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Show 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. (/ Neuro- Ophthalmol 2006; 26: 123- 127) The 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 ( non-visual) 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 OYN, 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 OYN, United Kingdom; E- mail: clifford. weir@ northglasgow. scot. nhs. uk 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 ofhuman 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 J Neuro- Ophthalmol, Vol. 26, No. 2, 2006 123 J Neuro- Ophthalmol, Vol. 26, No. 2, 2006 Weir 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 memory-guided 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 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 124 © 2006 Lippincott Williams & Wilkins Extraocular Muscle Proprioception J Neuro- Ophthalmol, Vol. 26, No. 2, 2006 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 best-corrected 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 follow-up 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. 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 trigeminal-oculomotor 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 125 J Neuro- Ophthalmol, Vol. 26, No. 2, 2006 Weir 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. 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