Extraocular Proprioception Research Articles

A noninvasive electromagnetic perturbation approach to probe extraocular proprioception

Extraocular proprioception has been shown to participate in spatial perception and binocular alignment. Yet the physiological approaches used to study this sensory signal are limited because proprioceptive signaling takes place at the same time as visuomotor signaling. It is critical to dissociate this sensory signal from other visuomotor events that accompany eye movements. We present a novel noninvasive and quantifiable method for probing extraocular proprioception independent of other visuomotor processing by attaching a rare-earth magnet to a real-time model eye and placing an electromagnet <20mm from the eye. An electromagnet can increase or decrease angular displacements and velocities of the model eye. Electromagnetic activation rapidly affected (<2ms) the rotation kinematics of the eye, which were correlated linearly with both the current supply and the distance of the electromagnet relative to the eye. This method circumvented the constraints of conventional physiological manipulation of extraocular proprioception, such as manually or mechanically tugging on the eye ball. It can be applied to produce the discrepancy between the intended and the executed eye movements, so that proprioceptive reafference signals are dissociated from corollary motor discharges and other visuomotor events.

Surgery and visual function restoration for congenital idiopathic nystagmus with or without strabismus

Background The surgery for congenital idiopathic nystagmus has make great progression recent year,but the influence of surgery on visual function is closely concerned.Objective This work was to study the surgeries for congenital idiopathic nystagmus with or without strabismus and explore the effect of horizontal rectus muscle surgery on the visual function and ocular movement in congenital idiopathic nystagmus.Methods This was a case-observational study.Sixty cases with idiopathic congenital nystagmus were enrolled assigned to four groups as follows:The patients of group Ⅰ appeared the head postures of less than 15 ° and heterotropia less than 15△underwent extraocular proprioceptiou resection,and those of group Ⅱ presented with the head postures of less than 20° and heterotropia more than 15△ underwent extraocular proprioception resection and stabismus surgery.In the group Ⅲ,the patients had the head postures of more than 15° and heterotropia less than 15△ underwent Park's surgery and part of them underwent extraocular proprioception resection) and the cases in group Ⅳ were selected with the head postures of more than15° and heterotropia more than 15△ underwent Park' s surgery and strabismus surgery ( part of them underwent extraocular proprioception resection).Baseline and follow-up evaluations included the best distance and near corrected visual acuity,head posture,ocular movement and Titmus stereotest.The examination results were compared between before and after operation.Results One year after operation,monocular and binocular distance visual acuity improved significantly in all four groups ( monocular:t =6.00,8.94,11.76,16.41,P =0.00 ; binocular:t=4.81,P=0.01 ; t =6.27,4.25,4.18,P =0.00 ),but monocular and binocular near visual acuity improved significantly only in groups Ⅲ and Ⅳ after operation compared with before operation ( monocular:t=2.91,P=0.01 ; t =5.32,P =0.00 ; binocular:t =3.36,t =4.30,P =0.00 ).The compensatory head posture from 39 subjects was disappeared after operation,showing an evident difference between before and after surgery ( group Ⅲ:t =29.90,P=0.00;group Ⅳ:t=16.91,P=0.00).Strabismus were corrected rightly for 24 patients and undercorrection for 2 patients.( group Ⅱ:t =29.15,P =0.00 ; group Ⅳ:t =36.79,P =0.00 ).The binocular visual function of 23 cases with the age below 12 years were improved throughout the follow up duration ( t =12.06,P =0.00).Conclusions Park' s surgery,extraocular proprioception resection and strabismus corrective operation can improve the visual function and head posture in congenital idiopathic nystagmus patients. Key words: Eyeball nystagmus/congenital, Idiopathic; Strabismus; Park's surgery; Extraocular proprioception resection

A new surgery for congenital nystagmus: Effects of tenotomy on an achiasmatic canine and the role of extraocular proprioception

Purpose: Human eye-movement recordings have documented that surgical treatment of congenital nystagmus (CN) also produces a broadening of the null zone and changes in foveation that allow increased acuity. We used the achiasmatic Belgian sheepdog, a spontaneously occurring animal model of human CN and see-saw nystagmus (SSN), to test the hypothesis that changes induced by surgical interruption of the extraocular muscle afference without a change in muscle-length tension could damp both oscillations. Methods: An achiasmatic dog with CN and SSN underwent videotaping and infrared oculography in a sling apparatus and head restraints before and after all extraocular muscles (stage 1: 4 horizontal rectus muscles and stage 2 [4 months later]: 4 vertical rectus muscles and 4 oblique muscles) were surgically tenotomized and immediately reattached at their original insertions. Results: The dog had immediate and persistent visible, behavioral, and oculographic changes after each stage of this new procedure. These included damped CN and SSN, increased ability to maintain fixation, and increased periods of maintaining the target image on the area centralis over a broad range of gaze angles. Conclusions: Severing and reattaching the tendons of the extraocular muscles affect some as-yet-unknown combination of central nervous system processes producing the above results. This new procedure may prove effective in patients with CN with either no null, a null at primary position, or a time-varying null (due to asymmetric, (a)periodic, alternating nystagmus). We infer from our results in an achiasmatic dog that tenotomy is the probable cause of the damping documented in human CN after Anderson-Kestenbaum procedures and should also damp CN and SSN in achiasma in humans. It may also prove useful in acquired nystagmus to reduce oscillopsia. The success of tenotomy in damping nystagmus in this animal suggests that the proprioceptive feedback loop has a more important role in ocular-motor control than has been appreciated. Finally, we propose a modified bimedial recession procedure, on the basis of the damping effects of tenotomy. (J AAPOS 1999;3:166-82)

Organisation of reciprocal connections between trigeminal and vestibular nuclei in the rat.

In order to study the connection patterns between the sensory trigeminal and the vestibular nuclei (VN), injections of anterogradely and/or retrogradely transported neuronal tracers were made in the rat. Trigeminal injections resulted in anterogradely labelled fibres, with an ipsilateral preponderance, within the VN: in the ventrolateral part of the inferior nucleus (IVN), in the lateral part of the medial nucleus (MVN), in the lateral nucleus (LVN) with a higher density in its ventral half, and in the superior nucleus (SVN), more in the periphery than in the central part. Moderate trigeminal projections were observed in the small vestibular groups f, x and y/l and in the nucleus prepositus hypoglossi. Additional retrogradely labelled neurones were seen in the IVN, MVN, and LVN, in the same regions as those receiving trigeminal afferents. Morphological analysis of vestibular neurones demonstrated that vestibulo-trigeminal neurones are relatively small and belong to a different population than those receiving projections from the trigeminal nuclei. The trigeminovestibular and vestibulo-trigeminal relationships were confirmed by tracer injections in the VN. The results show that, in the VN, there is sensory information from facial receptors in addition to those reported from the neck and body. These facial afferents complement those from the neck and lower spinal levels in supplying important somatosensory information from the face and eye muscles. The oculomotor connections of the respective zones of the VN receiving trigeminal afferents suggest that sensory inputs from the face, including extraocular proprioception, may, through this pathway, influence the vestibular control of eye and head movements.

The effect of gravity on the resting position of the cat's eye.

We measured rotation (horizontal, vertical and torisonal) and translation (horizontal and vertical) of the paralysed cat's eye in response to 45 degrees steps of orientation presented in a pseudorandom order around the roll and pitch axes (with respect to the horizontal canals). During changes of position of the animal in the roll plane, the eyes rotated towards the lowest part of the orbit (left with left ear down; top when the cat was upside down, etc.) by an average of 0.55 degree. Changing orientation in the pitch plane evoked vertical rotations of +/- 1.42 degrees (upwards eye movement during forwards head pitch) and torsional rotations of +/- 1.3 degrees. All these rotations taken together suggest that the centre of mass is in front of, below and temporal to the centre of rotation. The eyes translated temporally (thus separating by 0.72 mm) during forward pitching and there was a small vertical displacement (0.23 mm) when the animal was upside down. These findings are discussed with respect to a possible role of the extraocular proprioception system.

Short- and long-term effects of transection of the ophthalmic nerve on optokinetic nystagmus in the rabbit

The role of extraocular proprioception in optokinetic nystagmus (OKN) was examined, using adult pigmented rabbits following transection of the ophthalmic branch of the trigeminal nerve. OKN was induced by rotation of a drum at an angular velocity of 0.85 and 3.7 degrees/s. The eye on the operated side showed a delay in the transition from the OKN-induced quick phase to the slow phase regardless of closure of the eye on either the operated or unoperated side. In addition, the eye on the operated side showed an anticompensatory response in the vestibulo-ocular reflex (VOR) with an unstable drift in the dark. The above abnormalities in OKN and VOR following rhizotomy disappeared after 1-1.5 months. These results suggest that proprioception in the extraocular muscle plays an important role in the fine regulations of eye position for gaze accuracy. The recovery demonstrated appears to be due to a compensatory mechanism in the central nervous system.

Neuronal stereoscopic processing following extraocular proprioception deafferentation

In adult cats, after section of extraocular muscle proprioceptive (EOMP) afferents during the 'critical period', most cortical area 17 cells loose their ability to discriminate changes in binocular spatial disparity. After unilateral section this loss depends on whether or not cortical cells modulate their responses to the presentation of sinusoidal gratings linearly. For 'modulated cells', this loss is due to a reduction of binocular suppression while for 'unmodulated cells', it is due to a selective increase in the variability of the binocular response. These permanent neural dysfunctions show that balance in EOMP inflow plays a crucial role in cortical processing of binocular depth discrimination.

Chapter 10 Eye, head and skeletal muscle spindle feedback in the elaboration of body references

Evidence is presented to support the notion that the sensory feedback originating in muscles is of major importance in the central elaboration of motor representation. The muscle spindle messages during movement and postural performance may be processed in order to elaborate continuously updated static and dynamic body references. These may then form the basis for the interpretation of retinal information in terms of spatial coordinates. The main arguments supporting this view are as follows. Experimental manipulation of muscle spindle proprioceptive feedback by tendon vibration induced segmental or postural kinaesthetic illusory movements in the direction of stretch of the vibrated muscles. By modifying the spatial distribution (agonists and/or antagonists), the frequency and the duration of the vibratory stimuli it is possible to induce simple or complex kinaesthetic illusions the parameters of which may be predicted. Microneurographic recordings confirmed that vibration rather selectively excited spindle Ia afferents, eliciting 1:1 driving up to 80-100 Hz. Moreover painless vibration, applied at increasing frequency (from 10 to 80 Hz) to either the medial, lateral, superior or inferior rectus of a subject's eye, was found to induce directional perceptual and motor effects which were closely related to the postural context. Likewise, the subjects reported illusory directional shifts of a visually fixed target in darkness during extraocular muscle vibration. These data suggest that extraocular proprioception contributes to the coding of eye, head and body position in relation to postural and environmental conditions. As with eye muscle stimulation, directional visual and postural effects were induced by vibration of neck and/or ankle postural muscles. These effects were found to summate when vibrations were applied simultaneously to the eye, neck and ankle muscles. The likely involvement of extraocular proprioception in interrelating body space with extrapersonal space in oriented behaviour is discussed.

A biophysical approach to the spatial function of eye movements, extraocular proprioception and the vestibulo-ocular reflex.

The eyeball and the extraocular muscles are used as a paradigm to design a linear spatial model of a single joint with a redundant set of muscles. On the basis of this model relations are derived between orientation, torque, motor commands, and proprioceptive signals. These relations show that the tenet underlying the tensorial interpretation of neural signals in sensorimotor systems does not have general validity. A mechanism is proposed to show how proprioception may play a role in optimizing the coordination of muscles during spatial tasks. Further, a new concept is suggested that allows one to predict the neural connectivities mediating the redundant spatial vestibulo-ocular reflex. This concept has the advantage of minimizing both sensorial error and motor effort.

Role of extraocular muscle proprioception in the development of depth perception in cats.

1. The ophthalmic branch of the trigeminal nerve (V1), which carries extraocular proprioceptive afferents, was sectioned unilaterally or bilaterally in kittens and adult cats. Depth perception was measured behaviorally in these sectioned cats, as well as in control cats. 2. For kittens that underwent unilateral V1 sections at 6-11 wk of age, postsurgical values of binocular depth perception--measured 1.5-3 mo later--were 2-3 times worse than in normal control animals. Cats that underwent unilateral V1 sections as adults, however, showed no postsurgical deficits in binocular depth perception. 3. For kittens that underwent bilateral V1 sections at 6.5-7.5 wk of age, similar longterm impairments were found in binocular depth perception. No impairment was found in two kittens bilaterally sectioned at 11.5 wk of age. A cat that underwent bilateral sections as an adult also showed no binocular depth perception deficits. 4. Although these behavioral effects were observed only when unilateral and bilateral V1 sections were performed up to a certain age in development, they differed in two ways. 1) Imbalance of extraocular proprioceptive inflow produced by unilateral section had a deleterious effect at an age when the final adult level had been reached. At that stage, complete suppression of inflow produced by the bilateral section failed to impair the final level of binocular performance. 2) Short-term effects observed during the week following the section appeared in bilaterally operated animals as a transient freezing of the presurgical binocular performance whatever the age of the section during the sensitive period. In contrast, short-term effects produced by unilateral section were found to be age dependent: a progressive slowing down in the normal rate of improvement of binocular thresholds was observed following a section performed at 5 wk of age; an arrest in development was found when surgery was done at 6-7 wk of age. A significant impairment appeared within 2 days when the section was performed at 11 wk of age. 5. In all experimental kittens, monocular depth perception thresholds were unaffected or impaired only to a minor extent (less than 15% change) following the unilateral or bilateral section. In unilaterally operated kittens, there were no consistent differences associated with the side of the section. 6. A sham-operated kitten, in which the V1 was visualized but not cut, showed no impairments in binocular or monocular depth perception.(ABSTRACT TRUNCATED AT 400 WORDS)

Role of extraocular proprioception in the orienting behaviour of cats.

We investigated the effects of unilateral deafferentation of extraocular proprioception on the orienting behaviour of cats. The ophthalmic branch of the Vth cranial nerve, in which most of the extraocular proprioceptive fibers are known to run, was cut unilaterally in adult cats. The animals had been previously trained to jump from a start box to a luminous target at various possible locations in the right or left visual hemifield. The postsurgical orienting performance of the animals, evaluated from the difference between landing position and position of the target, differed from the presurgical performance. The postsurgical errors were typically: (1) ipsiversive to the side of the section, (2) usually of a larger magnitude in the hemifield contralateral to the section, (3) present in binocular as well as in monocular viewing conditions and approximately of the same magnitude for jumps guided by either eye. These findings indicate that extraocular proprioception plays a role in the orienting behaviour of cats.

The information basis in the perception of velocity

This is a theoretical-empirical contribution to the controversy about whether perceived velocity is a consequence of the interaction between phenomenal space and time, or an independent attribute directly extracted from the physical time and space information of moving stimulation. The paper includes the following problems. (a) After a brief methodological review, the quantitative relationship between perceived velocity, space and time is re-interpreted and its numerical validity evaluated. (b) It is contended that perceptions of velocity, space and direction of movement are parallel processes which occur on the basis of the information extracted directly from the space and time variables of motion stimulus. And, finally, (c) a new line of argument is advanced in support of the thesis that even in pursuit eye movements, information about motion is transmitted visually rather than via extraocular proprioception, and in this connection some questions concerning the control theoretical models of smooth pursuit eye movements are raised.

Somatotopic representation of eye muscle proprioception within the superior colliculus of the lamb

A somatotopic organization of the extraocular muscle proprioceptive afferent projection was observed in the superior colliculus of the lamb. Units responding to the stretching of each extraocular muscle were recorded along the dorsoventral axis in the superficial layers of the superior colliculus as follows: the inferior rectus and the inferior oblique were represented in the most dorsal layer of the superior colliculus, the superior rectus, and the superior oblique muscles in the intermediate layers, and the lateral and the medial recti in the deepest layers. The superior collicular sites influenced by stretching the extrinsic eye muscles could be activated by single-shock electrical stimulation of the cellular pool of the dorsal part of the semilunar ganglion and by stimulation of both the nucleus principalis and the pars oralis of the trigeminal nuclear complex ipsilaterally, where the eye muscle proprioception is represented. Our findings indicate for the first time that in the superior colliculus a somatotopic map of extraocular afferent input is present; the significance of this projection is discussed in relation to the control of head movements and extraocular proprioception.

Development of visual cortical orientation specificity after dark-rearing: Role of extraocular proprioception

Six-week-old dark reared kittens exposed to light for 6 h: (1) with head and body tightly cast into plaster; or (2) free to move around in the animal room. A few days before the visual experience, the opthalmic branch of the 5th nerve was severed bilaterally in experimental kittens, in order to suppress most of the proprioceptive afferents from extraocular muscles. Electrophysiological analysis of the properties of the receptive fields of visual cortical cells shows that only 6% (group 1) and 11% (group 2) of the cells were selective to orientation as opposed to 67% (group 1) or 32% (group 2) observed in the non-operated kittens.

Does Extraocular Proprioception Influence the Development of Visual Processes and the Oculomotor System?

Publisher Summary This chapter reviews the functions of extraocular proprioceptors, for eye motor control and position sense, and for visual processes. The participation of extraocular proprioceptors has been considered in fixation micronystagmus, in correcting overshoot of eye movements and oscillation, and as negative feedback for small deviations from fixation. The chapter points out that despite the fact that a monosynaptic stretch reflex has never been found, some reflex actions of extraocular muscles stretch receptors exist. The extraocular proprioceptors are involved in oculomotor control through their projections to structures such as cerebellum and superior colliculus. In particular conditions, these extraocular proprioceptors provide a conscious position sense. The chapter also reviews some observations that have led to the assumption that extraocular proprioceptors also have a function in visual processes. Recent experiments that provide evidence for the role of extraocular proprioceptors in the development of orientation specificity in visual cortical neurons are reported.

Planar relationships of semicircular canals in the cat.

Planar relationships of semicircular canals in the cat.

Cerebellar representation of extraocular and masticatory proprioception

Cerebellar representation of extraocular and masticatory proprioception

Extraocular proprioception in electrically induced eye movements.

Ocular movements evoked by stimulation of brain-stem sites in the feline encéphale isolé have been analyzed in an attempt to demonstrate an extraocular proprioceptive mechanism. Procedures designed to reduce extraocular proprioceptive input to the central nervous system included tenotomy of the muscles of one eye, procaine block of one or both Gasserian ganglia, and acute cerebellectomy. None of these procedures resulted in a consistent alteration in accuracy of the induced oculomotor responses. Immobilization of one eye, however, significantly reduced the accuracy of the freely moving eye in assuming the same final position with repeated stimulation of one site. All procedures tested, including occipital lobectomy, resulted in a significant shift of the final position reached by the eyes in response to repeated stimulation of one site. While the shift, unlike the decrease in accuracy seen with immobilization, cannot be interpreted as evidence for an extraocular proprioceptive mechanism, it is discussed with reference to the significance of the ‘goal’ position obtained by repeated stimulation of one site at constant stimulus parameters.