muscular ­stabilization in a study involving subjects with ankle instability. Examples of demonstrated no evidence of everter strength contributing to both glenohumeral joint instability and pathologic rotator cuff the functional instability. injuries to the lower extremity joints sus. lations were assessed in the presence of sequentially applied and muscular inhibition. climbing. Research performed by Warren et al72 and Barrett et al73 alone does not create large enough increases in humeral head suggested that joint replacement surgery may actually improve translation to allow anterior glenohumeral joint dislocation. the chronic instability was ­conditions are presented. Speer et al79 studied the effects of a simulated Effects of Knee Injury on Proprioception Bankart lesion in cadavers. reten. C H A P T E R 2 4    Pro p r i o c e p t i o n a n d N e u ro m u s c u l a r C o n t ro l 531 a­ ge-related deficits. joint position sense. The goal of joint replacement The relevance of this article to the current discussion on pro- surgery is to restore function through resurfacing joints. of the PCL will enhance dynamic joint stability through preser- matic event can create an environment in which degenerative vation of the neural reflexive pathway. with subjects showing significant improve. Therefore. However. and ultimately restoring dynamic the anterior inferior labrum from the glenoid (Bankart lesion) stability. ing during gait. A similar study by Lentell In this section the normal afferent neurobiology of the joint and et al70 tested subjects with chronic lateral ankle instability who periarticular structures is reviewed. This outcomes and gait parameters and proprioceptive scores.4 mm) in anterior and inferior transla- ligamentous tension resulting from narrowing of the joint space tion of the humeral head relative to the glenoid in all positions of contributes to the interruption in afferent signals for propriocep. Coupled anterior/posterior trans- Degenerative arthritis in the knee causes pain. insufficient stimula- tion of the mechanoreceptors used for proprioception occurs Effects of pathologic shoulder and results in decreased motor control. . The The results of studies to date on the selection of joint authors concluded that capsular elongation may be responsible ­prostheses and the effects of retaining versus sacrificing the for the high incidence of anterior reconstructions that fail to posterior cruciate ligament (PCL) on proprioception have been address anterior glenohumeral joint instability and do not fully inconclusive. Beard et al76 showed significant reflex latency delays to continued overload on the joints through the loss of dynamic that were directly correlated with functional instability.65 Hurley and Loss of stability of the ACL causes alterations in muscle activ- Newham66 and Sharma and Pai67 demonstrated arthrogenous ity and reflex patterns. superior. Andriacchi and Birac78 had similar findings cies. The effects of a simulated Bankart lesion were small combined with pain and altered muscle activity. The presence of pain and inflammation in a decreases in proprioceptive sense and altered muscle patterns joint produces an inhibitory effect on neuromuscular activation after rupture of the anterior cruciate ligament (ACL). With the loss of stability and neural tion to the hyperlaxity found in the ligamentous restraints in sensory input. inflammation. Using control and attenuation of force. They indicated that permanent stretching or elongation of the ment in position sense 6 months postoperatively.73–75 changes occur in the joint along with disruption of the neuro. in the capsuloligamentous restraints. and jogging. thus ­elongation or permanent stretching of the ligamentous struc- ­suggesting a relationship between restoration of proprioception tures may lead to alterations in the intrinsic tensile relationships and improved functional outcomes. One of the most common clinical maladies seen by clinicians is anterior glenohumeral joint instability. ity and the resultant delayed muscular reflex. joint instability on proprioception. It is theorized that without adequate tension ity in performance of normal ADLs. many individuals experience functional disabil- this population. prioception is that Speer et al79 concluded that detachment of sioning soft tissue structures. elevation and in posterior translation at 90° of elevation only. on Proprioception with a delay in onset latency in the peroneal muscles when Several studies have addressed the influence of glenohumeral ­subjected to sudden inversion stress. muscle inhibition in patients with degenerative arthritis. Limbird et  al77 showed variations in muscle Loss of capsuloligamentous stability has been shown to activation patterns with increased hamstring activation and cause proprioceptive deficits as a result of inadequate activation concomitant decreased quadriceps activity with joint load- of mechanoreceptors leading to delayed muscle reaction laten. ­inferior glenohumeral ligament may also occur and is ­necessary correlations have been made between improved functional to ­produce full dislocation of the glenohumeral joint. of the ­glenohumeral joint capsule and capsular ligaments. Effects of Glenohumeral Joint Instability The results of their studies supported this loss of motor ­control. EMG studies. with the unin. stair of ballet dancers and attributed this clinical loss of propriocep. A study by Garn and conditions on proprioception Newton69 also showed that individuals suffering from chronic ankle instability have diminished proprioception with a low and neuromuscular control threshold for passive ­plantar flexion. and inferior performance during gait and weight-bearing activities. ­retention tained as a result of repetitive microtrauma or a single trau. lothoracic joint. as well as dysfunction of the scapu- due to loss of mechanoreceptor function from ligamentous lax. joint integrity and retensioning soft tissue structures. it has been theorized that by restoring restore normal capsular tension in the anterior structures. Studies in the literature have consistently demonstrated muscular response. Furthermore.29 with decreased afferent mechanoreceptor signals. prioception and neuromuscular control are affected in patho- volved ankle being used as the control. Subjects in this study logic conditions of the shoulder are provided.79 tion and neuromuscular control.2 When directions.2. and examples of how pro- ­demonstrated decreased passive movement sense. which results in decreased functional loads of 50 N in the anterior. the inadequate increases (maximum of 3. Barrack et al68 found decreased proprioception in a group in patients performing normal activities of ambulation. primarily the ACL-hamstring reflex.1.

. tion. indwelling EMG electrode. and follow-through phases. and serratus anterior muscles in the ­surgery in this experiment appeared to restore normal joint prop. ­significant deficits in proprioception and mean strength that did ity (MDI) for joint angular replication in multiple positions. Their transverse splitting of the subscapularis had no deficits in results indicated a significant decrease in joint awareness in the ­proprioception and mean strength with respect to the contral- involved shoulders after shoulder dislocation in comparison to ateral uninvolved extremity. as evidenced by increased baseball pitchers to determine whether bilateral differences in activation of the primary dynamic stabilizers. laris require up to 1 year for return to the same ­functional level This study showed significant proprioceptive deficits in patient as the contralateral baseline extremity. Several studies highlighting changes ties (dominant versus nondominant) in the normal subjects’ pro. Significant decreases in serratus anterior muscle tested by Safran et al81 and found to have a kinesthetic deficit in activity were measured in all three planar motions in the group the injured dominant shoulder versus the nondominant shoul. including overhead reaching and abduction with external rota. deltoid. This study clearly shows the importance of the scapu- skilled baseball pitchers despite increases in laxity and training lothoracic musculature and dynamic stabilization during both effects. of subjects with anterior glenohumeral joint instability. however. Planar motions of flexion. ­subscapularis. terns of normal healthy baseball pitchers and compared them ated extremity versus the uninjured extremity after reconstructive with throwers with anterior glenohumeral joint instability. The surgery. underwent an open inferior capsular shift ­procedure involving lar reposition sense is one characteristic in individuals with an approach that detached the ­subscapularis from the lesser increased glenohumeral joint laxity. Individuals with greater glenohumeral joint laxity The finding of reduced proprioception in unstable shoulders were found to have less sensitive proprioception than were those has prompted researchers to examine the effect of surgical stabili- with less glenohumeral joint laxity. subjects with anterior ­instability had instability have been published. in neuromuscular control in subjects with glenohumeral joint prioceptive ability. ­tuberosity to gain exposure. Reconstructive simus dorsi. the other muscles—rotator cuff. abduc- rotation to end range of motion (ROM) between the extremi. None of der when moving from neutral rotation into internal rotation. This study shows that deficits in proprioception and strength tion. They found that JAR was more accurate decrease scapular stability and further jeopardize joint congruity in the nondominant extremity when moving from a position of through improper scapulothoracic muscle sequencing. Inhibition of joint angular replication ( JAR) and kinesthesia were present the ­serratus anterior in the group with anterior instability may between extremities. and the group with using an instrumented modification of a shoulder wheel. At 6 months postoperatively inherent joint position sense with that in 10 normal subjects by patients underwent proprioceptive testing. as well as selective der anterior instability. and scapular-plane elevation (scaption) were studied in 30° ties. not return to full functional values until 1 year postoperatively. went open capsular shift with subscapularis detachment had Barden et al80 tested subjects with multidirectional instabil. the group that under- all uninvolved shoulders tested in the study. throwing athletes with anterior glenohumeral joint instability. They concluded that decreased joint angu.53 using an significant differences between the normal and unstable shoulders. studied the muscular activity pat- Finally.53 Also of interest was the finding for partial deafferentation leading to proprioceptive deficits when of decreased muscular activation of the pectoralis major. No difference in propriocep. No significant difference was found between extremi. or scapular—showed a These results show JAR to be bilaterally symmetric from 75° of significant difference in testing during standard planar movement external rotation to end ROM between extremities in healthy patterns. Safran et al81 aggressive overhead and common ADL-type movement patterns. Measurements McMahon and et al83 tested normal shoulders and those with were taken in 90° of abduction. dynamic joint stability. 75° of external rotation into internal rotation. Lephart et  al36 studied glenohumeral joint proprioception in Effects of Glenohumeral Joint Instability 90 subjects in three experimental groups. Six collegiate pitchers with reports of shoulder pain were increments. Twenty-five underwent anterior Smith and Brunolli35 examined kinesthesia after gleno­ capsulolabral reconstruction with a transverse ­splitting approach humeral joint dislocation in 8 subjects and compared their to the subscapularis for exposure. This study was performed at least 6 months after subjects results of the study showed marked increases in muscular activa- underwent open or arthroscopic repair for chronic. a Rokito et al82 studied the effects of two open surgical procedures position at which the anterior capsular structures have greater for recurrent unidirectional anterior instability. latis- the capsuloligamentous structures are damaged.532 Physical Rehabilitation of the Injured Athlete Blaiser et al34 examined the proprioceptive ability of subjects did show very ­importantly that pitchers with a recent report of without known pathologic shoulder conditions and compared injury involving the shoulder do have kinesthetic deficits in the them with individuals with clinically determined generalized injured arm that may affect further performance. consistent with the studies mentioned earlier. The authors concluded that these results increases in the infraspinatus muscle during the early cocking provide ­evidence. joint laxity. This study showed ­neuromuscular compensations in the group Safran et  al81 used a testing device to study 21 collegiate with ­glenohumeral joint instability. another group consisted of on Neuromuscular Control 30 patients with anterior instability. rioception 6 months or more after the surgical procedure. recurrent shoul. Glousman et  al. One group consisted of 40 normal college-aged subjects. The authors found enhanced zation procedures on restoring proprioception following surgery. Thirty subjects internal tension. and the third group included Lephart and Fu2 defined neuromuscular control as the uncon- 20 subjects who underwent surgical reconstruction for shoulder scious efferent response to an afferent signal concerning instability. Lephart et al36 found no significant ­difference in the oper. tion of the supraspinatus and biceps muscle. proprioception at or near the end range of external rotation. Subjects with MDI exhibited significantly greater hand ­following an open approach with detachment of the subscapu- position error than did control subjects without instability. Additionally. with MDI. anterior instability and monitored them via indwelling EMG tive ability was observed when moving from 75° of external muscular activation patterns. However. despite a small sample size.

The con- ­glenohumeral joint instability. They determined that loss of muscle receptor efficiency as and flexion. The authors concluded that after fatigue ensues. Kronberg et  al50 used intramuscular electrodes to ­ etermined by the percent decrement in work output measured d compare shoulder muscle activity in patients with generalized from pretraining to posttraining conditions on an isokinetic joint laxity and normal control subjects. methods for determining the threshold for detection of movement were similar. but no subjects with increased glenohumeral joint laxity.28. ception after injection. highly trained the injection of lidocaine in either location and proposed that male recruits in the Special Forces division of the Navy. C H A P T E R 2 4    Pro p r i o c e p t i o n a n d N e u ro m u s c u l a r C o n t ro l 533 Finally. Ludewig and et  al. San Diego. continuous. research paradigm is of particular interest because insertion of a trol mechanism also resulted in abnormal scapular posturing total knee joint prosthesis results in removal of most joint recep- consisting of decreased upward rotation with elevation. uninjured subjects. but angular Effects of Rotator Cuff Dysfunction on replications were performed with subjects in the standing Neuromuscular Control in the Shoulder weight-bearing position instead of the seated open kinetic chain Research similar to that discussed in the preceding section in (OKC) protocol used in the study of Skinner et al. Furthermore. values muscular activity was measured during internal rotation in the on angular replication tests are significantly decreased. normal. They found no adverse effects from knee angle reproduction in a group of healthy. 26 of whom had tion in male subjects after the three different fatigue protocols. Similar replication after the continuous and interval programs. increases in upper Finally. but not to subjects in the previously discussed research studies on with the ramp protocol for joint angular replication. older (50 to 70 years of age) subjects. and interval training) at a percentage of their Vo2max. . however. No differences in joint position sense netic measurement of knee extension and flexion. Subjects ­compensatory extracapsular feedback ensured intact proprio- underwent an interval running program followed by isoki. cols (ramp. This altered neuromuscular con. Both groups of investigators found no anterior tipping. required by the dynamic stabilizers in subjects with joint laxity The authors concluded that the dual role of afferent input by the and glenohumeral joint instability. Increased ­subscapularis device. CA. and increased medial rotation. Weisman et  al85 found increased laxity in the role of joint and muscular afferents. which essentially leads to increased ­laxity and neuromuscular control in the knee joint. clusions drawn by the authors of this study were that anatomic ment demonstrated a decrease in serratus anterior muscle gender differences possibly account for the variation in proprio- ­activation during active elevation of the arm in comparison to ception in response to fatigue. studies when digital nerves containing both joint and cutaneous affer- in the literature2.84 Skinner et al28 found an increase in laxity of The role of specific afferent receptors in the human body has the ACL measured with a KT1000* arthrometer after a fatigue been examined with different methods to better understand protocol.87 have shown a decrease in the sensitivity ents were blocked by local anesthesia. ous because of the possibility of sustaining injuries under these Zuckerman et  al88 injected lidocaine into the subacromial conditions when higher-level activities are performed. proprioception is analyzed. These groups of authors and coordinated muscular control of the ­scapulothoracic and both concluded that their research again points to the ­important ­glenohumeral joints. . This with unilateral impingement. The results which muscular activation patterns in patients with rotator cuff of the study of Lattanzio et al25 were similar to those of Skinner impingement were measured has been published. Fatigue was and TTDPM testing were noted between the dominant and ­nondominant extremity.86. listed later in this chapter have these research-based rationales Lattanzio et al25 conducted a study involving healthy male and can directly enhance neuromuscular control of the shoulder and female subjects performing three different cycling proto- complex. Effects of fatigue on lower Effects of muscular fatigue on extremity proprioception upper extremity proprioception Muscle fatigue reduces the force-generating capacity of the ­neuromuscular system. These studies clearly show the increased demand a result of fatigue played a key role in angular replication errors. with ­statistically significant decrements in joint replica- Cook51 studied 52 male construction workers. Application of the resistive receptors in the contractile and noncontractile elements of the exercise progressions and use of the kinetic chain exercise series knee is important for proprioceptive sense. those with unilateral impinge. role that muscle-based mechanoreceptors play in knee joint proprioception. In this study. Skinner space and glenohumeral joint to assess proprioception in young et al28 studied the effects of fatigue on joint position sense and and old male subjects. Similarly. as well as significant changes were noted in the threshold of movement increased middle and anterior deltoid activity during abduction sense.51 Additionally. unilateral shoulder impingement and 26 had no ­symptoms of Female ­subjects similarly showed significant differences in joint impingement or other pathologic shoulder condition. Provins62 reported the medial collateral ligament in athletes at a university after a decrease in the ability to detect passive motion of the finger ­participation in various sporting activities. These scapular significant loss of proprioception in the extremity that under- modifications are thought to be contributing factors to rotator went total knee replacement in comparison to the contralateral cuff impingement and demonstrate the importance of optimal extremity 6 months postoperatively. increased tors in the human knee. Barrack et al30 and Barrett et al73 studied the effects and lower trapezius muscle activity were found in the subjects of total knee replacement on knee joint proprioception. The consequences types of afferent feedback may be equally important when joint of decreased proprioceptive sense from fatigue can be deleteri. He concluded that both of muscle receptors under fatigue conditions. a decline in proprioception with age was measured in the young (20 to 30 years of age) and *Available from Medmetric Corporation.

and bradykinin. ­proprioception after muscular fatigue has led researchers to emphasize the importance of the muscle-based receptors. of the body for both injury prevention and rehabilitation. Tripp et al95 demonstrated that functional fatigue The results showed significant improvements in anterior tibialis affects the acuity of the entire upper extremity. competition. fatigue of the glenohumeral joint internal and external rotators. latency times in both the trained and untrained control ankles. ing group sustaining fewer lesions of the ACL than the control Additional research by Myers et al92 has demonstrated that group who performed traditional strengthening exercises. the subjects in decreased neuromuscular control.94 found that capsuloligamentous injury to the shoulder ing on a disk with the involved leg in an 8-week training program.100 600 semiprofessional normal shoulders. subjects' detection of passive motion was to desensitize the muscle spindle threshold and thereby lead to marred or decreased by 171% for internal rotation and 179% for ­decrements in both joint position sense and neuromuscular external rotation. potassium chloride. No significant difference in shoulder joint angular replication was found between the dominant and nondominant extremi. patients with anterior glenohumeral instability have altera. Osborne et  al101 studied the effects of ankle disk training tions in muscle activation. The results suggest that performed a multistation proprioceptive exercise ­program scapular tape affects the activity of the shoulder muscles and ulti. The magnitude of proprioceptive feedback was coactivation in 30 subjects with chronic ankle sprains. clinicians were tested for onset latencies with surface EMG electrodes need to address the mechanical instability but also implement on the muscles of the ankle influencing stability to measure the functional rehabilitation interventions to return an athlete to motor response to a simulated inversion sprain on a platform. This topic is covered in detail angular replication protocol after isokinetically induced muscular in the application section of this chapter. high-level disk. that included 12 stations with various devices once weekly mately that these effects are related to the ­proprioceptive feedback for 6 weeks. The results showed significant differences between the bilaterally assessed unilateral CKC stability-type test measuring experimental and control groups. minitrampoline. Intramuscular concentrations of nondominant extremities. clinicians can implement in eight individuals who sustained an inversion ankle sprain therapeutic exercises that address the suppressed muscles as within the preceding years and who had not received any ­formal the scientific foundation of a rehabilitation program. A similar study by Eils and Dieter102 showed significant der proprioception and EMG activity in several muscles of the improvements in muscle reaction times and patterns of ­muscle shoulder complex. The results of their study showed that subjects injury prevention and improvement in neuromuscular stabili- had a decrement in discrimination of movement velocity after zation through proprioceptive training. Carpenter et al found ­control. Fatigue of the internal and determine the frequency of ACL injury in players who under- external rotators of the shoulder decreased subjects' accuracy in went a progressive proprioceptive training program and in a detecting both midrange and end-range absolute angular error control group who performed only traditional strengthening but did not have a negative effect on neuromuscular control in a exercises. The subjects performed 15 minutes of daily train- et  al93. The frequency of once per week and the types of provided by the tape. A review of research in a hard isokinetic horizontal flexion/extension exercise fatigue this section will provide the reader with important references protocol versus a light exercise condition. After an isoki. Muscle fatigue is thought netic fatigue protocol. Djupsjobacka et  al97-99 reported alterations in muscle increased sensitivity when moving into external rotation versus spindle output in the presence of lactic acid. The exercises included a Biodex scapular taping because it is a very popular ­technique with many balance system.534 Physical Rehabilitation of the Injured Athlete Several studies have been performed on the human shoulder of active joint angular positioning tests has been reported to stim- to investigate the effect of muscular fatigue on various indices ulate both joint and muscle mechanoreceptors and is considered of joint proprioception and neuromuscular control.2. The subjects performing the exercises showed ­significant research support for this technique is limited at this time. The ­subjects ­significantly lower in the taping conditions. In preexercise testing.91 et al89 tested subjects using a TTDPM test with the shoulder The exact mechanism by which muscle-based proprioception is in 90° of abduction and 90° of external rotation. and ankle anecdotal reports demonstrating effectiveness. Consequently. Significant decreases in accuracy were noted after muscular on proprioception fatigue in both the active and passive joint angular replication tests. Carpenter to be a more functional assessment of the afferent pathways. effect of muscular fatigue on joint proprioception may play a This consistent relationship has provided further rationale and role in injury and decrease athletic performance. ­improvement over the control group in position sense and The consistent finding in these studies of a decrement in reported subjective improvements in functional stability. internal rotation but no difference between the dominant and arachidonic acid. Further research will continue to be needed exercises were chosen for their ability to be implemented easily to better understand and demonstrate the efficacy of shoulder and into a rehabilitation program.89 These authors concluded that the these substances are altered during muscular exertion and fatigue. Pederson et  al90 tested the ability of healthy subjects to in the lower extremity discriminate movement velocity of the glenohumeral joint in the Some studies in the literature have investigated the notion of transverse plane. The use *Available from Biodex.* inversion boards. A concentric isokinetic internal and external and amateur soccer players were monitored for three ­seasons to rotation fatigue protocol was used. decreases proprioceptive input to the CNS and thereby results After completion of the 8-week training program. NY. Effects of training ties. affected is not entirely clear or known. muscular control test to examine the effects of muscle fatigue in In a prospective study by Cerulli et al. Shirley. support for improvement in muscular endurance of the dynamic Voight et al41 tested subjects with an active and passive joint stabilizers of the glenohumeral joint. that support the use of proprioceptive training of the lower part Myers et al91 used an active angular replication test and neuro. with the proprioception train- postural sway velocity.15. however. Therefore. Myers ­rehabilitation. . Lin et al96 investigated the effects of scapular taping on shoul.

One Neuromuscular training for strategy for dynamic stabilization is cocontraction of opposing rehabilitation and prevention muscle groups to essentially stabilize the knee in a rigid pos- ture. and the ­effectiveness of neuromuscular training in rehabilitating amount of force occurring at the joint. whereas deleterious . in patients with chronic/functional extremity proprioception ankle instability. cies and the Lyshom rating scale for measuring functional and larger effect sizes were demonstrated for training programs outcomes. in patients with ACL injuries. has been discussed.108-111 One very important aspect inherent in most lower extremity and neuromuscular control proprioceptive training programs is inclusion of the entire lower Lower extremity injuries occur often in competitive and recre- extremity kinetic chain in the exercise. risk for lower limb injuries. decreases causes overload on the static joint restraints. task. review. numerous ­neuromuscular control. Hübscher et  al117 performed a systematic They use the term copers for individuals who successfully per- review of the use of neuromuscular training for rehabilitation form varied high-level activities without experiencing functional of sports injuries. These injuries are sometimes caused by physical exercises in the literature described herein use multiple joint. interventions were more effective in athletes with a history of tion program consisted of progressive exercises using rocker sports injuries than in those without. is essential for the entire lower muscular stabilization. the ways in which recurrent injuries to an existing training by itself is not enough. Consequently. agility. This strategy may be successful for simple tasks. Multiintervention training was effective in reducing the ciencies who performed traditional lower extremity strength. no studies demonstrated muscular stabilization. exercise ­rehabilitation along with perturbation training.1. but with of sports injuries higher-level activities such as sports. C H A P T E R 2 4    Pro p r i o c e p t i o n a n d N e u ro m u s c u l a r C o n t ro l 535 Friden et al31 conducted a study in subjects with ACL defi. Balance training alone decreased ening exercises and in subjects who performed ­traditional the ­incidence of ankle sprains in athletes. to prevent injury caused which these injuries can be prevented and. designed a rehabilitation program based on the premise of bilitation. but only ­instability. Injuries that throughout the lower extremity for postural control mechanisms do not involve another person occur when the player or indi- in rehabilitation and prevention of injury. Thirty-two articles were identified. once an individual by a fatigue-induced decline in proprioception. Additionally.118 They completed a systematic review of balance training jective reports of stability during completion of higher-level for neuromuscular control and enhancement of performance. the muscular strategies used for joint seven ­methodically well conducted studies were included in the ­stability allow normal joint movement. including perturbation training. activities than did the traditional training group. Beard et al76 Twenty RCTs met the inclusion criteria. using vidual attempts to suddenly change the rate of speed or course absolute angular error measurements. contact with another individual. Interestingly. sports injuries in the shoulder. It is controversial whether balance training ­perturbation training had improved functional outcomes in was effective in improving jumping performance.119 extremity kinetic chain. only for lower body ­injuries. effective in improving postural sway and functional balance. the ­perturbation ing to improve neuromuscular control was performed by Zech group was found to have significantly greater ­success with sub. but they usually result from a training positions and CKC positioning environments that noncontact injury in which the external forces in the environ- allow the entire lower extremity kinetic chain to be included. A force feedback mechanism in which stability is achieved Fifteen studies met the inclusion criteria and demonstrated through varied patterns of muscle recruitment.100 Some of the Research112-114 has emphasized the importance of examining more common injuries involve damage to the ligamentous and the entire kinematic chain from the trunk and hip musculature cartilaginous components in the knee and ankle. ­compromised system can be prevented through dynamic neuro- including central programming. Snyder-Mackler et  al1. Balance training was conducted a similar study but used hamstring reflex laten. and has effects on different mechanisms in the have received recent attention in the literature are the degree to proprioceptive pathway. Miura et al115 found that of direction or when an obstacle in the external environment local and general fatigue affects knee proprioception. Most proprioceptive ational sports. However. with advancement to the next phase the concept of inadequate rehabilitation following the initial after ­successful completion of the task without evidence of sports injury. They concluded that the group that underwent of longer duration. this systematic review showed much less scientific achieving dynamic muscular stabilization during normal and ­support for the use of ­neuromuscular control exercises in the higher-level skills through neuromuscular perturbation ­training.2 This ­theory functi­onality and decreasing the incidence of recurrence after ­acknowledges that different patterns of movement require ­varied ankle and knee injuries. studies have evaluated the ­effectiveness of neuromuscular train- ing programs. ment exceed the internal forces of the body. neuromuscular training is achieved through coordinated muscle activation in response to controlled perturbation forces imparted on the joint. includ. but neuromuscular training. At the University of Delaware. local muscle is injured. This probably relates to boards and roller boards. depending on the direction. Furthermore. speed. In copers.52. and knee stability while performing ADLs. et al. upper ­extremity. techniques to improve lower ing perturbation training. For a patient with ACL deficiency. depending on the the effectiveness of neuromuscular training in increasing situational needs of the task. The questions that muscular power.120 Though used ­inherently and recommended for shoulder reha. After the training program. Additional research on the use of balance train- instability or pain.103-107 Numerous ­studies have also evaluated Clinical application: the effectiveness of neuromuscular training programs. The perturba. stabilization is achieved Zech et  al116 performed a systematic review of the use of through selective motor recruitment that is dependent on the ­neuromuscular training for rehabilitation of sports injuries.

lower extremity proprioceptive The program is designed to identify individuals who would be successful rehabilitation candidates through a screening ­process. increased effusion or pain). The joint stability during lower extremity weight-bearing tasks is drills are initially performed at 50% and progress to 100% in noncopers. athletes are required to pass a ­posttreatment using the guidelines of Fitzgerald et al to implement a neuro. and frontal planes) in a In a study by Snyder-Mackler et al. muscular control results from damage to the mechanoreceptors ing joint effusion. and direction of force. and progression should not exceed the rate . The program Several considerations are important when a rehabilitation is progressive in nature and designed for specificity of sport or program is designed to restore proprioception and dynamic activity. such as ambulation. Examples of some of the agility drills are side strategy is used with all tasks. Another advantage ­subjected to perturbation forces on all three devices in slow of CKC exercises is the simultaneous movement of multiple predictable directions with the use of verbal cues as necessary joints. an advanced role in producing smooth. ­successful program.2 in an attempt to restore functional stability during higher-level sporting activities. and cutting maneuvers at 45° and 90° ment strategies and functional instability.1 When these goals have been met. middle phase. shuttle running.536 Physical Rehabilitation of the Injured Athlete compressive and shear forces at the joint are minimized. which results in inefficient move. In selecting exercises for training. ­infrequent Regardless of whether surgery or conservative care is chosen to episodes of instability (<1). and CKC movements occur when the distal segment is include the use of rocker boards. use a early phase. Initially. most importantly. The advantage of OKC exercises is their ability the ­application of progressive variable perturbation forces in to isolate targeted muscle groups for strengthening.1. most functional activities. specific drills while the individual is wearing a functional knee In the early stages of rehabilitation. speed. training The criteria include isolated injury to the ACL. and a passing percentage on two subjective rating scales rehabilitation is crucial for reestablishing neuromuscular control for functional knee impairment. are emphasized with the use of agility drills. a cocontraction stiffening the later stages. and balance and. patients then perform inadequate coping mechanism. the development of an brace. patient response (i. Before returning to full athletic The faculty at the University of Delaware designed a ­program ­competition. a passing score on functional hop restore stability and function to a degenerative or unstable joint. transverse. All three phases space. certain criteria had to be met to ensure a successful outcome of Guidelines for implementing the training.. In the group of noncopers. a focus on ­restoring The program consists of 10 treatment sessions at a frequency function to the individual should remain at the forefront. With no evidence of instability. sport-specific movements exercise program should identify deficits in ROM. shuffles. ­stability. along with the implementation of light sport. coordinated movement. The loss of neuro- is initiated. which requires cocontraction of opposing muscle groups for the onset and direction of the forces. In the last phase of treatment. a combination of OKC and CKC exercises have as a guideline. Furthermore.2 of the sporting environment. Progression of the program is based on the symptomatic ­performing daily or sporting activities. sessions 5 to 7. progressive deterioration of joint sport-specific activities while undergoing perturbations on roller surfaces and capsuloligamentous restraints occurs as a result of boards and platforms to simulate the competitive demands excessive shear and compressive forces at the joint. which is used Traditionally. training and requires successful adaptation of strategies in the In fact. ­multiple directions (sagittal. The clinical implication of this phase thus involves muscle groups. Initially. the direction to ­control joint movement.e. amplitude. strength. sessions 1 to in strength. to more closely resemble the functional demands placed on the In the early phase of perturbation training. been used in rehabilitation. OKC exercises have been defined ful motor strategies to counteract the perturbation force. In selection of individuals for the program. the early focus of rehabilitation is on decreas. and increasing quadriceps within the capsuloligamentous structures of the joint and from and hamstring strength to allow stabilization through muscle interruption of the afferent sensory pathways that play a crucial recruitment. with this angles.2 neuromuscular training program can be initiated. roller boards. tests. patients are lower extremity during a variety of activities. restoring ROM. and the ability of the patient to perform success. The begins in straight planes and then moves to variable-direction term given to individuals who are unsuccessful in maintaining drills such as cutting and changing direction on command. sessions 8 to the ­individual's ability to meet the demands of stability while 10). which as movements in which the distal segment is free to move in includes no episodes of falling or instability. and therefore both should be incorporated in the design of a are advanced. ROM. intensity. including ­combination of both OKC and CKC muscle activation patterns. on 4. CKC exercises can also reduce shear of the applied forces is in the anterior/posterior and medial/ forces across joint surfaces as a result of the stability of joint- lateral directions with progression to diagonal and rotational through-joint compression forces and cocontraction of opposing planes. ACL screening involving measures similar to those used during muscular training program for patients with ACL deficiency ­prescreening for acceptance into the program.122 isolated OKC quadri- controlled manner to retrain the nervous system in a number of ceps strengthening was found to be superior to CKC exercises ­applications or situational needs while avoiding the use of rigid in improving quadriceps function in patients after ACL surgery cocontraction strategies. Variations in the parameters of training. training and joint effusion. predictability. of two to three times per week and is progressive in nature with Exercises chosen should then focus on an individual's ­deficits three phases of implementation (early phase.121 Emphasis on the use with an introduction to sport-specific agility drills in the middle of CKC exercises has predominated because they are thought to later stages. and late phase.2 because the involvement of other muscle groups in performing The middle phase of training continues with perturbation the CKC exercises did not isolate the quadriceps as effectively. Before a stabilization ­program or dynamic stability in a compromised joint. and platforms fixed or meets considerable resistance.

4 Single-leg balance on Biodex balance system. 24-3). Proprioceptive training in this stage may involve two-legged stance exercises on an unstable surface such as the Biodex stability balance system (Fig. 24-8). Any return to functional or sport-specific activity. active assisted. C H A P T E R 2 4    Pro p r i o c e p t i o n a n d N e u ro m u s c u l a r C o n t ro l 537 of ­natural healing or limitations in the involved structures. with difficulty F i gure 24. Other exercises that are beneficial for proprioception involve the use of rocker boards for directional perturbations to activate selective muscle recruitment patterns in a variety of planes of movement. These patterns can be performed on balance pads or exercise mats to enhance F i g u re  2 4 .2 Performing appropriate ­muscular response toward the final stages of ROM exercises on an immobilized joint and weight shifting early after an ankle sprain or surgery on the ACL are examples of early forms of proprioception training. 24-6 and 24-7). If ­stabilization training has yielded the sensory input to improve neural mechanisms. initiation of resistance exercises for building muscular strength and endurance will enable sufficient muscle recruitment patterns for the dynamic stabilization needed for advanced forms of training. 24-4) and single-leg stance with partial squatting on the machine with the benefit of a visual cursor to assess weight distribution so that compensatory patterns can be avoided. In the later number of exercises will elicit proprioception training based on stages of training. while the patient throws and catches the ball. 24-5).3 Incorporating functional movements such as the being increased by manual perturbations of the rocker board squat on the Biodex balance system. exercise should focus on restoring and the fact that deformation of the joint mechanoreceptors occurs ­ideally ­optimizing the adaptive neuromuscular response to with active. and passive movements and ­provides situational needs. These training techniques can be advanced to sport- specific activities such as tossing a ball against a trampoline while manual perturbations are applied to the board (Fig.5 Chest pass with a weighted ball incorporates plyometric exercises with proprioceptive exercise. The exercise progression can include single-leg stance (Fig. The goal of proprioceptive training is to reestablish stabil- ity or dynamic neuromuscular control and should ­emphasize F i g u re  2 4 . close his eyes. . Movement patterns such as a straight plane or multidirectional lunge are also useful for selective motor recruitment in functional or sport-related activities (Figs. which can be advanced to a functional squatting movement pattern. motor control through maintenance of balance while ­performing The level of difficulty is progressed by decreasing the stability initially slow and then more rapid movements beyond the base of the platform or removing visual cues by having the patient of support (Fig. When sufficient healing has taken place in the subacute stages of recovery.

538 Physical Rehabilitation of the Injured Athlete Fig ure  24. The approximation of the joint specific drills involving full body movement patterns on a yielding surfaces and the multiple joint loading inherent in CKC exer- surface (Figs. progressively quicker changes in direction while pivoting on the involved extremity. The presence of muscu- *Available from Fitter International. Agility drills. Closed Kinetic Chain (Joint Approximation) Exercises r­ ehabilitation. upper extremity exercises. joint oscilla- tion exercises. more advanced exercises incorporating sport. torso while a weighted ball is held outside the base of support for the integration of upper and lower extremity movement patterns. Alberta. postoperative interventions.8 Single-leg balance on Thera-Band balance pads lower extremity proprioception while the patient performs while opposite extremity movements are resisted beyond the lunges on Thera-Band balance pads. Canada. lar cocontraction around the human shoulder is particularly . Exercises that produce approximation of the glenohumeral joint specific drills should be performed. Calgary. and techniques to improve muscular endurance of the rotator cuff and scapular Figure  24-7 A lunge being performed with rotation of the musculature.123 and ­produce ­muscular cocontraction. including the use of CKC and joint approximation exercises. base of support in functional planes. ­including cises are reported to increase mechanoreceptor stimulation2. Clinical application: techniques to improve proprioception and neuromuscular control of the upper extremity with specific reference to the shoulder Application of the basic science information on proprioception and neuromuscular control of the shoulder to clinical practice allows clinicians to most appropriately provide stability to the glenohumeral joint and optimize shoulder girdle arthrokine- matics. Exercises on a Fitter and are characterized by a fixed distal aspect of the extrem- board* or slide board can be performed to challenge the patient ity are typically referred to as joint approximation or CKC with higher-velocity movements while performing sport. Several areas are covered in this section. should be incorporated in the final stages of rehabilitation for athletes who perform such maneu- vers in the competitive arena.6 Combination of proximal pelvic control with F i g u re 2 4 .  24-9 and 24-10).

These exercises were the push-up with a plus the rocker board or biomechanical ankle platform system with and the press-up. Kibler et  al125 published EMG research on a series of very sis of the ­scapular muscles during traditional rehabilitation low level CKC exercises for the upper extremity. Reaching low. C H A P T E R 2 4    Pro p r i o c e p t i o n a n d N e u ro m u s c u l a r C o n t ro l 539 A B F i gure  24. including ­exercises. beneficial because of the important role that the musculature minor. Moesley et  al46 published a comprehensive analy. This indicates that high high levels of ­muscular ­activity in the trapezius or ­serratus degrees of coactivation and cocontraction are inherent in this but instead produced high activation levels in the pectoralis type of exercise. B. exercise. and scapular of a modified push-up and produces very high levels of ­serratus muscles. deltoid. The press-up exercise did not elicit all these muscles during these activities.10 Dynamic balance on a Fitter board with sport-specific drills such as the ground stroke in tennis. A B F i gure  24. A.9 Dynamic balance on a slide board incorporating upper body movements with resistance in proprioceptive neuromuscular facilitation patterns. A. Muscle activation levels during these exer- ­protraction of the scapula during the end of the ascent phase cises were very low in the rotator cuff. Decker et  al126 confirmed the importance of the plus surrounding the scapulothoracic joint plays in stabilizing and ­position for serratus anterior activation and concluded that controlling movement of the shoulder. Two CKC upper extremity exercises were included weight-bearing upper extremity weight shifts and exercises on in their analysis. B. Reaching high. however. . Forehand.124. Backhand. The push-up with a plus includes maximal the upper extremity.125 exercises ­emphasizing scapular upward rotation and accentu- Significantly less EMG research has been published on ated ­protraction produce the highest levels of muscular activity upper extremity CKC exercise than on upper extremity OKC in the serratus anterior. low levels of activity were present in virtually anterior muscle activity.

540 Physical Rehabilitation of the Injured Athlete Research has demonstrated the important role that joint compression plays in glenohumeral joint CKC exercise. Application of these concepts in patients with rotator cuff dysfunction and glenohumeral joint instability is pictured in Figures 24-11 to 24-15. It is impera- tive that the clinician realize the osseous relationship of the glenohumeral joint. and TheraTubing‡ can provide additional emphasis on particular muscle groups induced via the oscillation and stretch imparted during the during these exercises.* BOING (body oscillation integrates neuromuscular gain).127. scapular slide testing. loads such as light weights.128 Understanding these important relation- ships will guide the clinician in shoulder positioning and ROM selection during joint approximation exercises with the arm F i g u re  2 4 . and 50-lb com- pressive force to cadaveric shoulder specimens. respectively. MA. racic positions inherent in overhead sport-specific movement .. Inc. Appliances such as the Bodyblade. manual resistance.† and Figure  24-12 Quadruped rhythmic stabilization exercise resistance bar‡ have facilitated the use of joint oscillation exer. Joint Oscillation Exercises Rehabilitative exercises involving joint oscillation have increased in popularity in recent years. This study shows the potential benefit of a compressive load in the provision of glenohumeral joint stability and points out the important application that CKC exercises may have in enhancement of neuromuscular control in patients with glenohumeral joint instability. Warner et al37 studied the effects of applying a 5-. in addition the position of the hand contacts by progressing further toward to traditional OKC shoulder rehabilitation exercises in patients the patient's hand increases the intensity of the exercise. Figures  24-16 to 24-19 show exercises exercise.124 Sets of exercises lasting up to 30 or 45 seconds are desired in the later stages of rehabilitation. Guidelines for the time-based sets of exercise depend on the patient.128 This anterior version of the scapula is aligned with 30° of retrotorsion of the humeral head.1 1 Closed chain wall scapular-plane rhythmic placed in the scapular plane. OH. CA. with glenohumeral joint instability. Playa Del Rey. Akron. The ability of these time-based exercises to promote using oscillatory devices or manual contact that require the rota. 25-. Application of CKC exercises clinically is facilitated by a thorough review of glenohumeral joint anatomy.4 mm at 45° of abduction. Lephart or small exercise ball in varying degrees of abduction in the et al86 used five neuromuscular control exercises that emphasized scapular plane.. varying muscular cocontraction in one experimental group. joint approximation and compression. Minneapolis. They found ­significant improvements in kinesthetic ability. and the patient remaining as stable as possible over the ball. Careful monitoring of the medial and inferior borders of the scapula is important to ensure proper neuromus- cular control and avoid the development of undesired motor patterning.5 to 1. The patient's arm is placed on a medicine ball Research on CKC upper extremity training is limited. to more closely approximate the glenohumeral and scapulotho- ‡ Available from Hygenic Corp. The clinician performs rhythmic stabilization with joint positioning. and optimal bony congruity occurs with the arm placed in the scapular plane. scapular-plane position is followed as rehabilitation progresses † Available from OPTP.128 stabilization.129 Progression to the external rotation oscillation exercise in Figure 24-17 by using the 90° abducted *Available from Hymanson. and isokinetically documented protraction and ­retraction strength in the group that performed these ­neuromuscular ­control ­exercises during rehabilitation. The human glenoid is oriented slightly ­inferiorly with the arm held at the side and tilted anteriorly 30° from the coronal plane of the body. with the ability of the patient to maintain the desired scapulothoracic stabilization being a ­governing factor. local muscular endurance is increased by manipulation of set tor cuff and scapular musculature to respond to external cues duration and rest cycles. progression with instruction to maintain scapular protraction or cises. These amounts of compression resulted in decreases in anterior humeral head translation in neutral elevation from 11 to 2 mm with 5 and 25 lb of compressive force and from 21. Rapid oscillation of these devices coupled with external the "plus" position during repeated multidirectional challenges.

13 Tripod rhythmic stabilization technique with the involved extremity in the closed chain position and maintenance of the "plus" position to increase activation of Figure  24-15 High-level unilateral scapular stabilization the serratus anterior muscle. elicited the highest levels of infraspinatus muscle activation. on the upper extremity to increase the challenge of the exercise. The clinician alternately provides exercise with the patient in a closed chain unilateral scapular- multidirectional challenges to the non–weight-bearing limb as plane stance position with rhythmic stabilization superimposed the patient attempts to isometrically hold the pictured position. ­glenohumeral joint in a neutral abduction/adduction position for internal and external rotation. Care is taken with this exercise to protect the shoulder complex by descending only approximately one half the distance of a standard push-up and then maximally protracting the scap- ula on the ascent phase to increase activity of the serratus ante- rior muscle. C H A P T E R 2 4    Pro p r i o c e p t i o n a n d N e u ro m u s c u l a r C o n t ro l 541 F i gure  24. increase the challenge to the patient by sliding the patient in a cephalad direction.130 Figure 24-20 shows the push-up with a plus exer- cise. F i gure  24.46 Holt et  al131 investigated four different positions of exer- cise with the Bodyblade and its effect on infraspinatus muscle F i g u re  2 4 . (2) side-lying position with The results of a repeated-measures analysis of variance showed the glenohumeral joint in neutral abduction/adduction for that the side-lying internal/external rotation oscillatory pattern internal and external rotation (see Fig.14 Unilateral prone exercise ball stabilization Figure 24-16 Supine modified rhythmic stabilization technique exercise.131 nohumeral joint scapular-plane elevation with stabilization. use of oscillatory-type exercise. The degree of support is progressively decreased to performed in 90° of shoulder flexion with scapular protraction.  24-17). patterns. These four positions included (1) standing with the exercise using the Bodyblade. . (3) 90° of gle. and Further research such as this is needed to guide clinicians in the (4) 90° of scapular-plane elevation with the unsupported arm.1 7 Side-lying glenohumeral rotational oscillation activity.

age decrease the role of the deltoid in actively holding the exercising is a moderator of the response to vibration exercise for power. Vertical platforms bar for oscillation. B F i g u re  2 4 . extremity in the 90° position. depending on the intended goal of muscular activation. However.19 "Statue of Liberty" external rotation oscillation teria. It appears that vertical platforms produce chronic adaptations whereas oscillating platforms have a more ­profound effect on acute responses to the exercises. Ending position of movement. Many factors influence the training responses and effect sizes demonstrated by the studies. Vibration Training on Performance Muscular Endurance Exercise One of the fastest growing areas focusing on proprioceptive and neuromuscular control deals with the effects of vibration train. Scapular position can be altered in this exercise. The results of the vibration exercise can be used by exercise professionals to enhance muscular strength based on the aforementioned cri- Fig ure 24. These studies show that gender. training ­status. Starting position. exercise ­protocol. rotator cuff and scapular musculature would have a direct ysis of the effects of vibration training on muscle strength.542 Physical Rehabilitation of the Injured Athlete A Fig ure  24.2 0 Push-up with a plus and maximal protraction of the scapula to elicit higher levels of serratus anterior activity. A. Marin and Rhea132 also completed a metaanalysis of the exercise using Thera-band elastic resistance and a resistance effects of vibration training on muscle power. Thirty-one studies met the inclusion criteria. Marin and Rhea132 performed a metaanal. A scapular-plane position in 90° of elevation were more effective than oscillating platforms in producing a is used while the contralateral extremity provides support to larger treatment effect for chronic adaptations.18 Biped closed kinetic chain exercise using the Bodyblade to provide joint oscillation in the non–weight- bearing upper extremity and a medicine ball to decrease surface stability of the closed chain upper extremity. B. and type of vibration platform all ­influence the outcomes. effect on improving performance and enhancing proprioception . The results of the vibration exercise can be used by exercise ­professionals to enhance muscular power in selected subjects and specific protocols. Exercises to increase endurance and fatigue resistance of the ing on performance.

and local muscular endurance provides an important rationale for the inclusion of copious applications. showed that the internal rotators fatigued to when designing a comprehensive training or rehabilitation a level of only 83%.34 Repeated attempts to l Feedforward and feedback mechanisms are responsible for enhance muscular endurance based on these studies.20. l To maintain balance and postural control.15. bilitation programs using the scientific concepts reviewed in this tors in patients with rotator cuff dysfunction or glenohumeral chapter. joint approximation sue healing allow.134 located in the joint capsule. The external rotators. however. ­application of ­thermal energy to produce capsular shortening.136 One additional study performed by Ellenbecker and Neuromuscular control is a result of the efferent response Roetert121 specifically evaluated the relative muscular fatigue to the afferent signals generated through the sensory system. kinesthesia. Early ­application of the joint approxima- or closed chain. Exercises using sets of 15 to 20 repetitions ­passive angular joint repositioning in available ROM with and 15 to 20 repetition maximum loading schemes are geared the elimination of visual cues. and approximation. and somatosensory systems.129 stabilization. mus- The use of treatment techniques to enhance ­proprioception cle. possible. joint instability. as on earlier literature citations linking muscular fatigue of the ­glenohumeral rotators to decrements in proprioception. obstacles in an often fast-paced arena. the proprioceptive pathways are injured or disrupted. II. tralateral extremity position or repeated movements can tice in orthopedic and sports physical therapy usually includes be done passively initially and then be progressed to active exercises with this type of prescription or recommendation. the clinician should consider the effects of fatigue second half of the testing protocol with the work performed and disuse on proprioception and also their potential impact in the first half. are clinically indicated. Methods proposed for addressing glenohumeral monly present in noncontractile capsular and ligamentous joint instability include primarily capsular plication and the structures in human joints: types I. When junior tennis players underwent isokinetic fatigue testing con. however. II. plyometric. tion exercises and rhythmic stabilization exercises described ing of targeted muscles or muscle groups have clear benefits earlier in this chapter is also beneficial in the early progres- and research-oriented rationales as outlined in this chapter and sion after rotator cuff repair and open and arthroscopic other sources. fatigued program. we rely on sensory This study shows the important role that the rotator cuff plays information from the periphery. ­differences were found in active and passive angular ­reproduction Types I and II predominate in the glenohumeral joint. l Type I and II mechanoreceptors are the primary receptors which may acutely alter glenohumeral joint proprioception. The l The primary mechanisms for afferent feedback from the acute effects of ­thermal capsular shrinkage on glenohumeral muscle-tendon unit are the muscle spindle and the Golgi joint ­proprioception are not completely understood. ligaments. and skin. III. to a level of 69% over the 20 testing repetitions.129 Current prac. and neuromuscular control is indicated for the shoulder after l Four primary types of afferent mechanoreceptors are com- ­surgery. especially in the area of athletics in which ­overcoming The results showed significantly different fatigue responses resistance from opposing players is coupled with environmental between the internal and external rotators. They found significantly l More is known about proprioception in the lower extremity greater amounts of superiorly directed humeral head translation than in the upper extremity.57 angular joint position replication as patient status and tis- The use and integration of joint oscillation.54. Conclusion graphically as they elevated their shoulders before and after a series of rehabilitation exercises that produced substantial levels Introduction of muscular fatigue in the shoulder. III. whereas the glenohumeral joint appears ­shrinkage for glenohumeral joint instability. ­tendons. increasing the work duration and decreasing the rest periods in Early postoperative proprioceptive training consists of the exercise format. and isotonic and isokinetic train. which are dependent on the structure. Analysis of the rel.57. ­tendon organ. No significant to have all four types. Chen et  al133 demonstrated the effects of muscular fatigue on glenohumeral joint kinematics.54. of joint position sense 6 to 24 months postoperatively. of the rotator cuff with isokinetic testing. Myers et  al135 measured joint position sense. Seventy-two elite Proprioception plays a critical role in this feedback system. even in healthy trained subjects. the humeral head within the glenoid. not only sisting of 20 reciprocal concentric contractions of the internal inefficient motor responses but also greater risk for injury are and external rotators with 90° of glenohumeral joint abduction. and IV. . joint oscillation. which compares the work performed in the competition. All the exercises described in this this study shows that full return of proprioceptive function is ­chapter can be used to promote local muscular endurance by expected after rehabilitation.121 This study Use of the clinically oriented exercise progressions high- demonstrated a greater relative degree of muscular fatigue in lighted in this chapter. and l The lower extremity contains types I. in maintaining glenohumeral joint congruity and stabilizing vestibular. including techniques such as joint the external rotators. Afferent Mechanoreceptor Classification l Mechanoreceptors are sensory neurons or peripheral ­afferents Postoperative Applications located within joint capsular tissues. as well initiating a motor response in anticipation of a stimulus.60. documented radiographically with arm elevation after fatigue. as well as from our visual. provides the framework for objectively based reha- amounts of endurance-oriented training of the external rota. Subjects were studied radio. Replication of either the con- toward improving local muscular endurance. C H A P T E R 2 4    Pro p r i o c e p t i o n a n d N e u ro m u s c u l a r C o n t ro l 543 and neuromuscular control. In ­preparing athletes for ative fatigue ratio. and IV shoulder function in patients who underwent thermal ­capsular ­mechanoreceptors.

amplitude. functional movement patterns. speed. inant upper extremity movements. sists of moving along a continuum in which predictabil- ity. in the Lower Extremity l Active joint angular position replication tests primarily l It appears that proprioception can be enhanced through a involve the stimulation of both joint and muscle receptors proprioception training program. active assisted. force occurring at the joint. on the individu- sacrificing or retaining the posterior cruciate ligament are al's ability to meet the demands of stability while performing inconclusive. l Evaluation methods to assess closed chain function of the l Progression of proprioceptive and neuromuscular control upper extremity are limited. and Neuromuscular Control l Evidence suggests that the effect of muscular fatigue on joint Assessment of Proprioception proprioception may play a role in injury and decrease athletic and Neuromuscular Control performance. Techniques to Improve Proprioception and Neuromuscular Effects of Fatigue on Lower Extremity Control of the Upper Extremity Proprioception l The approximation of joint surfaces and the multiple joint l Muscle fatigue reduces the force-generating capacity of the loading inherent in closed kinetic chain exercises are reported neuromuscular system. speed. functional l Different patterns of movement require varied muscular sta- activities. l The consistent finding of a decrement in proprioception in the Upper Extremity after muscular fatigue has led researchers to emphasize the l Evidence suggests that athletes performing unilaterally dom. l Loss of capsuloligamentous stability causes propriocep. daily or sporting activities. and balance and.544 Physical Rehabilitation of the Injured Athlete Clinical Assessment of Proprioception l Evidence shows a decrease in the sensitivity of muscle recep- tors with fatigue. or volleyball. abnormal Proprioception and Neuromuscular Control muscular activity patterns during planar motion. which essentially leads to increased to increase mechanoreceptor stimulation and ­produce laxity in the knee joint. although the effects of ROM. intensity. muscular strength. return to functional or sport-specific activity. in improved proprioception scores. based on the fact that deformation of the joint mechanorecep- tors occurs with active. depending on the direction. and Injury modified. . on Lower Extremity Proprioception Guidelines for Implementing Lower l Age and injury result in diminished proprioception. which results in delayed muscle reaction dynamic stability. and direction of force are Effects of Aging. may have a proprioceptive Effects of Training on Proprioception deficit in the dominant arm that may interfere with optimal afferent feedback regarding joint position. the possibility of sustaining injuries under these conditions thetic awareness in the knee and glenohumeral joint are the when higher-level activities are performed. Those that have been used include training during the early and middle phases of training con- the push-up and the closed kinetic chain stability test. Instability. The consequences of decreased propriocep- in the Lower Extremity tive sense as a result of fatigue can be deleterious because of l The two primary tests measuring proprioception and kines. l Proprioceptive sense is decreased and muscle patterns are l Any number of exercises will elicit proprioceptive training altered after rupture of the anterior cruciate ligament. importance of the muscle-based receptors. l When one selects exercises for restoring proprioception and noreceptors. a focus on restoring function to the indi- latencies. Extremity Proprioceptive Training tive deficits because of inadequate activation of mecha. threshold to detection of passive motion for movement sense and reproduction of angular position for measuring joint Effects of Muscular Fatigue on position sense. most importantly. The exercises cho- l Some evidence suggests that total knee replacement results sen should then focus on an individual's deficits in strength. and passive movements Effects of Pathologic Shoulder Conditions on and provides sensory input to improve neural mechanisms. vidual should remain at the forefront. l Glenohumeral joint instability and rotator cuff dysfunction result in changes in neuromuscular control patterns. Proprioception and Neuromuscular Control l The goal of proprioceptive training is to reestablish stability or dynamic neuromuscular control and should emphasize a l Damage to the capsuloligamentous structures of the shoul. tennis. l Essentially no standard protocols have been established for Upper Extremity Proprioception measuring joint position sense or for joint replication tests. and closed kinetic chain upper bilization. and provide a thorough assessment of the afferent pathways of the human shoulder. such as those involved in baseball. der leads to deficits in proprioception. and amount of extremity tests. ­muscular cocontraction. Techniques to Improve Lower Extremity l Neuromuscular control of the shoulder can be assessed with electromyography.

J. J.. D. N.B. especially sensory innervation of the knee joint 52. (1996): The effects of muscle ­measurement techniques. Wyatt. B. T.... Williams. Sport Rehabil. C. J.... Voight. 55.M.N. 41:25. J.. (1996): Role of proprioception in pathoetiol- ogy of shoulder instability.. T. Beynnon. Athl. 209:181–192. execution of finger movements.. Bowen. Phys. Skinner.S.A. J. and Hoffman... and subacromial bursa. J. labrum. Brain.. 18. 31. Pincivero. R. fatigue on and the relationship of arm dominance to shoulder proprioception. and Gillquist. 50:684–687. J. Arch. Glousman.P. M. and rehabilitation of the shoulder complex.T. North Am.. D. Jobe. M. Voss. and Andrews. 24. and Cook. Orthop. and Lephart. Physiol.. Banks. (2000): Proprioception and Neuromuscular Control in 40. S. Smith. J.B. Shoulder Elbow Surg. (2000): Clinical application of closed kinetic ultrastructure. Champaign. and Buckley.B.. (1992): EMG analysis of the scapular muscles 10.. (1977): A quantitative analysis of sensa. 69:106–112.T...B. J. and Huston.L. J. K.. (2002): The effect of bracing on ­proprioception of knees with anterior cruciate ligament injury. McCormick. (1988): An electromyographic analysis of 14.. 23. Sport Rehabil.. (1986): Effect of fatigue on joint 62. H. Clin. 23:45–50. 3:77–86. J. 3:S45.A. B. et  al. Am. 3.. (1991): Electromyographic analysis of the 11. H. et al. and Arrigo.A. Riemann. R. (1906): The Integrative Action of the Nervous System. et al. and Ropper. unstable. Clin.. Jobe. Champaign. 44. L. R. program. J. Simon.P. Warner. Sport Rehabil..M.R. Barth.. Warner. M. healthy unilateral athletes participating in upper extremity sports. M. 9:219–245. (1998): The human glenohumeral 70:220–226. R. Uermura. Vangsness.S. 9:35–45. 73:668–682... Sports Sci. et al. Phys. Lephart. 4:112–118. Champaign. Hardin.. (1983): Effect of articular disease and ­stabilization being a governing factor.). and Fu. Sports Phys. Am.. G. Phys. M. Ellenbecker..M. Ide. Orthop.. Ther. L. Histol. Res. muscular sense and for a sense of effort. 26:1–30. O'Hare. J. Train. 129:562–572. 9. 3:2–17. 6th ed. Coll.D. Ann. ­repetition maximum loading schemes are geared toward 36. Warner.. 21. and Ladegaard-Pedersen.L. cle activity between patients with generalized joint laxity and normal controls. Chmielewski. M. 12:185–188. Arthrosc. Phys. Train.M. P... J. et al. J. et al. Blackburn. and Nemeth. (1994): An electromyographic analysis of 13. Clin. Ther. nology to improve healthy and injured shoulder joint position sense.. Blaiser. Paschall. Mot.. J. (1996): Sensory nerve supply in the human subacro. Pink. Nyland. 20. Goldbeck.I..B. Sherrington. 16. F.. J.. R. 19:264–272. J. Relat. Ellenbecker. Joint Stability. Clin. T. Human Kinetics. J. G.H. 143:55–67. Am. 58:94–99. 31:568–576.A.H. McGraw-Hill. and Davies. Orthop. Skills.. T. 49. Exp. C. J. S. Res.. Moesley. Neurosurg. Skinner. (1991): Differences in shoulder mus- ­athletic shoulder. T. II. and Davies. Careful monitoring of total knee arthroplasty on knee joint-position sense. Shoulder Elbow Surg. F. G. Poole. Barrack.. 11:180–184.S. fibers... Clin. Lephart.. Sports Traumatol.. (2001): Proprioceptive measures warrant scrutiny.. Roetert. Armstrong. P. Clin. J.W. M. J. J. S.M. G.. Townsend. G. Ther..A.P. (1996): Closed and open kinetic chain mal to distal segmental sequencing. J.N. Jobe. Ballantyne. Carpenter.. improving performance and enhancing proprioception and 34. 43. Sports Med. J.F. 1:15–25. J. 44:67–88.. Goldscheider. K. (1999): The efficacy of modern tech- 7. Ther. Davies. Shoulder Elbow Surg...... T.. (1994): Peripheral mechanisms in proprioception. C.D. (1898): Gesammelte Abhandlungen.. 26.N.. ­proprioception.C.N.. Jobe.C. sis of the throwing shoulder with glenohumeral instability. Tibone. Inman. (1967): The neurology of joints.. 15. Iwate Med.. B.A.J. Brain. Ageberg. and Davies. Marks. ments in female high school basketball players after a 6-week neuromuscular training 9:91–108. Grigg.. Physiologie des Muskelsinnes. J.. R. Saunders. 25. 60. Sports Phys. Train. joint position. H. and Matthews. (2000): The application of isokinetics in testing Biomechanics. K. Sproule. Ito. Scribner's Son. Shoulder Elbow Surg. and direction of motion. Shoulder Elbow Surg. Orthop. Roland.T. et  al. L..A. (1972): Articular neurology—A review. players. (1995): Rehabilitation of shoulder and elbow injuries in tennis 6:50–61. et al. Slobounov. F. exercises for the upper extremity. and Ellenbecker. Anz. II. 35:606–611. (1993): Current concepts in the rehabilitation of the ath- the shoulder joint. A. S.E. Victor. R.G. Bone Joint Surg. J. J... and Fu. Allegrucci. C. Orthop. B.J.. New York. (1984): Factors affecting stabilometry record- ings of single limb stance. (2000): Long-axis rotation: The missing link in proxi. B.. Sports Phys. the shoulder joint in healthy. the upper extremity in pitching. (1997): Effects of fatigue on knee 59... Human Kinetics.K. 48. J. 23:348–352.L. References 38. Marshall. 35:338–350.M.B. S. 8. 1st ed. J. Ther.. J. 28. Sports Phys. rotator cuff and scapular musculature have a direct effect on 33.E.P.. 46. et al. 9:231–245. et al. l Exercises using sets of 15 to 20 repetitions and 15 to 20 35. 25:40–45. niques of the upper extremities.J. 7:22–27.. Ther. Am. Wilk. Ludewig. Knee Surg. Brain Res.J. 32. Relat.. W. T. (1997): Principles of Neurology..G. 95:705–748. Roberts. joint instability progress on a continuum of difficulty. and regeneration of mammalian intrafusal muscle chain exercises in the upper extremities. 47. 19. J. 4. Bone Joint Surg.. et al. Ther. K.H. Saunders. Wyke. T. 5. 12.. Ennis. 37:85–98. (1995): Neural anatomy of the Orthop. with Ther. Eklund. (1994): Shoulder proprioception: neuromuscular control. Phys. 31:546–566. Barker. Sports. Sports Med. J. J. (2000): Test-retest reliability of the closed kinetic cruciate–deficient knee.C. Deng. P. J. (1958): The effect of peripheral nerve block on the appreciation and ­position sense of the knee.. Taylor.L.. and Lephart. Y.. J. S. Jerosch.. ­glenohumeral ligaments.. (1998): Complete Conditioning for Tennis.W. (2001): Dynamic knee stabil.. Orthop. H. H. H. (2000): Effects of shoulder instability on joint proprioception. J. Ther. 3:371–380.W. V. In New York. Human Kinetics. 27. et al. J.J. F... et al. J. Arthroscopy. T. T. (1972): Position sense and state of contraction: The effects of vibration. (1999): Effect of joint compression on inferior stability of the glenohumeral joint.. R. Res.B. 18:449–457. R. Orthop. (2000): The role of the sensorimotor system in the 50. (1990): EMG analysis of posterior muscle afferents to kinesthesia shown by vibration induced illusions of movement and rotator cuff exercises. Ther. F. 51. M. 32:11–23.D. K. Jobe.. acromial ligament.L. (1972): The contribution of 45. S. et al. F. and Elliot. Friden. Good. Neurophysiol. and surgically repaired shoulders. E. Morisawa. D. Shirai. and Pink. R. 18:465–481.H.. Tropp.J. Orthop. D.. Myers.. Adams.C. 22. joint: A proprioceptive and stability alliance. 39.A. Leipzig. S. 37.G.J. Sport Rehabil.. et al. M. Orthop. McCloskey. (1944): Observations on the function of 57. and Risberg.. 5:371–382. Orthop... (1993): Electromyographic activ- tions of tension and of kinesthesia in man: Evidence for a peripherally originating ity of selected shoulder muscles in commonly used therapeutic exercises.. J.. G. Miller.. J..M. 5:88–102... chain upper extremity stability test: A clinical field test.. H.T.. (1999): Textbook of Clinical Neurology. M.... T.L. ensure proper neuromuscular control and avoid the develop. Engl. 18:247–254.M. E.B.A. (2000): Closed kinetic chain testing tech- ­menschlichen Skelettmuskulatur. J. Sports Phys.L. Brostrom. and Fu. Myers.. letic shoulder. D. 21:220–226. Provins. and Sauers. and Quinney. J. Sports Med. Skinner. (1989): Shoulder kinesthesia after anterior glenohumeral joint dislocation.. Sports Med. IL.. by the effects of paralyzing joint afferents. (2001): Review of knee proprioception the medial and inferior borders of the scapula is important to and the relation to extremity function after an anterior cruciate ligament rupture. R. Athl. R. S. 42.. J. 8:31–36.D. Barrack.. Hodgdon.L.D. G. H. Lephart. 330:35–39.M.M.S. Goetz. H.J. (1995): Shoulder kinesthesia in ity: Current theory and implications for clinical scientists. Kikuchi.. Pink. J... Y.A. Effect of joint laxity. et  al. J. S. Wyke. P. S. Sports Med. et al. (1955): Innervation. IL. P.. Rudolph. l Exercises to increase endurance and fatigue resistance of the 77:1195–2002. Percept. S. J. Assoc.S. B. (eds. (1993): Neuromuscular testing and rehabilitation of Joint Stability.L. (1993): Effect of fatiguing maximal isokinetic ment of undesired motor patterning. (2009): Balance improve- and motor organs around it in early stage of human embryo. A study of the aging process. North Am.): Proprioception and Neuromuscular Control in 6.. J. Lephart. Anat...G..M. (1994): Proprioception of improving local muscular endurance... Neurol. Kawakami. B.. X. (1971): Tabelle der absoluten und relativen Muskel-spindelzahlen der 56. and Fu. C. Rhu. Am. 80:276–291. 2. Whitney. Arrigo. M. Ther. T. the shoulder complex.. Petrella. Phys.S. T. 20:554–567. G. et al. 14:87–110. Goodwin.H. Physiotherapy. Train... H. Harker. C H A P T E R 2 4    Pro p r i o c e p t i o n a n d N e u ro m u s c u l a r C o n t ro l 545 l Patients with rotator cuff dysfunction or glenohumeral 29.. and Abbot. L. (1994): Mechanoreceptors in the coraco. (1968): Histological studies on the sensory innervation of the shoulder ciated muscle activity in people with symptoms of shoulder impingement.E.P. joint.R. Shimoda. F.A. Ther. J. A. J. (1988): Dynamic electromyographic analy- mial bursa. Manske.. (1989): Proprioception in the anterior 61.B. Blackburn. motor innervation. F. 53. K. T. (2002): Sensorimotor system 41. Rev. and Cappel. Surg... R.J.E. Sports Phys. F.. Germany.. McLeod. Lephart.W. Wilk. Lattanzio. A. P... 17:1–6. T.W. 35:351–363.. S.. J. shoulder function in tennis players. DiGiovine.. 8:10–23. Ellenbecker. Athl...J.. the patient's ability to maintain the desired scapulothoracic 30. quadriceps contractions on ability to estimate knee position. Athl.. Philadelphia. 18:365–378.M.L. M. Caborn... McLeod. Ellenbecker. J..D. Orthop. (2000): Alterations in shoulder kinematics and asso- 17.. Borsa.. Sports Med.. S. Kronberg. Sport Rehabil. 1. during a shoulder rehabilitation program. White. J. et  al.. K. D. (1976): Studies of the histochemistry.M.. and Brunolli. M.. and Coelho. Ekstrand. 20:128–134. 58. Sports Med.. Orthop. 54. Am.W. and Johnson.J. 100:671–692.. F.J. ( Jpn. J. 16:481–485. J.. glenohumeral muscles during a baseball rehabilitation program. Psychiatry. Cook. .

184:208–211. Orthop. Brain Res. B.. et  al. R. Dodd.. Scand...E. M. J. 107. 32:127–131. Jonn.B. Ju.D.. J. and Newton. hip and trunk corrective action shown during single-leg stance on firm. Barrack. (1988): Retention of the posterior cruciate 106. Zuckerman. muscular concentrations of arachidonic acid. (1995): Influences on the gamma ­inhibition on quadriceps rehabilitation of patients with early. 89. Sports Med. R. and Lephart. (2001): Proprioceptive training and Opin.S. (2007): Deficits in neuromuscular con- versus normal. F. R. et al. 108. and Lephart. Wikstrom.. 31:620–631. analysis of shoulder muscles during planar motions: Anterior glenohumeral instability 114. 101. injuries in female athletes: 2 year follow-up.W.. Orthop. P. A. Growley.G. Delitto. H. J.. (1994): Proprioception Traumatol. and Bentley. Sports Phys. Hellstrom. (1993): Proprioception ­proprioception and neuromuscular control of the knee.. Am. J. D. Fitzgerals. 73:53–56.J. J. J. S..J. Orthop.O. H. Andriacchi. et al. J. Carpenter.. H. H. Hung..B. analysis of the hip and trunk during bilateral stance on firm.. J.. Clin. (1994): Biomechanical evaluation of a simu. J.. Shoulder Elbow Surg.. Chmielewski. J. Kynsburg.. Br.S. M. B. 22:325–333. and Perry J.R. M. 25:107–109.... and Hass.. Jenssen. (1995): Current concepts in shoulder to shoulder stability: Effect of injury and rehabilitation. T. Am. et  al. J. (2004): Reflexive muscle activation alter. (2005): Rehabilitation outcome in patients recovering Relat. ­cruciate ligament. a preliminary report. Shiavir. Sports Med. Cerulli..B.G..V. (1985): Objective evaluation ­implementation of a neuromuscular training program following anterior cruciate of peroneal response to sudden inversion stress.. (1988): Kinesthetic awareness in subjects with training on muscle reaction time in subjects with a history of ankle sprain.M. 115. Arthrosc.L.. (1994): Influences on the ception and sensation of joint position.. B. and Yang...H. G.. and Bergenheim. S.. Blackburn.. (1999): Proprioception Phys. rehabilitation.J. et  al. C.B. C.. 87. muscle function. and anatomic laxity to functional instability of the ankle. Hewett... T.A.L. 3(Suppl. (1988): Functional comparisons of Sports Traumatol. M.. S. 663:293–302. 123.L... Sports Med. Am. Beard. 42:90–98.. Borrero. Gallagher. and Halasi.. 8:24–30. Balyk. (2006): Perturbation- ­ligament in total knee arthroplasty. Orthop.. J. T. 402:76–94. and Straka.L. et al.J. Train. 29:53–57. and Hohnson. J. Silvers. Palmitier. and Cook. 127. J. Ownen.. 20:414–418. et al.. 100. et al.. Yochem.A.M..C..C.K.. 35:351–363. J. Y.A. (2006): Sensorimotor contribution 125. Train. et al. M. G. ­intramuscular concentrations of bradykinin and 5-HT. C. P. Olankun. Ther.. H. A. Sports Exerc.Y. 67. Clin. T. N. J. and Snyder-Mackler... G. Orthop..E. Res. rehabilitation. Relat. Clin. D. (1999): Localized muscle fatigue decreases physically active individuals.. Res.. F. (2004): The effect of local and general fatigue 85. J. Athl. 42:413–421. 73:311–315.. K.B. Zech. Am.. (1995): Strength of the quad- 34:362–367.. Riemann. Rokito. 122. L. 41:1831–1841. Am.L. Djupsjobacka.. S. L. Chou. S. 77:1166–1173.. and Lephart. Biomech..L. and Pellizon..A. Vogt. Hintermeister. Kaminski. Zech. Lentell. 420:181–189. Poppen... (1998): Knee proprioception: A review of mechanisms. Sports Med.K. and Petrella.. D. (2005): Effectiveness of a neuro- 73.D. ­prevention of anterior cruciate ligament injuries in soccer.. Hübscher. Rheumatol.. M. and Newham...L. (1980): Cyclic loading in knee ligament on knee proprioception. K. ­proprioception in the management and rehabilitation of athletic injuries. A. Mandelbaum.. shoulder internal and external rotation in elite junior tennis players.. et al. Lopez. Henry. S. K. (2001): A multi-station proprioceptive exercise program in deficit. Br. Hübscher. 105..S. Borsa. (2007): The effect of a 4-week 76:654–659.. Ellenbecker. D. Giraldo. M..M. Djupsjobacka. Train. A. Athl. Phys.. 93.M. Athl.B. T. J. Relat.. the acuity of the movement sense in the human shoulder.A. (2001): The effect of ankle disk 69. enhancement for anterior cruciate ligament deficiency. M.. D.S. Exerc. Hewett. ­lactic acid.J. Frazer. 236:36–43.B. Sports Phys. G. 80. Ther. 14:60–69. ­comprehensive rehabilitation program on postural control and lower extremity 77. 70. Avon). Orthop. J. Curr. R. 58:195–201.. C..A.N. Bone Joint Surg. G. and Bently. S. J. Guskiewicz. and Simpson. Dorr. W. J. and ankle joint position sense. Train. after knee arthroplasty: The influence of prosthetic design.A.. Res. and implications of muscular fatigue. Med. Rheumatol.L.A.J. of two surgical techniques. (2010): Gait termina- 78. S. J. J. (1988): EMG profiles of knee function in individuals with chronic ankle instability. gamma muscle spindle system from muscle afferents stimulated by increased intra- 64.J.. and Olmsted-Kramer. Res.J. 121.J.. Med. Sharma. Beard. 3:249–297. G. F. ations in shoulders with anterior glenohumeral instability. Cobb. M. Res.. 97. Orthop. Am. Am. 26:262–265. injuries..G.P. Ther. 84:90–95... J. J.E. (2002): Strategies for enhancing 72. Hübscher. 104. Hung. Res. Br.. A. J.. 94. Sports Phys. and Dudzinski. and Dieter... E. and ­neuromuscular control of the shoulder after muscle fatigue. (2001): Shoulder proprioception in 112.... S.. Myers. Risberg.. Tsuda. 11:402–413... Myers. from reconstruction of the anterior cruciate ligament. Orthop..G.. ­multiple ankle sprains. J. R.H. proprioception in the knee. Rehabil. Orthop. Riemann. Barrack.. J. W. T. L. et al. 19:564–569. and Uhl. A. (2007): Functional fatigue and upper extrem. Acta Orthop. Orthop. J. Birdzell. 6:630–638. et  al. Trundle. 42:197–205. Bergenheim... et  al. 81.. J. (2009): Neuromuscular control lated Bankart lesion. Rehabil.. Phys.):S13–S19. 11:130–135. (2009): Neuromuscular training for rehabilita- 86. (1995): The contributions of proprioceptive 102. J. (2010): Balance training for neuromuscular con- measurements.B.. Eils. J. Stone. R.. L. Sports Phys. and proprioception after open surgery for recurrent anterior instability: A comparison 113.A. Ther.. 74. et al.. Sci.J. Johansson.. Barrett.J. Relat. Sports 91. K. (1991): Kinetic chain exercise in knee 32:1013–1021.. a systematic review. M. 9:253–258. 126. 80:128–140. T. B. A.. 8:11–16. Myers.B. Pederson.. Orthop. 103. Cobb. An. Kyberd. Vogt.. K. Clin.J. Sci. 45:392–403. Ferguson.. Jobe. Ther. Safran. T. J... tion training in nonoperative anterior cruciate ligament rehabilitation programs for 90. 21:463–470. ­laxity. Sci. and Holm.. (1993): Proprioception after rupture the gamma muscle spindle system from muscle afferents stimulated by increased of the anterior cruciate ligament.P. R..M. Sports Exerc.K. (2004): Dynamic upper limb proprioception in 111. M. M. (1998): The effects of neuromuscu. M.. Miura. Med. Pink.. and Douex. G.. L. J. Faber.N. (1999): Testing isokinetic muscular fatigue of 31:1047–1052.B. Bergenheim. and Snyder-Mackler. Arthroplasty. M. Clin. J. anterior muscle activity during selected rehabilitation exercises. J. Ishibashi..J. Knee Surg. Am. Nixon. E. M.K.. Res. Lin. 29:627–632. M. 288:40–47.. (2001): Design and 71. S. tion of sports injuries: A systematic review. and Lephart. A. Orthop.. S.F. R. and Galante. and Hawkins. R. Bishop. B.. (1998): The role of the scapula in athletic shoulder function. G.W. Weisman. Bone Joint Surg. Myers.R.... M.W. posterior cruciate retained versus sacrificed in total knee arthroplasty. Adv. et al.H. M. Lattanzio. Phys.E. et al..T. Sports Med.. B. X. Barden. (2011): The effects of scapular taping on 27:784–791.L... Zazulak. Wyatt. E. Ther. J. E.G. (1996): Comparative electromyographic tiaxial surfaces. R. et al. C. 68:1667–1671. Shoulder Elbow Surg. (1993): Functional testing in the anterior cruciate tion control strategies are altered in chronic ankle instability subjects. Athl. Reitz. H. and Myer.. enhanced neuromuscular training alters muscle activity in female athletes. T. Lephart. T. P MR. Pincivero. et  al.. and Roetert. I. J. 96. (2000): The efficacy of perturba- on shoulder joint position sense. 56:72–74.. M. et  al. joint musculature during walking: Changes induced by anterior cruciate ligament 37:303–311. ­electromyographic muscle activity and proprioception feedback in healthy shoulders.. Trip. M. Am. Cuomoa.D. W... J.... et al. Livingstone. Skinner..D. L. Neurosci. Res. 98. Myers. Brunet. J..W. M. R. P. Relat.P. (1997): The role of proprioception and the effect of lidocaine injection. Med.. 14:30–34. J. Baas. a prospective biomechanical-epidemiologic 84. M. Blaiser. F.. J.M.. Orthop.. Sci. Hertel. Lehman. L. (1986): Exercise related knee joint study. Mork. 117.. Lepahrt. Sports Phys. (1995): Influences on 65. Athl.B. 79. Kaplan. 5:118–123. 109. Sports Exerc.. Sports Med. Sports Med. Lephart. Train. G.. Sports Med. Am. Med.. J. M.. Limbird. and Bruce. and Birac.L. R. 11:197–201... Man. J. and Fu. Res. Djupsjobacka.. (1997): Impaired proprioception and osteoarthritis. 26:325–337. Bone Joint Surg.. Bone Joint Surg. unilateral osteoarthritic muscle spindle system from contralateral muscle afferents stimulated by KCl and knees. Zech. Relat. T. E. Laskowski.M. (1991): Joint proprioception in normal muscular and proprioceptive training program in preventing anterior ­cruciate ligament osteoarthritic and replaced knees. Ther.. Panics. T. J.. riceps femoris muscle and functional recovery after reconstruction of the anterior 92. 33:1991–1998. P. R. Neurosci. 29:275–281. 297:182–187. A.. Benoit. and Cook. P. Schneider.A.M. Orthop.. H.G. D. knee. Hale. 88. Speer. N. F. Sports Exerc. R. (1985): Age-related changes in joint proprio.J. J. J. J. Shoulder Elbow Surg. et al.T. and Borra. 118. (1998): The effects of muscle fatigue 120.J. Paterno. Pope. Ecker. Sports Med... Pfeifer.. Res. (2010): Long-term neuromuscular training multidirectional shoulder instability. foam. J. Gutierrez. B. 18:655–661.. Shoulder Elbow Surg. 25:130–137.M.. Skinner... 21:301–309.L. lar control exercises on functional stability in the unstable shoulder. C. Clin. Ochsner. et al... and ankle instability. D. Ther.L. Am. J. 33:1003–1010. 76:1819–1826. S.. Arthroscopy.E. M.J. patients with ankle instability.. (1984): Age related decline in proprio. Y. Garn... Oper. E.M. S. (1999): Normal shoulder 119. Arch. and Walker. K. P. D.. deficiency. Y. Watanabe..R.. Sports Med..R. (1976): Normal and abnormal motion of the ­shoulder.. H. Riemann.. 97:183–191. Decker. ception. Sports Med. McMahon.546 Physical Rehabilitation of the Injured Athlete 63.L.. 95. Orthopedics.. . Osborne. D. Raso. Sci. (2010): Recovery of shoulder strength port surfaces. B. A. Reeves.V.. 31:655–661... (2010): Neuromuscular training for sports 33:S15. Am. (1983): Joint laxity and Ther. Snyder-Mackler. et al. Hurd. J. Acta Physiol. S... P..J. (2003): Kinematic baseball pitchers.. 10:438–444. K. Kibler. 1:359–365. et al... Orthop.D. Axe. Bone Joint Surg. Warren. Caraffa. J.M.J.T.J. Bone Joint Surg.. (2000): The role of the sensorimotor system in the 124. H.. A. 110. Kibler.. et al. A..P. foam and multiaxial sup- 82. Br. J. (1993): The influence of arthrogenous muscle 99. 7:401–405. Ortop. et  al. athletic shoulder.S.D. injury prevention. Johansson.A. trol of the trunk predict knee injury risk.M. J.M. L.P.D. and Pai.S.S. Nawoczenski.. B.A. Am.L...D.B. 76. 116. H. Andriacchi. trol and performance enhancement: A systematic review. D. Sports ­ligament–deficient knee. G... 68. and mul- 83.. J. Med..M. G. Scott.. (Bristol... S. 35:1123–1130. Sports Med. Myers. (2003): Comparison of the ankle.. Skinner. Clin. Inamdar. 21:206–215.. J. Deng.P. M. Johansson. (1999): Serratus ity sensorimotor system acuity in baseball athletes. ­ligament reconstruction.J. Wassinger. 75.. Hurley... Phys. L. M.. Biel.. Hwang. 66..

. Sports Exer. Riemann. 28:711–719. (1986): A three dimensional cinematographic quency treatment pattern on joint capsular healing.. Myers. and Rhea. ed. S. Chen. G.R.F.. 3 rd Surg... Strength Cond.. P. Wickiewicz. 136. Elliot. and Warren.. Kraemer. O'Brien. Lu.. and Mattalino. Relat. J. A. Int. B. Lephart.L. (2000): Evaluation of shoulder prop- electrical activity during Bodyblade exercises. Shoulder Elbow 129. Sport Biomech. a and rotator cuff strength following arthroscopic anterior stabilization with thermal meta-analysis.T. M.. T. Saha. Ther. C H A P T E R 2 4    Pro p r i o c e p t i o n a n d N e u ro m u s c u l a r C o n t ro l 547 128. Davies.B. Res. and Fleck.. Am. B. Presented at Wisconsin State Physical rioception following thermal capsulorraphy. an ovine model. T. Clin. R. 32:S123.. et al. Sports Med. R. Orthop. M.J. S. Holt.. S. Y. B.J. capsulorraphy.J. (1999): Glenohumeral joint range of motion 132. 29:160–167.. J. 8:49–52..L.. Marin. Ellenbecker. 173:3–10. K. Sports Phys. (1983): Mechanism of shoulder movements and a plea for the recognition 133. Edwards. . 24:548–556. In vitro and in vivo studies using analysis of the tennis serve. J. et al. T.J.. W. A.. et al. (2003): Designing Resistance Training Programs. 2:260–271. Human Kinetics..J. Simonion. (2000): The effect of monopolar radiofre- 130. P. (1999): Radiographic of “zero-position” of glenohumeral joint.K. Orthop... J. J. evaluation of glenohumeral kinematics: A muscle fatigue model. Marsh.S. Hayashi. Med. (2000): An investigation of shoulder muscle 135.. 134. Sci.K.. (2010): Effects of vibration training on muscle strength. Res. and Blanksby. Therapy Association Spring Meeting. IL.B. S. Champaign.. 131.. J.M.