The directional effects of passive eye movement on the directional visual responses of single units in the pigeon optic tectum

 We have investigated the visual responses of 184 single units located in the superficial layers of the optic tectum (OT) of the decerebrate, paralysed pigeon. Visual responses were similar to those reported in non-decerebrate preparations; most units responded best to moving visual stimuli, 18% were directionally selective (they had a clear preference for a particular direction of visual stimulus movement), 76% were plane-selective (they responded to movement in either direction in a particular plane). However, we also found that a high proportion of units showed some sensitivity to the orientation of visual stimuli. We examined the effects of extraocular muscle (EOM) afferent signals, induced by passive eye movement (PEM), on the directional visual responses of units. Visual responses were most modified by particular directions of eye movement, although there was no unique relationship between the direction of visual stimulus movement to which an individual unit responded best and the direction of eye movement that caused the greatest modification of that visual response. The results show that EOM afferent signals, carrying information concerning the direction of eye movement, reach the superficial layers of the OT in the pigeon and there modify the visual responses of units in a manner that suggests some role for these signals in the processing of visual information. Received: 17 June 1996 / Accepted: 29 April 1997     

Effects of viewing distance on the responses of horizontal canal-related secondary vestibular neurons during angular head rotation.

Effects of viewing distance on the responses of horizontal canal-related secondary vestibular neurons during angular head rotation. The eye movements generated by the horizontal canal-related angular vestibuloocular reflex (AVOR) depend on the distance of the image from the head and the axis of head rotation. The effects of viewing distance on the responses of 105 horizontal canal-related central vestibular neurons were examined in two squirrel monkeys that were trained to fixate small, earth-stationary targets at different distances (10 and 150 cm) from their eyes. The majority of these cells (77/105) were identified as secondary vestibular neurons by synaptic activation following electrical stimulation of the vestibular nerve. All of the viewing distance-sensitive units were also sensitive to eye movements in the absence of head movements. Some classes of eye movement-related vestibular units were more sensitive to viewing distance than others. For example, the average increase in rotational gain (discharge rate/head velocity) of position-vestibular-pause units was 20%, whereas the gain increase of eye-head-velocity units was 44%. The concomitant change in gain of the AVOR was 11%. Near viewing responses of units phase lagged the responses they generated during far target viewing by 6-25 degrees. A similar phase lag was not observed in either the near AVOR eye movements or in the firing behavior of burst-position units in the vestibular nuclei whose firing behavior was only related to eye movements. The viewing distance-related increase in the evoked eye movements and in the rotational gain of all unit classes declined progressively as stimulus frequency increased from 0.7 to 4.0 Hz. When monkeys canceled their VOR by fixating head-stationary targets, the responses recorded during near and far target viewing were comparable. However, the viewing distance-related response changes exhibited by central units were not directly attributable to the eye movement signals they generated. Subtraction of static eye position signals reduced, but did not abolish viewing distance gain changes in most units. Smooth pursuit eye velocity sensitivity and viewing distance sensitivity were not well correlated. We conclude that the central premotor pathways that mediate the AVOR also mediate viewing distance-related changes in the reflex. Because irregular vestibular nerve afferents are necessary for viewing distance-related gain changes in the AVOR, we suggest that a central estimate of viewing distance is used to parametrically modify vestibular afferent inputs to secondary vestibuloocular reflex pathways.     

Afferent signals from cat extraocular muscles in the medial vestibular nucleus, the nucleus praepositus hypoglossi and adjacent brainstem structures

The responses of single units in the vestibular nuclei, nucleus praepositus hypoglossi and in the brainstem, deep and posterior to the abducens nucleus, were studied in anaesthetized, paralysed cats. Natural vestibular stimulation was provided by horizontal, sinusoidal oscillation of the animal and extraocular muscle afferents of the ipsilateral eye were activated either by passive eye-movement or by electrical stimulation of the inferior oblique branch of the oculomotor nerve in the orbit. Unit responses to vestibular and/or orbital stimuli were examined in sets of peristimulus time histograms interleaved in time. Of 127 units exposed to both types of stimulus, 40 (32%) responded only to vestibular input; 46 (32%) were affected only by the orbital afferent signal and 19 (15%) received both signals; the remaining 22 units (17%) were discarded because they had polymodal (usually somaesthetic) input. Of the 93 units whose recording sites were determined histologically, 24 were in the medial vestibular nucleus, 16 in the n. praepositus hypoglossi and 45 in the magnocellular nucleus of the reticular formation posterior and deep to the abducens nucleus. In these three nuclei 19 units in total were found which carried the orbital proprioceptive afferent signal and also responded to horizontal vestibular stimulation. The input from the eye muscles proved able to modify the vestibular response by adding excitation or inhibition or both. Effects of the orbital signal were generally phasic. About half of the units which responded to passive eye-movement showed statistically significant differences between their responses to horizontal and to vertical eye-movement. We have shown previously that signals from extraocular muscle proprioceptors reach the vestibulo-oculomotor system in an amphibian and a bony fish; the present experiments show that this is the case in a mammal also. The fact that the visual and visuomotor behaviour of these three species is very different suggests that the proprioceptive signal may play some rather fundamental role in the vestibulo-ocular system. The principal interest of the present results is that they demonstrate that units in the central vestibular system of the cat, in structures which are known to be concerned in oculomotor control, and particularly in the organization of horizontal eye-movement, receive an afferent signal from the eye muscles during passive eye-movement. These brainstem nuclei are known to receive various combinations of input from the vestibular and visual systems and of signals which represent neck movement and eye position and velocity.(ABSTRACT TRUNCATED AT 400 WORDS)     

Input from proprioceptors in the extrinsic ocular muscles to the vestibular nuclei in the giant toad,Bufo marinus

Summary Extracellular unit records were made from the left brain stem of decerebrate, paralysed giant toads (Bufo marinus) during passive movement of the ipsilateral eye. Units in the vestibular nuclear complex (VN) were identified by their short-latency responses to electrical stimulation of the anterior branch of the ipsilateral VIII cranial nerve.Of 58 units in the region of VN, as judged from field potentials to VIII nerve stimulation, fourteen gave phasic excitatory responses to passive movement of the eye and were also identified as vestibular nuclear units. A further twelve units which responded to eye-movement could not be assigned to VN; the remaining 32 units were in VN but did not respond to passive eye-movement. Also, of 16 units whose recording sites were identified histologically in the VN complex, 11 gave responses to vestibular nerve stimulation and to passive eye-movement and 5 responded to eye-movement only.Control experiments eliminated auditory, visual and cutaneous sources for the signal produced by passive eye-movement; thus, the signal must have arisen from intraorbital proprioceptors. Units in VN were also found which were excited by electrical stimulation of the intraorbital part of the fourth (trochlear) nerve; this provides strong evidence that proprioceptors in the extrinsic ocular muscles (EOM) are included in the receptors which provide the signal to VN during passive eye-movement.The effects of vestibular stimulation and of passive eye-movement were found to interact upon units in VN. When passive eye-movement and vestibular stimulation were paired the response to the second stimulus was significantly reduced over a range of interstimulus intervals.The conclusions are that orbital proprioceptive signals, including those from the EOM, project to the vestibular nuclei in the toad and, there, are able to influence processing of vestibular afferent signals. We suggest, therefore, that orbital proprioceptive signals may play a part in oculomotor control. The significance of the results is discussed in relation to the strategic position of the VN in the oculomotor control system.     

Effects of viewing distance on the responses of vestibular neurons to combined angular and linear vestibular stimulation.

Effects of viewing distance on the responses of vestibular neurons to combined angular and linear vestibular stimulation. The firing behavior of 59 horizontal canal-related secondary vestibular neurons was studied in alert squirrel monkeys during the combined angular and linear vestibuloocular reflex (CVOR). The CVOR was evoked by positioning the animal's head 20 cm in front of, or behind, the axis of rotation during whole body rotation (0.7, 1.9, and 4.0 Hz). The effect of viewing distance was studied by having the monkeys fixate small targets that were either near (10 cm) or far (1.3-1.7 m) from the eyes. Most units (50/59) were sensitive to eye movements and were monosynaptically activated after electrical stimulation of the vestibular nerve (51/56 tested). The responses of eye movement-related units were significantly affected by viewing distance. The viewing distance-related change in response gain of many eye-head-velocity and burst-position units was comparable with the change in eye movement gain. On the other hand, position-vestibular-pause units were approximately half as sensitive to changes in viewing distance as were eye movements. The sensitivity of units to the linear vestibuloocular reflex (LVOR) was estimated by subtraction of angular vestibuloocular reflex (AVOR)-related responses recorded with the head in the center of the axis of rotation from CVOR responses. During far target viewing, unit sensitivity to linear translation was small, but during near target viewing the firing rate of many units was strongly modulated. The LVOR responses and viewing distance-related LVOR responses of most units were nearly in phase with linear head velocity. The signals generated by secondary vestibular units during voluntary cancellation of the AVOR and CVOR were comparable. However, unit sensitivity to linear translation and angular rotation were not well correlated either during far or near target viewing. Unit LVOR responses were also not well correlated with their sensitivity to smooth pursuit eye movements or their sensitivity to viewing distance during the AVOR. On the other hand there was a significant correlation between static eye position sensitivity and sensitivity to viewing distance. We conclude that secondary horizontal canal-related vestibuloocular pathways are an important part of the premotor neural substrate that produces the LVOR. The otolith sensory signals that appear on these pathways have been spatially and temporally transformed to match the angular eye movement commands required to stabilize images at different distances. We suggest that this transformation may be performed by the circuits related to temporal integration of the LVOR.     

Contribution of vestibular nerve irregular afferents to viewing distance-related changes in the vestibulo-ocular reflex

The contribution of irregular vestibular afferents to viewing distance-related changes in the angular vestibulo-ocular reflex (AVOR) and combined angular and linear VOR (CVOR) was studied in squirrel monkeys trained to fixate earth-stationary targets that were near (10 cm) and distant (90–170 cm) from their eyes. Perilymphatic anodal galvanic currents were used to reversibly silence irregular vestibular afferents for periods of 4–5 s during the AVOR and CVOR evoked by 0.5- to 4-Hz sinusoidal rotations (6–20°/s peak velocity) or 250–400°/s² acceleration steps. The direction and magnitude of linear translation were changed by positioning the monkeys at different distances off the axis of turntable rotation. The effects of irregular afferent galvanic ablation (GA) on viewing distance-related changes in the AVOR were studied in four animals. Viewing distance-related changes in the AVOR could not always be evoked and were frequently small in amplitude. GA reduced viewing distance-related change in the AVOR by an average of 64% when it was present. Thus vestibular irregular afferents appear to play an important and necessary role in viewing distance-related changes in the AVOR – on those occasions when the changes occur. Viewing distance-related changes in the CVOR were large and reliably evoked. GA had very little effect on the gain or phase of viewing distance-related changes in the CVOR, although the viewing distance-related CVOR responses of individual central vestibular neurons were affected. We conclude that irregular afferents probably contribute to central signal processing related to both the AVOR and the CVOR, but the signals carried by these afferents are only essential for viewing distance-related changes in AVOR. Received: 13 June 1997 / Accepted: 12 August 1997     

Effects of afferent signals from the extraocular muscles upon units in the cerebellum, vestibular nuclear complex and oculomotor nucleus of the trout

The responses of single units in the cerebellum, the vestibular nuclear complex and adjacent regions of the brainstem and in the oculomotor nucleus were studied in decerebrate, paralysed rainbow trout (Salmo gairdneri). Natural vestibular stimulation was provided by horizontal, sinusoidal oscillation of the fish and extraocular muscle afferents of the eye ipsilateral to the recording were activated either by passive eye-movement or by electrical stimulation of the trochlear (IV) nerve in the orbit. Unit responses to vestibular and/or orbital stimuli were examined in peristimulus-time histograms interleaved in time. In the cerebellum and brainstem, of 124 units exposed to both types of stimulus, 26 (21%) responded only to vestibular input, 26 (21%) were affected only by the orbital signal and 23 (18%) received both signals. The remaining 49 units (39%) responded to mechanical stimulation of the head or body or to vibration; they were labelled "polymodal" and discarded. The recording sites of 56 units were verified by histology; 30 were in the cerebellum and 26 in the brainstem. Input from the eye muscles had excitatory or inhibitory effects upon the vestibular responses. The effects of the orbital signal were usually phasic but rare tonic responses also occurred. About half (15 of 34) of the units which responded to passive eye-movement showed statistically significant differences in the magnitude of their responses to horizontal and to vertical eye-movement. More units preferred horizontal movement (11) than preferred vertical passive eye-movement (four). Note that the plane of vestibular stimulation was always horizontal. In the region of the oculomotor nucleus, of 19 units, five (26%) gave vestibular responses only and three (16%) were affected only by the orbital signal; three units (16%) with polymodal responses were discarded. Of the eight units carrying both signals, histological confirmation that the recording site lay in the column of cells forming the oculomotor/trochlear nuclei was obtained in four. The responses and interactions were similar to those found in the brainstem. The results present two principal points of interest. 1. They reinforce the accumulating body of evidence that, in species with widely different oculomotor and visual behaviour, signals from extraocular muscle proprioceptors reach the vestibulo-ocular system; this, in turn, suggests that these signals may play some rather fundamental role in the oculomotor system.(ABSTRACT TRUNCATED AT 400 WORDS)     

Basic organization principles of the VOR: lessons from frogs

Locomotion is associated with a number of optical consequences that degrade visual information processing in the absence of appropriate compensatory movements. The resulting retinal image flow is counteracted by coordinated eye-head reflexes that are initiated by optokinetic and vestibular inputs. The contribution of the vestibulo-ocular reflex (VOR) for stabilizing retinal images is relatively small in amplitude in frogs but important in function by compensating for the non-linearities of the neck motor system. The spatial tuning of the VOR networks underlying the angular (AVOR) and linear (LVOR) with respect to canal and extraocular motor coordinates is organized in a common, canal-related reference frame. Thereby, the axes of head and eye rotation are aligned, principle and auxiliary VOR connections transform vestibular into motor signals and parallel AVOR and LVOR circuits mediate vergence and version signals separately. Comparison of these results with data from other vertebrates demonstrates a number of fundamental organization principles common to most vertebrates. However, the fewer degrees of behavioral freedom of frogs are reflected by the absence of, e.g. a functioning velocity storage network or of a fixation suppression of the VOR. In vitro experiments with the isolated brainstem and branches of N.VIII attached were used to study the putative transmitters of vestibular nerve afferent inputs, the postsynaptic receptor subtypes of second-order vestibular neurons and their dynamic response properties. Evidence is presented that suggests that afferent vestibular nerve fibers with different dynamic response properties activate different subtypes of glutamate receptors. The convergence pattern of monosynaptic afferent nerve inputs from different labyrinthine organs onto second-order vestibular neurons is remarkably specific. As a rule, second-order vestibular neurons receive converging afferent nerve inputs from one semicircular canal and from a specific sector of hair cells on one otolith organ. This convergence pattern remains malleable even in adulthood and reorganization is initiated by activity-related changes in vestibular nerve afferent fibers. The output of second-order vestibular neurons is modified by at least three inhibitory control loops. Uncrossed inhibitory vestibular side loops appear to control specifically the dynamic response tuning, whereas coplanar commissural inhibitory inputs improve mainly the spatial tuning and the cerebellar feedback loop controls the response gain. Among the targets of second-order vestibular projection neurons are extraocular motoneurons and internuclear neurons. Extraocular motoneurons differ among each other by the presence of very different response dynamics. These differences may represent a co-adaptation to the response dynamics of twitch and non-twitch extraocular muscle fibers. Different dynamical properties are required for a rapid acceleration of the globe at the one end and for the maintenance of a stable eccentric eye position over long periods of time at the other end of a continuum of variations in dynamic response properties. The maintenance of a given eccentric eye position over long periods of time is especially well developed in frogs and assists visual surveillance during lurking in the absence of saccades.     

A stretch reflex in extraocular muscles of species purportedly lacking muscle spindles

It is generally assumed that proprioceptive feedback plays a crucial role in limb posture and movement. However, the role of afferent signals from extraocular muscles (EOM) in the control of eye movement has been a matter of continuous debate. These muscles have atypical sensory receptors in several species and it has been proposed that they are not supported by stretch reflexes. We recorded electromyographic activity of EOM during passive rotations of the eye in sedated rats and squirrel monkeys and observed typical stretch reflexes in these muscles. Results suggest that there is a similarity in the reflexive control of limb and eye movement, despite substantial differences in their biomechanics and sensory receptors. Like in some limb skeletal muscles, the stretch reflex in EOM in the investigated species might be mediated by other length-sensitive receptors, rather than muscle spindles.     

Primate disconjugate eye movements during the horizontal AVOR in darkness and a plausible mechanism

Disconjugate eye movements during the horizontal angular vestibulo-ocular reflex (AVOR) evoked in response to steps or pulses of head velocity have been previously reported in lateral eyed animals. In this study, we measured binocular responses to sustained sinusoidal and pseudo-random vestibular stimuli in yaw, delivered in darkness, in both human and monkey. The vestibular stimuli used in our experiments had peak velocities in the range of 120–200°/s, frequencies in the range of 0.17–0.5 Hz, and durations between 60 and 75 s. Our results show a large vergence component to the AVOR response that systematically modulated with head velocity. We also examined our results for temporal–nasal preponderance in slow eye velocity. Although each subject showed some degree of directional preference, we did not find a systematically greater eye velocity for temporal–nasal direction across all subjects. Here, we present these findings and discuss that at least two possible sources could result in disconjugate eye movements during the horizontal rotational VOR in darkness: peripheral and central mechanisms.     

Vergence-mediated modulation of the human angular vestibulo-ocular reflex is unaffected by canal plugging

The angular vestibulo-ocular reflex (AVOR) normally has an increased response during vergence on a near target. Some lines of evidence suggest that different vestibular afferent classes may contribute differentially to the vergence effect. For example, lesions that selectively affect those afferents sensitive to acceleration, i.e. irregular afferents, (galvanic ablation, intratympanic gentamicin) have been found to markedly reduce the vergence-mediated modulation of the AVOR. We hypothesized that a nonspecific and incomplete reduction in the AVOR response caused by canal plugging should have minimal effect on vergence-mediated modulation of the AVOR. The AVOR response to passive head impulses in canal planes (horizontal canals, left anterior-right posterior canals, right anterior-left posterior canals) while viewing a far (124 cm) or near (15 cm) target was measured in seven human subjects before and after anterior canal (AC) plugging to treat vertigo caused by dehiscence of the AC (i.e. superior canal dehiscence). The impulses were low amplitude (∼20°), high velocity (∼150°/s), high-acceleration (∼3,000°/s²) head rotations administered manually by the investigator. Binocular eye and head velocity were recorded using the scleral search coil technique. The AVOR gain was defined as inverted eye velocity divided by head velocity. Before plugging, AVOR gain for the dehiscent AC went from 0.87 ± 0.10 for far targets to 1.04 ± 0.13 for near targets (+19.1 ± 7.3%). After plugging, the AC AVOR gain went from 0.50 ± 0.10 for far targets to 0.59 ± 0.11 for near targets (+19.7 ± 6.1%). There was no difference in the vergence-mediated gain increase between pre- and post-plugged conditions (multi-way analysis of variance: P = 0.66). AC plugging also did not change the latency of the AVOR for either AC. We hypothesize that canal plugging, unlike gentamicin or galvanic ablation, has no effect on vergence-mediated modulation of the AVOR because plugging does not preferentially affect irregular afferents.     

Latency of vestibular responses of pursuit neurons in the caudal frontal eye fields to whole body rotation

The smooth pursuit system and the vestibular system interact to keep the retinal target image on the fovea by matching the eye velocity in space to target velocity during head and/or whole body movement. The caudal part of the frontal eye fields (FEF) in the fundus of the arcuate sulcus contains pursuit-related neurons and the majority of them respond to vestibular stimulation induced by whole body movement. To understand the role of FEF pursuit neurons in the interaction of vestibular and pursuit signals, we examined the latency and time course of discharge modulation to horizontal whole body rotation during different vestibular task conditions in head-stabilized monkeys. Pursuit neurons with horizontal preferred directions were selected, and they were classified either as gaze-velocity neurons or eye/head-velocity neurons based on the previous criteria. Responses of these neurons to whole body step-rotation at 20 degrees/s were examined during cancellation of the vestibulo-ocular reflex (VOR), VOR x1, and during chair steps in complete darkness without a target (VORd). The majority of pursuit neurons tested (approximately 70%) responded during VORd with latencies <80 ms. These initial responses were basically similar in the three vestibular task conditions. The shortest latency was 20 ms and the modal value was 24 ms. These responses were also similar between gaze-velocity neurons and eye/head-velocity neurons, indicating that the initial responses (<80 ms) were vestibular responses induced by semicircular canal inputs. During VOR cancellation and x1, discharge of the two groups of neurons diverged at approximately 90 ms following the onset of chair rotation, consistent with the latencies associated with smooth pursuit. The shortest latency to the onset of target motion during smooth pursuit was 80 ms and the modal value was 95 ms. The time course of discharge rate difference of the two groups of neurons between VOR cancellation and x1 was predicted by the discharge modulation associated with smooth pursuit. These results provide further support for the involvement of the caudal FEF in integration of vestibular inputs and pursuit signals.     

Multiplicative computation in the vestibulo-ocular reflex (VOR)

Multiplicative computation is a basic operation that is crucial for neural information processing, but examples of multiplication by neural pathways that perform well-defined sensorimotor transformations are scarce. Here in behaving monkeys, we identified a multiplication of vestibular and eye position signals in the vestibulo-ocular reflex (VOR). Monkeys were trained to maintain fixation on visual targets at different horizontal locations and received brief unilateral acoustic clicks (1 ms, rarefaction, 85 approximately 110 db NHL) that were delivered into one of their external ear canals. We found that both the click-evoked horizontal eye movement responses and the click-evoked neuronal responses of the abducens neurons exhibited linear dependencies on horizontal conjugate eye position, indicating that the interaction of vestibular and horizontal conjugate eye position was multiplicative. Latency analysis further indicated that the site of the multiplication was within the direct VOR pathways. Based on these results, we propose a novel neural mechanism that implements the VOR gain modulation by fixation distance and gaze eccentricity. In this mechanism, the vestibular signal from a single labyrinth interacts multiplicatively with the position signals of each eye (Principle of Multiplication). These effects, however, interact additively with the other labyrinth (Principle of Addition). Our analysis suggests that the new mechanism can implement the VOR gain modulation by fixation distance and gaze eccentricity within the direct VOR pathways.     

Directionally-specific effects of afferent signals from the extraocular muscles upon responses in the pigeon brainstem to horizontal vestibular stimulation

The responses of single units in the brainstem of the decerebrate, paralysed, pigeon were studied. Natural vestibular stimulation was provided by horizontal, sinusoidal, oscillation of the bird and extraocular muscle afferents of the ipsilateral eye were activated by passive eye-movement. Unit responses to vestibular and/or orbital stimuli were examined in sets of peristimulus time histograms interleaved in time. Of 352 units in the brainstem, in the region of the vestibular nuclei, which were exposed to the effects of both vestibular stimuli and passive eye-movement, 40 (11%) responded only to the latter; the other 312 units (89%) responded to vestibular stimulation at 0.4 Hz (amplitude +/- 8 degrees). Of these 312 units, 129 (41%) were affected only by vestibular stimuli; in the other 183 units (59%) passive eye-movement produced clear modification of the vestibular responses by adding excitation or inhibition, or both. There were phasic modifications in most units; in 77 there were longer-lasting changes in the vestibular responses, often following a phasic response. In 124 units whose responses were subjected to statistical analysis, the vestibular responses of 42 (34%) were modified only by horizontal eye-movement and eight (6%) were affected only by vertical movement. A further 18% showed larger effects from horizontal than from vertical eye-movement; in 2% vertical eye-movement was preferred. Further examination of the specificity of the effects of eye-movement in planes between the vertical and horizontal was possible in 29 units which showed various degrees of "tuning" of the effect. In some units there was additional specificity for eye-movement in (a) particular directions (towards the beak rather than towards the tail, for example); (b) in particular arcs of the orbit (centre-to-temporal rather than nasal-to-centre, for example). Note that all these effects were upon the responses of the units to horizontal vestibular stimulation. Thus, the modifications of the vestibular responses depended upon specific characteristics of the passive eye-movement. The exact recording sites of 29 units were determined histologically; some were in the medial vestibular nucleus but many were in the adjacent reticular formation. The principal interest of the results is that they provide more detailed information than was available previously on the specificity of the effects of afferent signals from the extraocular muscles upon the vestibular responses of units in regions of the brainstem known to be involved in oculomotor control. The decerebrate pigeon proves to be a particularly good preparation in which to study these effects.(ABSTRACT TRUNCATED AT 400 WORDS)     

Vestibular nerve and nuclei unit responses and eye movement responses to repetitive galvanic stimulation of the labyrinth in the rat

Summary Two-second cathodal current pulses were applied at one-minute intervals at a point external to the round window in the ear of each albino rat subject. Responses were recorded in the vestibular nerve ganglion, the vestibular nuclei (single units), or in the eye movements (search coil recording method) of anaesthetized, decerebrated, or alert rats. The unit responses to the galvanic stimuli were characterized and compared with responses to galvanic and rotational stimuli reported in the literature. The main focus of the study, however, was effects of stimulus repetition. In both the vestibular nerve and vestibular nuclei recordings, the responses of many units were substantially larger or smaller at the end of a 13-pulse stimulus train than at the beginning. In the vestibular nuclei, but not in the nerve, there was a slight bias towards a decrease in response magnitude, with 10/88 units showing decreases great enough to be considered as reflecting an habituation process. In contrast, the eye movement responses showed more consistent response decrements, especially in the alert condition, but also in the other conditions (none of the unit recordings were done in alert rats). It is concluded that some of the modifications underlying habituation of the vestibuloocular reflex probably occur in portions of the neuronal reflex pathways that are downstream from the vestibular nuclei.Prof. Precht died on March 12, 1985     

Latencies of response of eye movement-related neurons in the region of the interstitial nucleus of Cajal to electrical stimulation of the vestibular nerve in alert cats

Summary Recent studies have shown that the interstitial nucleus of Cajal (INC) in the midbrain reticular formation is involved in the conversion of vertical semicircular canal signals into eye position during vertical vestibuloocular reflexes. Secondary vestibulo-ocular relay neurons related to the vertical canals, which constitute the majority of output neurons sending signals from the vestibular nuclei directly to the oculomotor nuclei, have been shown to project axon collaterals to the region within and near the INC. To understand how the INC is involved in the signal conversion, latencies of response of neurons in the INC region to electrical stimulaton of the vestibular nerve were examined in alert cats. The responses of 96 cells whose activity was clearly modulated by sinusoidal pitch rotation (at 0.31 Hz) were analyzed. These included 41 cells whose activity was closely correlated with vertical eye movement (38 burst-tonic and 3 tonic neurons), and 55 other cells (called pitch cells as previously). Twenty nine of the 96 cells (30%) were activated at disynaptic latencies following single shock stimulation of the contralateral vestibular nerve. Disynaptically activated cells were significantly more frequent for pitch cells than for eye movement-related cells (25/55 = 45% vs 4/41 = 10%; p < 0.001, Chi-square test). Conversely, cells that did not receive short-latency activation (< 6 ms) were more frequent among eye movement-related cells than pitch cells (26/41 = 63% vs 13/55 = 24%; p < 0.001, Chi-square test). Pitch cells showed significantly less phase lag (re head acceleration) than eye movement-related cells during sinusoidal pitch rotation (mean ± SD 124° ± 17° vs 138° ± 14°. p < 0.01, t-test). These results suggest that 1) cells in the INC region other than burst-tonic and tonic neurons mainly receive direct inputs from secondary vestibulo-ocular relay neurons, and that 2) vertical canal signals reach eye movement-related neurons mainly polysynaptically.     

Role of the primate flocculus in adaptation of the vestibulo-ocular reflex

Neuronal events associated with adaptation of the horizontal vestibulo-ocular reflex (HVOR) induced by sustained vestibular-visual mismatching were investigated in the primate flocculus. The floccular area related to the HVOR (H-zone) was identified by electrical micro-stimulation which induced ipsilaterally directed horizontal eye movement. It was thus found that Purkinje cells in the H-zone consistently changed their simple spike responses to head rotation in parallel with the adaptive HVOR gain change. This was demonstrated by observing the change of simple spike firing of Purkinje cells during adaptation of HVOR either in a population study or an individual study. Since similar changes occurred even after bilateral lesioning of vestibular nuclei had extinguished the HVOR, these changes appear to represent vestibular, but not eye velocity, mossy fiber responsiveness. The complex spike discharge, on the other hand, modulated during vestibular-visual stimulation with a reciprocal pattern to the adaptive changes in the simple spike discharge. These results are consistent with the hypothesis that the flocculus Purkinje cells adaptively control the HVOR through their simple spike activity under influences of retinal error signals conveyed by visual climbing fiber pathways.     

Neural correlates of the dependence of compensatory eye movements during translation on target distance and eccentricity

To stabilize objects of interest on the fovea during translation, vestibular-driven compensatory eye movements [translational vestibulo-ocular reflex (TVOR)] must scale with both target distance and eccentricity. To identify the neural correlates of these properties, we recorded from different groups of eye movement-sensitive neurons in the prepositus hypoglossi and vestibular nuclei of macaque monkeys during lateral and fore-aft displacements. All neuron types exhibited some increase in modulation amplitude as a function of target distance during high-frequency (4 Hz) lateral motion in darkness, with slopes that were correlated with the cell's pursuit gain, but not eye position sensitivity. Vergence angle dependence was largest for burst-tonic (BT) and contralateral eye-head (EH) neurons and smallest for ipsilateral EH and position-vestibular-pause (PVP) cells. On the other hand, the EH and PVP neurons with ipsilateral eye movement preferences exhibited the largest vergence-independent responses, which would be inappropriate to drive the TVOR. In addition to target distance, the TVOR also scales with target eccentricity, as evidenced during fore-aft motion, where eye velocity amplitude exhibits a "V-shaped " dependence and phase shifts 180 degrees for right versus left eye positions. Both the modulation amplitude and phase of BT and contralateral EH cells scaled with eye position, similar to the evoked eye movements during fore-aft motion. In contrast, the response modulation of ipsilateral EH and PVP cells during fore-aft motion was characterized by neither the V-shaped scaling nor the phase reversal. These results show that distinct premotor cell types carry neural signals that are appropriately scaled by vergence angle and eye position to generate the geometrically appropriate compensatory eye movements in the translational vestibulo-ocular reflex.     

Co-modulation of stimulus rate and current from elevated baselines expands head motion encoding range of the vestibular prosthesis

An implantable prosthesis that stimulates vestibular nerve branches to restore sensation of head rotation and vision-stabilizing reflexes could benefit individuals disabled by bilateral loss of vestibular sensation. The normal vestibular system encodes head movement by increasing or decreasing firing rate of the vestibular afferents about a baseline firing rate in proportion to head rotation velocity. Our multichannel vestibular prosthesis emulates this encoding scheme by modulating pulse rate and pulse current amplitude above and below a baseline stimulation rate (BSR) and a baseline stimulation current. Unilateral baseline prosthetic stimulation that mimics normal vestibular afferent baseline firing results in vestibulo-ocular reflex (VOR) eye responses with a wider range of eye velocity in response to stimuli modulated above baseline (excitatory) than below baseline (inhibitory). Stimulus modulation about higher than normal baselines resulted in increased range of inhibitory eye velocity, but decreased range of excitatory eye velocity. Simultaneous modulation of rate and current (co-modulation) above all tested baselines elicited a significantly wider range of excitatory eye velocity than rate or current modulation alone. Time constants associated with the recovery of VOR excitability following adaptation to elevated BSRs implicate synaptic vesicle depletion as a possible mechanism for the small range of excitatory eye velocity elicited by rate modulation alone. These findings can be used toward selecting optimal baseline levels for vestibular stimulation that would result in large inhibitory eye responses while maintaining a wide range of excitatory eye velocity via co-modulation.     

Analysis of signal content of Purkinje cell responses to optokinetic stimuli in the rabbit cerebellar flocculus by selective lesions of brainstem pathways

The heterogeneous signal content of floccular Purkinje cell responses to optokinetic stimuli was analyzed in alert rabbits by means of selective lesions to brainstem pathways. Extracellular spike activities of Purkinje cells were recorded from rostral areas of the flocculus where local electrical stimulation elicited abduction of the ipsilateral eye. Chronic unilateral destruction of the nucleus reticularis tegmenti pontis, interrupting the visual mossy fiber afferent pathway to the flocculus, reduced the gain of the optokinetic eye movement (OKR) to one-third of the control. Concomitantly, simple spike responses of Purkinje cells to optokinetic stimuli were reduced to less than one-third of the control values. Severance of the visual climbing fiber afferent pathway by rostral inferior olivary lesions reduced the OKR gain little, and decreased the simple spike responses of the Purkinje cells only slightly. Bilateral lesions of the rostral half of the medial vestibular nucleus and rostro-ventral part of the lateral vestibular nucleus, which reduced the eye velocity in the OKR to less than one-third of the control value, did not induce any appreciable change in the simple spike responses of the Purkinje cells. It is concluded that visual mossy fiber signals are the most dominant factor which determines Purkinje cell responses to optokinetic stimuli, while visual climbing fiber signals and eye velocity mossy fiber signals make only subsidiary contributions.