STATE OF
THE
ART
Proprioception in Extraocular Muscles
Clifford R. Weir, BSc (Hons), MD, FRCOphth
Abstract: Human extraocular muscles are richly
endowed with sensory receptors. The precise role of
afferent signals derived from these proprioceptors in
ocular motor control and spatial localization has been
the subject of considerable debate for more than
a century. Laboratory-based and clinical studies have
increasingly suggested that proprioceptive signals
from extraocular muscles influence visuomotor
behavior.
(J Neuro-Ophthalmol 2006;26:123–127)
T
he coordinated movement of the eyes is essential for
effective vision and visually-guided behavior. For this
to occur accurately, the brain must ‘‘know’’ the direction of
gaze. If the eyes were fixed in the orbits, retinal (visual)
information would, by itself, be sufficient to tell us where
we are looking. However, the eyes and the visual world
move, and under these circumstances, extraretinal (nonvisual) information is required to determine gaze direction.
The source of this extraretinal signal has generated
a great deal of controversy over the last century. For many
years, it was accepted that central monitoring of the outflow
(efferent) innervation sent to the extraocular muscles during
eye movements was exclusively responsible for this
extraretinal eye position signal (1). The outflow hypothesis,
attributed to Helmholtz (2), has also been described as
‘‘efference copy’’ (3) and ‘‘corollary discharge’’ (4).
Although there is abundant evidence supporting the
outflow hypothesis as the predominant source of the
extraretinal eye position signal (1,5), there is increasing
evidence that inflow (afferent) information may also
contribute to the extraretinal eye position signal (6–9).
The inflow hypothesis, first attributed to Sherrington (10),
was dismissed for many years, but recently there has been
evidence of a non-visual afferent feedback signal, most
likely from extraocular muscle proprioceptors. Much of the
Tennent Institute of Ophthalmology, Gartnavel General Hospital,
Glasgow G12 0YN, United Kingdom.
Address correspondence to Clifford R. Weir, BSc (Hons), MD,
FRCOphth, Tennent Institute of Ophthalmology, Gartnavel General
Hospital, 1053 Great Western Road, Glasgow G12 0YN, United Kingdom;
E-mail: clifford.weir@northglasgow.scot.nhs.uk
J Neuro-Ophthalmol, Vol. 26, No. 2, 2006
work on this subject relates to animal studies (8), and
perhaps such studies have little relevance to everyday
clinical problems. However, recent human studies have
postulated a clinical role for extraocular muscle
proprioception.
EXTRAOCULAR MUSCLE RECEPTORS
The sensory innervation of the extraocular muscles is
a contentious issue. Two distinct types of sensory receptors
have been identified within human extraocular muscles,
namely muscle spindles (11,12) and palisade endings
(myotendinous cylinders) (13), but their precise function is
not fully understood. The other main sensory receptors
found within skeletal muscle, Golgi tendon organs, have as
yet not been identified within human extraocular muscles,
although they have been described in monkeys (14).
Muscle spindles are found within the proximal and
distal regions of human infant and adult extraocular muscles
and are located at the junction of the orbital and global layers
(12,15). Although they are found at a density similar to that
of spindles in hand and neck muscles, suggesting a role in
fine motor control, they also show peculiar features that have
led some authors to wonder about their ability to generate
a proprioceptive signal (16,17).
Palisade endings, a class of muscle receptor found
exclusively within extraocular muscles, including those of
humans, are located at the distal myotendinous junction of
the multiply innervated non-twitch fibers of the global layer
(18). They may be the principal source of proprioceptive
feedback from extraocular muscles (19,20), although as
with muscle spindles, this has been disputed (21).
Studies in the monkey suggest that proprioceptive
signals ascend from the extraocular muscles to the central
processing structures via the trigeminal nucleus (22).
However, as with other aspects of extraocular muscle
proprioception, this issue is in dispute. The precise pathway
in humans has yet to be established (8).
EXTRAOCULAR MUSCLE
PROPRIOCEPTION AND OCULAR
MOTOR CONTROL
There is increasing evidence that extraocular
muscle afferent signals can influence certain types of eye
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movements in humans (8,9,23). This viewpoint is supported by experimental and clinical studies.
Experimental Studies
Two specific experimental techniques have been
described for modifying the presumptive proprioceptive
signal from the extraocular muscles: 1) vibration of the
muscle tendon; and 2) using a suction contact lens to passively rotate or impede the movement of one eye. Although
it could be argued that neither technique reproduces the
pattern of proprioceptive input that may be encountered
during normal eye movements, each provides a means of
investigating the effect of manipulating afferent input on
ocular motor behavior.
It is generally accepted that human skeletal muscle
spindles can be stimulated by means of a vibrating stimulus
(24). It has therefore been suggested that when such
a stimulus is applied to the extraocular muscles, it simulates
stretching of the vibrated muscle (25), thereby modifying
the afferent stimulus. Lennerstrand et al (26) reported that
after vibration of a single extraocular muscle, the vertical
and horizontal position of the non-stimulated eye could be
altered. For example, vibration of the inferior rectus in one
eye of a normal subject induced an upward movement of
both eyes; vibration of the lateral rectus caused an outward
movement of the contralateral eye. These findings, however, were in contrast to those of Velay et al (27), who
observed a downward movement only of the vibrated eye
when the inferior rectus was vibrated and no change in eye
position when the lateral rectus was vibrated.
At first glance, the discrepancy between these studies
is difficult to explain. However, given the close proximity of
the inferior rectus muscle to the inferior oblique muscle,
perhaps slight differences in experimental technique could
have affected the respective stimulation of these muscles,
which in turn could have affected the eye movement. It is
more difficult to explain the difference in the observed
effects on the lateral rectus muscle. Allin et al (28) used
a similar technique and showed an effect on memoryguided but not visually-guided saccades. They suggested
that when retinal information is constantly available, an
extraretinal signal is not required to program an accurate
saccade.
The use of a contact lens held in place by gentle
suction to passively rotate or impede the movement of one
eye has also been proposed as a means of altering
proprioceptive feedback from the extraocular muscles
(29). It potentially affects the afferent input from all six
extraocular muscles simultaneously rather than the input
from a single muscle (as occurs with vibration). Whether
the modified signal produced by this technique resembles
that occurring during voluntary eye movements is debatable
(6). Nevertheless, it does provide the opportunity to
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Weir
manipulate afferent signals from one eye and assess the
effect on the contralateral eye under different experimental
conditions. With the use of this technique, alterations have
been observed in eye alignment (30), visually-guided
saccades (31), and smooth pursuit (32,33). It would be
interesting to repeat these experiments in patients with
various ocular motility disorders to see if the findings differ.
Based mainly on animal studies, Buttner-Ennever
et al (20,23) have suggested that each layer of the extraocular muscles has its own type of sensory receptor to
generate afferent signals, with the orbital layer utilizing
muscle spindles and the global layer relying on palisade
endings. These investigators also suggest that sensory
signals from palisade endings form part of a proprioceptive
feedback network that modulates the non-twitch motor
neurons that innervate the slow non-twitch extraocular
muscles fibers.
Clinical Studies
Perhaps of more relevance to clinical practice are
observations relating to patients with strabismus. Corsi et al
(34) noted an altered receptor structure (possibly palisade
endings) when analyzing resected rectus muscle specimens
from 11 patients who had undergone surgery for congenital
strabismus. They speculated that deranged proprioceptive
function contributed to the cause of the strabismus. However, they also acknowledged that such changes could also
be the result of strabismus.
Mitsui (35) described the ‘‘magician’s forceps
phenomenon,’’ in which he found that in strabismus
patients under general anesthesia, passively adducting the
dominant eye with forceps caused the deviating eye to
assume a normal position. This phenomenon was attributed
to an imbalance of proprioceptive input from the two eyes.
However, this interpretation has been questioned (36).
More recently, modification of proprioceptive feedback from the extraocular muscles has been described as
a means of treating congenital nystagmus. Hertle et al (37)
reported their findings from a cohort of ten adult patients
with different subtypes of congenital nystagmus undergoing tenotomies of all four horizontal rectus muscles. This
procedure involves detaching all four horizontal rectus
muscles and reattaching them at their original insertion
sites. Visual acuity and the Nystagmus Acuity Function
eXpanded (NAFX) were assessed before surgery and for
up to one year after surgery. (NAFX, a measure of the
foveation ability for any nystagmus waveform (38), is
essentially an assessment of the potential visual acuity of
patients with poor foveation.) One year after surgery, nine
of ten patients were reported to have an increase in their
NAFX. The average NAFX increase was 28% for the
congenital nystagmus group (a potential increase of
one Snellen line); it was 58% for the congenital
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Extraocular Muscle Proprioception
nystagmus/asymmetric periodic alternating nystagmus
group (a potential increase of 2.5 Snellen lines). However,
formally-measured binocular acuities (Early Treatment
Diabetic Retinopathy Study letter change) only revealed
an increase in visual acuity in five of ten patients. A
questionnaire assessment of visual health status showed an
improvement in nine of ten patients, although there was
significant variability between patients.
These investigators (39) have recently reported
improvement of visual function in four of five children
with infantile nystagmus undergoing tenotomies of their
horizontal rectus muscles. Both visual acuity and NAFX
were assessed before surgery and up to one year after
surgery. Four of five patients showed an increase in bestcorrected binocular visual acuity, equating to approximately one line of minimal angle of resolution (logMAR)
acuity after surgery. The visual acuity of the fifth patient
was unchanged. In two of three patients in whom accurate
NAFX data were collected, average NAFX values increased
by approximately 20%, although there was a significant
variation between the two subjects.
In each of these studies, the authors speculate that the
observed effects are due to changes in afferent information
derived from the extraocular muscles, proprioceptors being
the most likely source of such information. They argue that
the effect of tenotomy on visual performance may be
interruption of the afferent proprioceptive loop involved in
maintaining resting muscle tension. However, Miura et al
(40,41) have questioned this interpretation as their followup studies suggested that the four-muscle tenotomy procedure had no significant effect on the waveform structure
or the underlying mechanism of the congenital nystagmus.
It would be interesting to repeat the above studies on greater
numbers of patients and to assess the effect of this treatment
in different types of acquired nystagmus.
EXTRAOCULAR MUSCLE
PROPRIOCEPTION AND SPATIAL
LOCALIZATION
Determining the position of targets in surrounding
visual space (spatial localization) is an important aspect of
visual function, and as with ocular motor control, it requires
the integration of visual and non-visual information.
Although it has been suggested that extraocular muscle
proprioception may not be the predominant source of this
non-visual signal, under certain circumstances, it may play
a role (7,8). Such a claim is based on findings from two
different sources: 1) experimental studies involving normal
and strabismic subjects in whom the afferent signal has
been transiently manipulated; and 2) patients in whom the
afferent input has been modified either pathologically or
surgically.
J Neuro-Ophthalmol, Vol. 26, No. 2, 2006
Experimental Studies
As with the experimental studies involving ocular
motor control described earlier in this article, passive eye
rotation and extraocular muscle vibration have been used to
assess the effect of proprioception on spatial localization.
Several studies have shown that vibration of individual
extraocular muscles can cause the illusion of target
movement under certain viewing conditions (25,42). For
example, vibration of the inferior rectus muscle of one eye
produced an apparent upward movement of the object being
viewed and errors of spatial perception when trying to
accurately point to the object (42). It was concluded that
proprioceptive receptors in the extraocular muscles were
activated by the vibrating stimulus, thereby signaling an
apparent stretch of the muscle. The subject erroneously
interprets this as a change in the position of the eye, which
in turn results in the illusion of target movement. A similar
study carried out on normal subjects and strabismic patients
has suggested that proprioceptive activation can influence
spatial localization in both groups (43). Gauthier (29,30)
has also demonstrated that passively rotating one eye can
cause errors in spatial perception when viewing with the
contralateral eye.
Patient Observations
Observations in different groups of patients with
dysfunction of the trigeminal nerve, which is thought to
carry the sensory innervation of the extraocular muscles,
have added weight to the belief that proprioception can
influence spatial perception. For example, several patients
who have undergone surgical sectioning or thermocoagulation for trigeminal neuralgia have impaired accuracy in
visually-guided eye movements (44,45). Patients with
active herpes zoster ophthalmicus also demonstrate errors
in spatial localization (46). Lewis and Zee (47) reported
their findings from a patient with congenital trigeminaloculomotor synkinesis in whom contraction of the left
lateral pterygoid muscle resulted in an adduction movement
of the left eye caused by innervation of the left medial
rectus by the trigeminal nerve. They observed significant
errors in spatial perception, and as they believed the normal
oculomotor efferent command was unchanged, they
attributed the change to an alteration in proprioception.
However, until the actual sensory pathway from the
extraocular muscles in humans is fully elucidated, these
conclusions will remain speculative.
Steinbach et al (48) first reported differences in
spatial localization after strabismus surgery and later
suggested that those undergoing recessions were affected
to a lesser extent than those undergoing myectomies (49).
They speculated that this difference was due to the fact that
the recession procedure was less damaging than the
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myectomy procedure to the palisade endings. More recently
it has been shown that a shift in spatial localization occurs
among children with fully accommodative esotropia in
viewing targets when their eyes are aligned (wearing
glasses) as compared to viewing the same targets when
there is a manifest deviation (not wearing glasses) (50).
Their perception of the position of the viewed target shifted
in the direction of the non-deviating eye when their ocular
misalignment was manifest. Although the observed changes
were small, they were reproducible. It was speculated that
these changes were due to an alteration in extraretinal eye
position information, derived in part from extraocular muscle proprioception, which helps to specify visual direction.
Other forms of ophthalmic surgery involving
manipulation of the extraocular muscles have been shown
to affect spatial localization. In a small group of patients
undergoing retinal detachment surgery in which an
encircling band was placed beneath the muscles, Campos
et al (51) described errors in spatial perception when viewing with the operated or unoperated eye. A more extensive
study investigated spatial localization in two groups of
patients undergoing different types of surgery for primary
rhegmatogenous retinal detachment (52). The results
showed that patients undergoing conventional external
scleral buckling procedures, and to a lesser extent, vitrectomy procedures, demonstrated significant short-term
changes in spatial perception when viewing targets with
their unoperated eyes. The findings from both studies have
been interpreted as due in part to an alteration in extraocular
muscle proprioception derived from the operated eye as
a consequence of the surgical procedure.
CONCLUSION
There is increasing scientific and clinical evidence
that a non-visual afferent signal, most likely to be derived
from extraocular muscle proprioceptors, can under certain
conditions influence visuomotor behavior. It may well be
that for the majority of individuals with normal visual
function and normal oculomotor systems that vision itself,
combined with efference copy, is sufficient to determine
eye position. In such individuals, extraocular muscle proprioception may have little to contribute to the control of
eye movements and the representation of visual space.
However, under certain circumstances of reduced or impaired vision or in those with ocular motility disorders,
afferent feedback from the extraocular muscles might
assume greater significance. This is of potential importance
in patients with strabismus who are often amblyopic, as
their greater reliance on proprioceptive feedback is likely to
be compromised further after surgery, which inevitably
involves the very areas of the muscles richly endowed with
sensory receptors.
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Although much needs to be done to fully understand
the sensory innervation of the extraocular muscles, it is
difficult to accept that a complex system such as that
controlling the oculomotor apparatus would not utilize all
available information to meet its exacting and demanding
needs. Perhaps the clinical relevance of extraocular muscle
proprioception has been overlooked for too long and
deserves further scrutiny.
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