590390

research-article2015
JHS0010.1177/1753193415590390Journal of Hand Surgery (European Volume)Hagert et al.

Review Article
JHS(E)
The Journal of Hand Surgery

The role of proprioception and (European Volume)

XXE(X) 1­–8
© The Author(s) 2015
neuromuscular stability in carpal Reprints and permissions:
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instabilities DOI: 10.1177/1753193415590390

jhs.sagepub.com

E. Hagert1,2, A. Lluch3,4 and S. Rein5,6

Abstract
Carpal stability has traditionally been defined as dependent on the articular congruity of joint surfaces, the
static stability maintained by intact ligaments, and the dynamic stability caused by muscle contractions
resulting in a compression of joint surfaces. In the past decade, a fourth factor in carpal stability has been
proposed, involving the neuromuscular and proprioceptive control of joints. The proprioception of the wrist
originates from afferent signals elicited by sensory end organs (mechanoreceptors) in ligaments and joint
capsules that elicit spinal reflexes for immediate joint stability, as well as higher order neuromuscular influx
to the cerebellum and sensorimotor cortices for planning and executing joint control. The aim of this review
is to provide an understanding of the role of proprioception and neuromuscular control in carpal instabilities
by delineating the sensory innervation and the neuromuscular control of the carpus, as well as descriptions of
clinical applications of proprioception in carpal instabilities.

Keywords
Carpal instability, joint innervation, mechanoreceptors, neuromuscular control, proprioception, wrist

Date received: 30th March 2015; revised: 30th April 2015; accepted: 12th May 2015

Introduction
The brief definition of carpal instability is that it is a
joint instability occurring between bones located in
the same carpal row, defined as a ‘carpal instability
dissociative’ (Wright et al., 1994) or as ‘carpal insta-
bility non-dissociative’ (CIND) when there is a dys-
function of the entire proximal carpal row, manifested
at either the radiocarpal (RC) joint, the midcarpal
(MC) joint, or both (Wolfe et al., 2012).
There are two types of CIND: extrinsic and intrin-
sic. Extrinsic CIND is when the carpal dysfunction is
the consequence of an injury or deformity outside
the wrist. Intrinsic CIND results from RC and/or MC
ligament attenuation plus inadequate neuromuscu-
Carpal stability was first described by Linscheid
et al. in 1972 (Linscheid et al., 1972) as being depend-
ent primarily on the articular congruity of joint sur-
faces and the static stability maintained by intact
ligaments. Later, the authors amended this to also
include the dynamic stability caused by muscle con-
tractions resulting in a compression of joint surfaces
(Linscheid and Dobyns, 2002). In the past decade, a
fourth factor in carpal stability has been proposed,
1Department of Clinical Science and Education, Karolinska
Institutet, Stockholm, Sweden
2Hand & Foot Surgery Center, Stockholm, Sweden

lar control of the joint. In turn, three subtypes of
intrinsic CIND can be distinguished: anterior or pal-
mar midcarpal instability (PMCI), posterior or dor-
sal MC instability, and multidirectional combined
RC–MC instability (Garcia-Elias, 2008; Lichtman
3Institut Kaplan, Barcelona, Spain
4Department of Orthopaedic Surgery, Vall d’Hebron Hospital,
Barcelona, Spain
5Department of Orthopaedic and Trauma Surgery, University
Hospital ‘Carl Gustav Carus’, Dresden, Germany
6Department of Hand and Plastic Surgery, Burn Unit, Berufsgenos-

and Wroten, 2006). PMCI or palmar CIND is the senschaftliche Klinik Bergmannstrost, Halle (Saale), Germany
most common type of non-dissociative instability.
Corresponding author:
However, before we further discuss carpal instabili- E. Hagert, Hand & Foot Surgery Center, Storängsv 10, 11542
ties, a definition of what constitutes carpal stability Stockholm, Sweden.
is needed. Email: elisabet.hagert@ki.se

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2 The Journal of Hand Surgery (Eur)
involving the neuromuscular and proprioceptive con-
trol of joints (Hagert, 2010b).
The term proprioception is derived from Latin, ‘pro-
prius’, belonging to one’s own, and ‘-ception’, to per-
ceive. The term was first established by the 1932 Nobel
laureate in Physiology or Medicine, Sir Charles Scott
Sherrington, who, in 1906, (Sherrington, 1906) defined
proprioception as sensations arising in the deep areas
of the body, contributing to conscious sensations
(‘muscle sense’), total posture (‘postural equilibrium’),
and segmental posture (‘joint stability’).
The term proprioception thus includes a broad
description of the afferent information that is derived
from sensory nerve endings in skin, joint capsules/
ligaments, and muscle spindles, which converge to
provide a conscious and unconscious appreciation of
skin deformation, muscle force, and action, as well
as joint position and movement (Fortier and Basset,
2012; Proske and Gandevia, 2012). To distinguish the
complex physiological processes involved in proprio-
ception and joint control, the term sensorimotor sys-
tem was adopted at the 1997 Foundation of Sports
Medicine Education and Research workshop to
describe the sensory, motor, and central integration
and processing components involved in maintaining
functional joint stability (Riemann and Lephart, 2002).
In this description of the sensorimotor system, con-
scious and unconscious proprioception senses both
exist and are most frequently analysed as joint posi-
tion sense, kinaesthesia (joint motion sense) and
neuromuscular joint control (Hagert, 2010b).
The latter, neuromuscular joint control, includes
the anticipatory control of muscles around a joint
through so-called feed-forward control, as well as the
ability to unconsciously maintain joint stability and
equilibrium (Lephart et al., 2000; Sjolander et al.,
2002). The unconscious neuromuscular sense is pri-
marily influenced by afferent signals from sensory end
organs (mechanoreceptors) in ligaments and joint
capsules that elicit spinal reflexes for immediate joint
stability, as well as higher order neuromuscular influx
to the cerebellum and cerebrum for planning, antici-
pating, and executing joint control (Hagert, 2010b).
The aim of this review is to provide an understand-
ing of the role of proprioception and neuromuscular
control in carpal instabilities by delineating the sen-
sory innervation and the neuromuscular control of
the carpus, with a description of clinical applications
of proprioception in carpal instabilities.
Sensory innervation of the carpus
Innervation of the wrist joint
In general, the wrist is innervated by articular
branches arising from the median, ulnar, radial, and
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musculocutaneus nerves (Ferreres et  al., 1995)
(Figure 1).
The lateral antebrachial cutaneous nerve (LACN),
a terminal sensory branch of the musculocutaneus
nerve, innervates the radial aspect of radiocarpal
joint (Van de Pol et al., 2006).
The median nerve gives off two branches as it
courses through the forearm, namely the anterior
interosseous nerve (AIN) as well as the palmar cuta-
neous branch (PCB). The AIN, after innervating the
pronator quadratus muscle, contributes innervation
to the central two-thirds of the volar wrist capsule
and the radioscapholunate ligament (Fukumoto
et al., 1993). The radioscapholunate, containing the
terminal branch of the AIN, in turn supplies the
innervation to the volar aspect of the scapholunate
interosseous ligament (SLIL) complex (Berger, 2001).
The PCB innervates the volar MC space in the area
of the lunate and capitate. Rarely, a connection
between the PCB and the LACN has been found, indi-
cating that the LACN may also contribute innervation
to the radial part of the carpus (Van de Pol et al., 2006).
The ulnar nerve is primarily important in the
innervation of the triangular fibrocartilage complex
(Shigemitsu et al., 2007). However, minor contribu-
tions are also made to the innervation of the carpus.
A recurrent branch of the deep ulnar nerve may be
found innervating the carpal ligaments around the
head of the capitate, and branches of the dorsal sen-
sory ulnar nerve contribute innervation to the dorsal
wrist capsule and intercarpal ligaments (Van de Pol
et al., 2006).
The radial nerve, through the posterior interosse-
ous nerve (PIN) and the superficial sensory branch, is
a major contributor of innervation to the wrist joint.
The PIN innervates the dorsal wrist capsule, the dor-
sal SLIL and lunotriquetral interosseous ligament, as
well as the dorsal radiocarpal and intercarpal liga-
ments (DRC/DIC, respectively) (Ferreres et al., 1995;
Van de Pol et al., 2006). The superficial sensory
branch provides minor articular branches to the dor-
soradial and radiovolar wrist capsule (Van de Pol
et al., 2006).
Mechanoreceptors and innervation of
wrist ligaments
Sensory nerve endings, so called mechanoreceptors,
are the primary focus of innervations studies in joints.
They are able to detect mechanical stimuli, e.g.
changes in joint position or velocity, transform them
into neural excitations, and signal this information
from the joint via afferent nerves and dorsal root gan-
glia to the spinal cord. Sensory nerve endings in liga-
ments are classified according to Freeman and Wyke
(Freeman and Wyke, 1967) into four types, based on
Hagert et al. 3

Figure 1.  Innervation of the wrist joint and distribution of sensory nerve endings in the carpus. (A) Volar view of the wrist
where the radiovolar wrist ligaments have sparse innervation (yellow) and the ulnovolar ligaments have intermediate
innervation (blue). (B) Dorsal view of the wrist, the dorsal wrist ligaments consistently have rich and abundant innervation
(green).
SBRN: superficial sensory branch of the radial nerve; LACN: lateral antebrachial cutaneous nerve; PCB: palmar cutaneous branch of
the median nerve; AIN: anterior interosseous nerve; UN: ulnar nerve; DSUN: dorsal sensory branch of the ulnar nerve; PIN: posterior
interosseous nerve.

their typical morphology (Figure 2) and neurophysio- Proprioception and neuromuscular

logical traits (Table 1). The Ruffini ending (Figure
2(a)), a low-threshold sensory nerve ending respon-
sible for mediating joint position sense, is the pre-
dominant mechanoreceptor type found in the carpus
(Hagert et al., 2007; Lin et al., 2006).
Sensory nerve endings are found mostly close to
ligament insertions into bone, as well as in the epi-
ligamentous region of ligaments (Hagert et al., 2007;
Lin et al., 2006; Tomita et al., 2007) where they can
act as monitors of tension and force applied to the
ligament (Takebayashi et al., 1997).
The specific innervation pattern of wrist ligaments
has been studied in great detail (Hagert et al., 2004,
2005, 2007; Lin et al., 2006; Mataliotakis et al., 2009;
Petrie et al., 1997; Tomita et al., 2007). The degree of
innervation has been found to vary distinctly, with a
pronounced innervation in the DRC/DIC and in the
entire scapholunate ligament complex (Hagert et al.,
2004; Mataliotakis et al., 2009), an intermediate
innervation in the volar triquetrocapitate and tri-
quetrohamate ligaments (TqC/TqH, respectively), and
sparse innervation of the volar radial ligaments
(Hagert et al., 2007) (Figure 1).
control of the carpus
Unconscious proprioception and reflex
control
As mentioned, the unconscious proprioception sense
of neuromuscular joint control includes the anticipa-
tory control of muscles around a joint through so-
called feed-forward control, as well as the ability to
unconsciously maintain joint stability and equilibrium
(Lephart et al., 2000; Sjolander et al., 2002).
To date, the role of neuromuscular reflex control
has only been studied with regard to the scapholu-
nate ligament complex. In-vivo wrist joint proprio-
ception studies have been performed using
electromyography (EMG) (Hagert et al., 2009) and
sensory action potentials (Vekris et al., 2011). These
two studies have shown that the wrist has a distinct
pattern of reflex activation following disturbance of
the scapholunate ligament. Within 20 msec of joint
perturbation, antagonist muscles that control the
wrist are activated. In other words, if a wrist flexion
was performed at the time of ligament perturbation,
the wrist extensors were activated. This type of

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4 The Journal of Hand Surgery (Eur)

Figure 2.  Immunohistochemical staining of sensory nerve endings using low-affinity nerve growth factor receptor p75
(p75). (A) A Ruffini ending characterized by p75 immunoreactive (IR) dendritic nerve endings (arrowhead), a clearly visible
central axon without IR (arrow), and a thin, partial encapsulation of the corpuscle. (B) In contrast, the Pacini corpuscle this
has an onion-layered p75 IR capsule (arrowhead) and central axon (arrow). (C) The Golgi-like ending is larger, with an affer-
ent nerve fascicle and smaller, grouped corpuscles (arrowhead) within the Golgi-like ending. (D) Free nerve endings (arrow)
with a typical undulating appearance and p75 IR.
Original magnification 400×.

neuromuscular reaction is indicative of fast joint pro-
tective reflexes through monosynaptic spinal control
(Hagert et al., 2009).
If the SLIL was desensitized, by anaesthetizing the
PIN that innervates the ligament, a significant loss of
these joint protective reflexes was noted (Hagert and
Persson, 2010) (Figure 3). Similarly, sectioning of the
SLIL significantly reduced the afferent sensory action
potential signals through the median and radial nerve
(Vekris et al., 2011). These findings show that dener-
vation of the anterior and/or PINs will have adverse
effects on the unconscious neuromuscular control of
the wrist joint.
Neuromuscular control and
proprioception in carpal instabilities
When a normal wrist deviates from radial to ulnar
inclination, the entire proximal row rotates from flex-
ion to extension. This change in position is progres-
sive and smooth if the MC ligaments, mainly the most
proximal fibres of the triquetrum–hamate–capitate
ligament complex (TqC/TqH), the scapho–trapezio–
trapezoid (STT) ligament and the DRC, and the coor-
dinated contraction of the flexor carpi ulnaris and
extensor carpi ulnaris (ECU) are normally functioning
(Garcia-Elias, 2008). Since the TqC/TqH and DRC liga-
ments are among the most innervated ligaments in
the wrist, they are believed to provide important pro-
prioceptive information in this carpal motion.
PMCI is a kinematic dysfunction of the proximal
row that occurs when these supportive structures
become dysfunctional, either by rupture, attenuation,
or increased elasticity, together with poor proprio-
ception (Wolfe et al., 2012). In these individuals, the
proximal carpal row remains abnormally flexed when
changing from radial to ulnar inclination until it sud-
denly rotates into extension at the end of the move-
ment, sometimes with a visible and even audible
clunk (so-called ‘catch-up clunk’) (Garcia-Elias,
2008; Lichtman and Wroten, 2006; Wolfe et al., 2012).
The clinical MC shift test, described by Lichtman
et al., will usually reproduce the clunk (Lichtman
et al., 1981).

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Hagert et al. 5

Table 1.  Classification of mechanoreceptors in ligaments based on Freeman and Wyke (1967), modified by Hagert (2008),
outlining the morphology and function of the various sensory nerve endings found in the human hand.
(Reprinted by kind permission from Hagert E ‘Wrist Ligaments—Innervation Patterns and Ligamento-Muscular Reflexes’,
PhD thesis, Karolinska Institutet, 2008, p.24.).

Type Eponym/Name Characteristics Neurophysiological Role in joint IR patterns in

(descriptive) trait function mechanoreceptors
I Ruffini Coil-shaped. Partial Slowly adapting Static joint Central axon –
  (dendritic) encapsulation. Arborizing Low-threshold position PGP9.5, S100
  nerve branches with bulbous Changes Terminal nerve
terminals. 50–100 μm. in velocity/ branches – PGP9.5,
amplitude trkB
Incomplete capsule
– p75
II Pacini Rounded, ovular corpuscle. Rapidly adapting Joint Central axon –
  (lamellated) Thick lamellar capsule. Low-threshold acceleration/ PGP9.5, S100
20–50 μm. deceleration Thick capsule – p75
III Golgi-like Large, spherical. Partial Rapidly adapting Extreme ranges Terminal nerve
  (grouped encapsulation. Groups of High-threshold of joint motion branches – PGP9.5,
dendritic) arborizing and terminal S100, trkB
nerve endings. >150 μm. Incomplete capsule
– p75
IV Free nerve Varicose appearance, often A∂ fibres - fast Noxious, Axon – PGP9.5, trkB
  endings close to arterioles. Groups or C fibres - slow nociceptive,  
single fibres. inflammatory
V Unclassifiable Variable size, appearance, Unknown Unknown Incomplete capsule
and degree of encapsulation. – p75
  Variable IR pattern

PGP9.5: Protein Gene Product 9.5; S100: S-100 protein; trkB: tyrosine kinase receptor B; p75: low-affinity neurotrophic receptor p75; IR:
immunoreactions.

Figure 3.  Rectified electromyography chart from a flexor carpi ulnaris muscle, illustrating the electromyography excita-
tions seen following stimulation of the scapholunate interosseous ligament (A), and the loss of excitatory reactions follow-
ing desensitization of the posterior interosseous nerve (B).

Previous studies have analysed the role of forearm 2009; Salva-Coll et al., 2011a, 2011b, 2013). The
muscle control on the stability and motion of the car- results of these studies indicate that the muscles
pus (Leon-Lopez et al., 2013;Salva and Garcia-Elias, acting on the wrist have different roles in the

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6 The Journal of Hand Surgery (Eur)

Figure 4.  Illustration of the instability pattern seen in palmar midcarpal instability. (A) The proximal carpal row (PC) moves
into flexion due to distability of the triquetro–capito–hamate, scapho–trapezio–trapezoid, and dorsal radiocarpalligaments,
as well as inadequate wrist proprioception. (B) The extensor carpi ulnaris (ECU) causes a pronating (PRO) effect on the
distal carpal row, causing an extension moment on the triquetrum and reducing the proximal carpal row. The ECU thus
contributes neuromuscular stability in patients with palmar midcarpal instability.

neuromuscular control of the carpus, with an ability
to act as stabilizers or destabilizers depending on the
ligamentous integrity of the joint.
In a recent study by the same research group, the
role of neuromuscular control in simulated PMCI has
been analysed (Lluch Bergada et al., 2015). In this
cadaveric study, only one forearm muscle was found
to statistically counteract the excessive flexion of the
proximal row seen in PMCI, the extensor carpi ulnaris.
The ECU tendon has an oblique direction, from the
dorsum of the ulna to the anteromedial corner of the
fifth metacarpal. When this muscle contracts, aside
from causing an extension and ulnar deviation of the
wrist, it generates a pronation moment of the distal
carpal row (Leon-Lopez et al., 2013; Salva-Coll et al.,
2011a) (Figure 4). This ‘pronation’ describes a rota-
tion movement of the distal carpal row relative to the
radius that is different from a forearm rotation. Distal
row pronation generates an extensor moment to the
triquetrum, which in turn helps balancing the char-
acteristic flexion tendency of the proximal carpal row
seen in wrists with PMCI. The ECU thus has an impor-
tant role in neuromuscular stability of the MC joint.
Clinical applications of
proprioception
Hand therapy and proprioception
Several orthotics have been designed for the treat-
ment of carpal instabilities. In the instance of PMCI,
they are fabricated to force the pisiform dorsally and
try to prevent the wrist from collapsing into a volar
intercalated segment instability pattern (Chinchalkar
and Yong, 2004; Lichtman and Wroten, 2006; O’Brien,
2013). However, in patients with carpal instability due
to a benign hypermobility joint syndrome, in particu-
lar adolescents, static orthotic treatment should be
used with caution as to avoid loss of muscular
strength and control (Smith et al., 2014).
The results of the neuromuscular control of the
carpus in PMCI patients indicates that these are best
trained conservatively using a training programme to
strengthen the ECU (Lluch Bergada et al., 2015). As
the two main muscles inducing pronation of the distal
row are the ECU and flexor carpi radialis (FCR) (Salva
and Garcia-Elias, 2009), it may be useful to perform
alternating isometric exercises of both, and comple-
ment this with ‘reverse dart-throwing’ exercises; that
is, exercises emphasizing rotation of the wrist from
flexion–radial deviation to extension–ulnar deviation
(Garcia-Elias, 2008). Studies on the role of proprio-
ceptive training following ligament injury in knee and
ankle joints has suggested that the more efficient the
re-educational neuromuscular programme is, the
lesser the needs for surgery (Ageberg, 2002; Ageberg
et al., 2007; Eils and Rosenbaum, 2001). Overall, a
combination of proprioceptive treatment regimes
appears to yield the greatest improvement in senso-
rimotor control in both therapeutic (Aman et al.,
2014) and preventive rehabilitation strategies (Winter
et al., 2015). However, the exact role of wrist proprio-
ceptive training in carpal instabilities following injury
or in benign hypermobility joint syndrome needs to
be further elucidated (Valdes et al., 2014).
Surgery and proprioception
Should conservative treatment fail, surgery may be
necessary. Based on the role of proprioception and

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Hagert et al. 7
neuromuscular control of the wrist joint, there are a
number of issues with surgery that must be addressed.
Since the innervation of the wrist joint has been
shown to be important for an adequate neuromuscu-
lar reflex control (Hagert et al., 2009; Vekris et al.,
2011), and the fact that denervation of the joint radi-
cally diminishes these reflexes (Hagert, 2010a), any
surgery done in the carpus should be meticulously
performed to minimize damage to the innervation
of the wrist joint, using nerve-sparing surgical
approaches to the wrist (Hagert et al., 2010).
Similarly, arthroscopic electrothermal shrinkage
of the insufficient ligaments has been described as a
treatment of carpal instabilities (Hargreaves, 2014;
Mason and Hargreaves, 2007). Despite the reported
promising results, we believe that the beneficial
effect of creating a less elastic collagen tissue may
not compensate the fact of destroying the mechano-
receptors and nervous terminal endings contained in
these ligaments, and the consequent disturbance of
proprioception.
A recently published study has shown how increas-
ing the pronation tendency of the distal row by means
of a partial transfer of the extensor carpi radialis bre-
vis (ECRB) to the dorsum of the hamate, lead to an
improvement in 11 of 13 treated MC instability
patients (Ritt and de Groot, 2015). These findings
coincide with the known neuromuscular control of
the carpus, where induced pronation by the ECU can
reduce and alleviate the instability of the proximal
carpal row seen in PMCI.
Acknowledgements
The authors wish to express their gratitude to Dr Marc
Garcia-Elias for assistance with line drawings, to Professor
Manuel Llusá for anatomical contributions, and PhD stu-
dent Manuel Semisch for aid in photography.
Conflict of interests
None declared.
Funding
This research received no specific grant from any funding
agency in the public, commercial, or not-for-profit sectors.
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