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ARTICLE IN PRESS

Manual Therapy 13 (2008) 2–11


www.elsevier.com/locate/math

Masterclass

Sensorimotor disturbances in neck disorders affecting postural


stability, head and eye movement control
Julia Treleaven
Neck Pain and Whiplash Research Unit, Division of Physiotherapy, University of Queensland, Brisbane, Qld 4072, Australia
Accepted 8 June 2007

Abstract

The receptors in the cervical spine have important connections to the vestibular and visual apparatus as well as several areas of the
central nervous system. Dysfunction of the cervical receptors in neck disorders can alter afferent input subsequently changing the
integration, timing and tuning of sensorimotor control. Measurable changes in cervical joint position sense, eye movement control
and postural stability and reports of dizziness and unsteadiness by patients with neck disorders can be related to such alterations to
sensorimotor control.
It is advocated that assessment and management of abnormal cervical somatosensory input and sensorimotor control in neck pain
patients is as important as considering lower limb proprioceptive retraining following an ankle or knee injury. Afferent information
from the cervical receptors can be altered via a number of mechanisms such as trauma, functional impairment of the receptors,
changes in muscle spindle sensitivity and the vast effects of pain at many levels of the nervous system. Recommendations for clinical
assessment and management of such sensorimotor control disturbances in neck disorders are presented based on the evidence
available to date.
r 2007 Elsevier Ltd. All rights reserved.

Keywords: Sensorimotor; Eye; Head; Postural stability; Cervical; Management

1. Introduction spindles per gram (Kulkarni et al., 2001; Boyd Clark


et al., 2002; Liu et al., 2003). The cervical muscles,
Sensorimotor control of stable upright posture and especially the suboccipital muscles, relay information to
head and eye movement relies on afferent information and receive information from the central nervous system
from the vestibular, visual and proprioceptive systems, and there are specific connections between the cervical
which converge in several areas throughout the central receptors and the visual and vestibular apparatus and
nervous system. The cervical spine has an important role the sympathetic nervous system (Selbie et al., 1993;
in providing the proprioceptive input and this is Bolton et al., 1998; Corneil et al., 2002; Hellstrom et al.,
reflected in the abundance of cervical mechanoreceptors 2005). The cervical afferents are also involved in three
and their central and reflex connections to the vestib- reflexes influencing head, eye and postural stability: the
ular, visual and central nervous systems. cervico-collic reflex (CCR), the cervico-ocular reflex
Muscle spindles in the cervical region are found in (COR) and the tonic neck reflex (TNR). These reflexes
high densities especially in the suboccipital region where work in conjunction with other reflexes, which are
there are up to 200 muscle spindles per gram of muscle. influenced by vestibular and visual input for coordinated
This number is considerable when compared to the first stability of the head, eyes and posture. The CCR
lumbrical in the thumb where there are 16 muscle activates neck muscles in response to stretch to assist in
the maintenance of head position (Peterson, 2004). The
Tel.: +617 3365 2275; fax: +617 3365 2775. COR works with the vestibuloocular reflex and optoki-
E-mail address: j.treleaven@shrs.uq.edu.au netic reflex, acting on the extraocular muscles, to assist

1356-689X/$ - see front matter r 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.math.2007.06.003
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J. Treleaven / Manual Therapy 13 (2008) 2–11 3

Cerebral cortex

Thalamus Superior colliculous


Hypothalamus Medial and lateral vestibular nucleii
Reticular formation Central cervical nucleus
Dorsal column nucleii

Spinothalamic
Spinocerebellar Cerebellum
Propriospinal Tracts
Ventral
Dorsal horn

Cervical SNS
COR
CCR

OKR VCR
Ocular Vestibular

VOR

VSR
TNR

Lower limb

Fig. 1. Central and reflex connections associated with the cervical spine afferents.

clear vision with movement (Mergner et al., 1998). 1996; Treleaven et al., 2003), postural stability (Karlberg
The TNR is integrated with the vestibulospinal reflex et al., 1996; Sjostrom et al., 2003; Treleaven et al.,
to achieve postural stability (Yamagata et al., 1991) 2005a, b; Field et al., 2007) and oculomotor control,
(Fig. 1). such as altered smooth pursuit and saccadic eye move-
The importance of the cervical central and reflex ment (Tjell et al., 2003; Treleaven et al., 2005a, b; Storaci
connections can be realized from response to artificial et al., 2006), can present in patients with neck disorders
disturbances to the cervical afferents in asymptomatic of either an insidious or traumatic nature as a result of
individuals. Sectioning of the cervical nerves or anaes- cervical somatosensory dysfunction. An increased gain
thetic injections into the neck causes nystagmus, of the cervico-ocular reflex has also been demonstrated
disequilibrium and severe ataxia (DeJong and DeJong, in patients with whiplash (Montfoort et al., 2006).
1977; Ishikawa et al., 1998). Vibration of neck muscles, Altered smooth pursuit neck torsion control occurs in
which is thought to stimulate muscle spindle afferents, neck pain subjects (both idiopathic and traumatic) but
induces several disturbances in asymptomatic indivi- not in those with vestibular disorders and central
duals including changes to eye and head position, nervous system dysfunction. Smooth pursuit neck
alterations to body sway and the velocity and direction torsion control is a difference in eye movement control
of gait and running (Lennerstrand et al., 1996; Bove when measured with the neck in torsioned (i.e., trunk
et al., 2002; Courtine et al., 2003). Similar effects have turned 451 but the head remains neutral compared to a
been demonstrated by either simple isometric neck neutral head, neck and trunk position) and supports the
muscle contractions or induced neck muscle fatigue premise of neck afferent dysfunction as the cause of the
(Gosselin et al., 2004; Schmid and Schieppati, 2005; smooth pursuit eye movement disturbances (Tjell and
Vuillerme et al., 2005). Such disturbances are thought to Rosenhall, 1998; Tjell et al., 2003; Treleaven et al.,
result from a mismatch between abnormal information 2005a, b).
from the cervical spine and normal information from the Complaints of dizziness and or unsteadiness can also,
vestibular and visual systems. but not necessarily, occur in patients with chronic
cervical headache and persistent whiplash-associated
disorders (Treleaven et al., 2003; Jull et al., 2007). Some
2. Disturbances in sensorimotor control in neck disorders neck pain patients also report visual complaints, loss of
balance and actual falls (Hulse and Holzl, 2000;
Considering the experimental evidence, it is not Treleaven et al., 2003). Cervical vertigo is considered a
surprising that disturbances in cervical joint position principle cause when associated with a whiplash injury
sense (JPS) (Revel et al., 1991; Heikkila and Astrom, (Wenngren et al., 2002; Treleaven et al., 2006) but other
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4 J. Treleaven / Manual Therapy 13 (2008) 2–11

causes of dizziness and unsteadiness should be consid- (Le Pera et al., 2001; Thunberg et al., 2001; Flor, 2003).
ered, such as damage to the vertebral artery, vestibular Psychosocial stresses might also alter muscle spindle
receptors or central nervous system, elevated anxiety or activity via activation of the sympathetic nervous system
medication intake (Baloh and Halmagyi, 1996; Ernst (Passatore and Roatta, 2006).
et al., 2005; Sturzenegger et al., 1994). Greater deficits in It is likely that several processes combine to cause an
tests of head and eye movement control and postural immediate and sustained alteration in somatosensory
stability have been measured in patients with neck function originating from the cervical spine, which
disorders of traumatic origin, in association with the influence the tuning and integration of input within
complaint of dizziness (Tjell et al., 2003; Treleaven et al., the sensorimotor control system. Secondary impairment
2003, 2005a, b), although these deficits can present in the of vestibular system functioning might also occur
absence of dizziness as well as in patients with idiopathic (Fischer et al., 1997) and this has implications for
neck pain (Kristjansson et al., 2003; Tjell et al., 2003; management of such disturbances in neck disorders. The
Field et al., 2007). Although the causes of the majority of the research into sensorimotor control
disturbances are similar it has been shown that an disturbances has been undertaken in patients with
individual patient may present with dysfunction in either persistent neck pain, however there is evidence that
one or several systems. For example, an individual deficits could occur soon after the onset of pain (Sterling
patient may have moderate disturbances to eye move- et al., 2003) and may have an influence on prognosis
ment control but not necessarily have the same degree (Hildingsson et al., 1993). Thus, routine assessment of
or any disturbance in cervical JPS or balance (Treleaven head and eye movement control and postural stability in
et al., 2006). neck disorders is recommended.
It would appear that either decreased or increased Evidence to date would suggest that management of
cervical somatosensory activity can result in distur- disturbed sensorimotor control due to cervical somato-
bances of sensorimotor function (Hinoki and Niki, sensory dysfunction might need to address the primary
1975; DeJong and DeJong, 1977). This occurs via a causes of the altered somatosensory activity as well as
number of mechanisms (Fig. 2). Cervical mechanor- secondary effects. Specific treatments to the neck such as
eceptor function could be altered as a result of direct acupuncture, manual therapy and cranio-cervical flexion
trauma to mechanoreceptors (Loescher et al., 1993; training have improved cervical joint position error,
Chen et al., 2006), functional impairment of muscles vertigo and/or standing balance in patients with neck
such as increased fatigability (Falla, 2004) or degene- pain (Fattori et al., 1996; Heikkila et al., 2000; Reid and
rative changes in the muscles such as fibre transforma- Rivett, 2005; Palmgren et al., 2006; Jull et al., 2007).
tion, fatty infiltration and muscle inhibition or atrophy Alternatively, programs that emphasize gaze stability,
(Uhlig et al., 1995; McPartland et al., 1997; Kristjansson eye/head co-ordination and cervical position sense
et al., 2004; Elliott et al., 2006). In addition, the effects without local cervical spine treatment have resulted in
of pain at many levels of the nervous system can change decreased medication intake, improved neck pain and
muscle spindle sensitivity and alter the cortical repre- disability and cervical joint position sense (Revel et al.,
sentation and modulation of cervical afferent input 1994; Humphreys and Irgens, 2002; Jull et al., 2007).

CNS
Represenatation cortex
Somatic reorganisation

Visual Altered Vestibular


system Altered cervical afferent Altered system
reflexes reflexes
input

Altered mechano receptor

Altered muscle spindle activity

Trauma Pain
Ischaemia Stress-SNS activation
Inflammation
Altered neuromuscular control
Morphological changes

Fig. 2. Mechanisms of disturbances of cervical somatosensory input in neck disorders.


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J. Treleaven / Manual Therapy 13 (2008) 2–11 5

Improvements in balance and symptoms of dizziness


have also been observed following a vestibular or
oculomotor rehabilitation program in patients with
persistent whiplash (Hansson et al., 2006; Storaci
et al., 2006). Currently local treatment to the cervical
spine in conjunction with tailored programs for sensori-
motor control is recommended for patients with neck
disorders. The tailored sensorimotor program is similar
to that used in vestibular rehabilitation (Herdman,
2000). This combined approach will address the local
causes of abnormal cervical afferent input and consider
the important links between the cervical, vestibular and
ocular systems and any secondary adaptive changes in
the sensorimotor control system.

3. Clinical assessment of sensorimotor control


disturbances in neck disorders

Based on the evidence to date, the assessment of


sensorimotor control in the neck pain patient should Fig. 3. Test of joint position sense using a laser pointer. A measure of
joint relocation error is gained from measuring the distance between
include: investigation of the symptom of dizziness and the return and starting positions.
unsteadiness and measurement of cervical joint position
error, postural stability and oculomotor control. The
clinician though should be aware of other possible provides a quantitative assessment tool as errors as little
causes of the disturbances and interview the patient and as 3–41 (4–5 cm) can indicate a deficit in cervical JPS
choose tests accordingly to determine the most likely (Revel et al., 1991; Treleaven et al., 2003). Errors are
cause. With respect to dizziness, the description, measured following active return from cervical exten-
temporal pattern, associated symptoms and history of sion, flexion and rotation. Relocating to selected points
the complaint of dizziness can be useful in assisting in range (Loudon et al., 1997) and accuracy in retracing
differential diagnosis of cervicogenic dizziness. Other patterns (Kristjansson et al., 2004) can also be used to
symptoms such as visual complaints (blurred vision, assess cervical kinaesthesia. Jerky movements, searching
words jumping and unclear contours of objects) loss of or overshooting the initial position, reproduction of
balance, actual falls, difficulty walking in the dark, on dizziness and/or a noticeable difference of cervical
stairs or negotiating doorways should be noted. The movement patterns in the test with eyes closed may
Dizziness Handicap Inventory Short Form Question- also indicate impaired cervical kinaesthetic sense.
naire (Tesio et al., 1999) can be used to quantify the
functional impact of the dizziness. The physical exam- 3.2. Oculomotor
ination may include measures of cervical joint position
sense, postural stability and oculomotor control as Oculomotor assessment incorporates assessment of
indicated. In research, precise measurements are taken gaze stability (the ability to maintain gaze while moving
of these features. However, they can be assessed the head), smooth pursuit (eye follow while keeping the
satisfactorily in the clinical situation albeit with lesser head still), saccadic eye movement (rapid eye move-
precision. ments to change a point of fixation) and eye/head co-
ordination (maintaining gaze when both the eyes and
3.1. Cervical joint position sense (JPS) head are moving). The tests are usually performed with
the patient in a sitting position but can be tested initially
A simple measure for cervical JPS is the use of a small in supine lying if necessary. The starting position will
laser pointer or torch mounted onto a lightweight depend on the severity of the patient’s complaints and
headband as used by Revel et al. (1991) (Fig. 3). The overall physical findings.
patient is seated 90 cm from a wall and the starting point
projected by the laser is marked. The patient (blind- 3.2.1. Gaze stability
folded or eyes closed) performs an active neck move- Gaze stability is assessed by asking the patient to keep
ment and then returns as accurately as possible to the the eyes focused on a target while actively moving the
starting position. The final laser position is measured head into flexion, extension and rotation (Fig. 4).
against the starting position in centimeters. This method Inability to maintain focus on the target, reduced or
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awkward cervical motion or reproduction of symptoms these neck torsion positions compared to the neutral
such as dizziness, blurring of vision or nausea are signs position. Often patients with neck disorders will be
of an abnormal response. unable to keep up with the target and demonstrate quick
catch up eye movements when the neck is in torsion
3.2.2. Eye follow particularly when the target is crossing the midline.
The patient keeps the head still while following a Saccadic eye movements at the extremes of the visual
moving target with the eyes as closely as possible. The angle and with the change of movement direction are
target is moved slowly side to side (201/s through a not considered abnormal.
visual angle of 401). The test is repeated with the head
still but with the trunk rotated up to 451 (Fig. 5). The 3.2.3. Saccadic eye movement
test is repeated on the opposite side. Any difference is The patient follows and fixes their gaze on a target
noted in smooth eye follow or symptom reproduction in that is quickly moved and then held still momentarily.
The target is moved in several different directions. The
patient’s ability to quickly move to the target and fixate
on it is noted.

3.2.4. Eye/head co-ordination


The patient moves the eyes and head in the same
direction to focus on a point, leading with the eyes first
to a target and then the head ensuring the eyes keep
focused on the target. This can be performed to the left,
right and up and down.

3.3. Postural stability

A modified sensory organization test is used to assess


postural stability. Visual and proprioceptive input from
the lower limbs is altered as the tests progress (Shum-
way-Cook and Horak, 1986). Balance in comfortable
and narrow stance can be assessed with the patient
standing on a firm and then a soft surface such as a piece
of 10 cm dense foam. The tests should be performed
with both eyes open and closed. Inability to maintain
stance for 30 s, noticeably large increases in sway, slower
Fig. 4. Testing gaze stability during head rotation to the right. responses to correct sway or rigidity to prevent sway are

Fig. 5. Eye follow keeping the head still is tested (a) with the neck in a neutral position and repeated (b) with the neck torsioned via trunk rotation.
The neck torsion is tested to both the left and right. A deterioration in eye follow in the neck torsion positions, when compared to the neutral position
suggests a cervical origin of deficits in eye movement control.
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considered abnormal responses. It is thought that people mechanoreceptor input as well as the effects resulting
with neck disorders rely more on vision and other from the potential conflict arising from abnormal
somatosensory inputs for balance and thus deficits will cervical afferent input and normal vestibular and ocular
be greatest when these inputs (e.g., vision) are reduced. input.
For increasing challenge, the patient can be tested in Exercises for each system should be performed two to
tandem and then single leg stance on a firm surface with five times per day. Temporary reproduction of dizziness
eyes open and closed. It is reasonable to expect that a is acceptable however exacerbation of neck pain or
person under the age of 60 years can maintain stability headache is not acceptable. If this occurs the exercises
for up to 30 s in the comfortable and narrow stance tests. should be modified by decreasing the number of
Subjects under 45 years should also be able to complete repetitions or altering the patient position to a more
tandem and single leg stance tests. (Treleaven et al., supported position such as supine lying. Progression of
2005a, b) Assessment of the ability to complete the 30 s each exercise set can be achieved by altering the
of the tandem stance can be a useful screening test duration, repetitions and the degree of difficulty of the
(Treleaven et al., 2005a, b; Field et al., 2007). task. Exercises can also be progressed by performing
activities such as an eye task or cervical JPS practice
3.4. Additional tests while sitting on an unstable surface or while standing
with the feet in an unstable base of support for example,
There is some evidence that the neck may directly heel toe stance, or while walking. Some examples follow.
influence vestibular functioning (Fischer et al., 1997). In
addition, primary vestibular pathology is also possible 4.1. Cervical joint position sense
following a whiplash injury or in the middle aged/elderly
population. Thus, assessment of postural control The patient practices relocating the head back to the
disturbances may need to address secondary vestibular natural head posture and to pre-determined positions
influences on postural control. While there is certainly in range from the movement directions assessed to be
overlap between cervical and vestibular systems in a abnormal. The patient may practice first with the eyes
number of the testing procedures already described, open and then with eyes closed, lining up their natural
additional tests to investigate vestibular function more head posture and target positions with points on the
closely may be necessary in some neck pain patients, wall to check their accuracy on return. The exercise can
especially those complaining of loss of balance and falls. be made more precise for home use with the use of a
Factors such as ageing, pre-existing vestibular patho- pencil torch or laser attached to a headband. Higher
logy and medical conditions might increase the degree of level skills training could include tracing intricate
disturbances in those with neck disorders (Poole et al., patterns, such as a figure of 8 placed on the wall, with
2007). Additional tests might include tests of dynamic the head using the head torch or laser for feedback.
balance and functional ambulation (Herdman, 2000;
Alpini et al., 2005), as well as testing of the vestibulo- 4.2. Oculomotor exercises
ocular reflex (Herdman, 2000). In cases where Benign
Paroxysmal Positional Vertigo is suspected the Hall- The exercise level is set on the basis of the oculomotor
pike-Dix manoeuvre should be included (Herdman, assessment. The degree of difficulty for oculomotor
2000). Referral for a more thorough investigation of the exercises can be increased by increasing the speed of the
vestibular or central nervous system may be warranted task, range of motion, changing the patient’s position
in those where cervical causes of the disturbances cannot and the focus point or background (Fig. 6). Table 1
be substantiated. outlines how each of the various variables can be altered
to progress the exercises.

4. Management of sensorimotor control disturbances in 4.2.1. Eye follow with a stationary head
neck disorders The patient eyes follow a target moving side to side
and up and down keeping the head still. For home use,
The findings of the assessment will direct and tailor the patient could practice tracking a tennis ball tossed
the most appropriate management of sensorimotor sideways or up and down whilst keeping the head still.
control disturbances in the individual patient with a
neck disorder. It is suggested that management include 4.2.2. Saccadic eye movements
both local treatment to the neck to decrease pain and Saccadic movements of a target are performed at
improve neuromuscular function in combination with randomised eye positions. Progression can include
tailored sensorimotor exercises to improve any deficits increasing the speed of the movements, position of
in cervical JPS, oculomotor control and postural the patient and the visual background or focus point
stability. This addresses the causes of abnormal cervical (Table 1).
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8 J. Treleaven / Manual Therapy 13 (2008) 2–11

Focus on
Focus
these words

Focus on
Focus
these words

Focus on
Focus
these words

Fig. 6. Progression of eye exercises by altering either the focus point or the background of the focus point.

Table 1
Various methods of progression of the oculomotor exercises

Variable Start Progress Further progression

Target Single spot Word Business card


Background to target Plain Stripes Checker board
Patient position Supine—sitting Standing—vary stance Walking
Neck position Neutral Torsion 301 Torsion 451
Speed Slow Medium Fast
Vision Unrestricted Restricted peripheral Restricted peripheral
Range of motion Small Medium Large
Duration of exercise 30 s 1–2 min 5 min
Frequency of exercise 2  day 3  day 5  day

4.2.3. Gaze stability and down directions. As a progression, the eyes are
Training may commence with the clinician perform- moved first, then the head, but the patient continues
ing slow passive neck movements or the patient to maintain focus on two targets which can be
performing active neck movements, while they fixate positioned horizontally or vertically. Further progres-
their gaze on a point on the ceiling. The clinician can sion could include the patient performing active
also passively move the trunk while the patient neck rotation to follow a slow moving target while
maintains gaze on a target. The patient can be asked their peripheral vision is restricted. The patient
to fix their gaze on a point, close their eyes and perform can also practice rotating the eyes and head to
a neck movement and open their eyes after the head the opposite side in both directions. For home
movement to check for stable gaze on the target. Any practice, the patient could hold a target in front of
task may be progressed by restricting peripheral vision, them and move the target and their head in opposite
using a pair of swimming goggles that have been directions.
blackened out except for a small area in the center of The patient should also practice moving the eyes,
each side. head, neck and arm following their thumb or moving
the eyes, head, neck and trunk to look as far behind as
4.2.4. Eye/head co-ordination possible. Active movements of the head to follow a
The exercises commence with rotating the eyes and moving target can be performed both with unrestricted
head to the same side, in both left and right and up and peripheral restricted movement.
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as a tailored sensorimotor exercise program to improve


identified deficits in postural stability and head and eye
movement control. The recommended clinical assess-
ment and management is based on the available
evidence to date, however this is an emerging area and
more extensive research is needed to refine and identify
methods for assessment and determine the optimal
strategies for management of such disturbances in
patients with neck disorders.
There will be a case study published online to support
this Masterclass at a later date.

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ARTICLE IN PRESS
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