Anatomical segregation of different adaptative processes within the vestibulocerebellum of the cat.

Bilateral surgical lesions of the flocculus or the nodulo-uvular lobes were performed in the cat. Effects of these lesions on optokinetic and optokinetic afternystagmus OKAN), vestibulo-ocular reflex (VOR), visual suppression, and adaptation and habituation of VOR were studied using an identical experimental protocol. After flocculectomy, all these functions were impaired, except for habituation. Long-term postoperative recordings only revealed a recovery of the suppression of VOR, suggesting a limited contribution of the flocculus to this function. After nodulo-uvulectomy, only habituation and OKAN were modified. When the lesion was restricted to part of the uvula, OKAN duration was decreased. For other lesions involving the uvula together with the nodulus and/or the lobules VII-VIII,OKAN duration was increased. Habituation was lost after destruction of the nodulo-uvular lobes. When this latter structure was damaged, the retention component of habituation was selectively impaired, sparing the acquisition. Additional lesions outside the vestibulocerebellum appeared necessary to suppress the two components. Comparison of results obtained after flocculectomy and after nodulouvulectomy confirms and extends to non-primate species the concept of a "differential control" of adaptation and habituation by distinct vestibulocerebellar structures.

Longterm impairment of cat optokinetic nystagmus following visual cortical lesions.

Binocular and monocular gain of optokinetic nystagmus (OKN), OKN dynamics, vestibulo-ocular reflex (VOR) and VOR adaptation were measured in 5 normal cats and in 5 cats which underwent bilateral visual cortical lesions involving the 17-18 complex at least 4 months before testing. We observed longterm deficits after bilateral lesions involving area 17 and variable parts of area 18 but failed to observe deficits after 18-19 lesions. These deficits were limited to the OKN gain and the build-up time constant of OKN; the VOR and the optokinetic after-nystagmus (OKAN) time constant were within normal limits. Our results suggest that areas 17-18 operate in parallel to control the encoding of retinal slip velocity at the level of the nucleus of the optic tract (NOT) and the accessory optic system (AOS), which are known to represent the initial stage of the optokinetic pathways.

Optokinetic nystagmus in the ferret: including selected comparisons with the cat.

The aim of this study was to evaluate the functional significance of similarities observed in the anatomy and the physiology of cat and ferret visual systems. Optokinetic nystagmus (OKN) in response to movement of the entire visual field, and optokinetic after nystagmus (OKAN) were measured in 8 ferrets with binocular stimulation. A shift of the beating field in the same direction as the fast phase of eye movements was observed both in ferret and cat. The absence of a fast rise in slow phase velocity (SPV) and similarities in the time constant to reach the steady state OKN gain, using step velocity stimuli are noted. As in the cat, primary OKAN was observed with a gradual decrease in its SPV. Following termination of stimulation, no sudden fall in SPV was noted for either species. However, for the ferret, the decrease was more rapid. With monocular stimulation, small differences were observed in OKN gain when responses to temporonasal and nasotemporal directions of the stimulus were compared in the two species. In contrast, the ferret displays a OKN gain which is approximatively twice that of the cat at stimulus velocities of 100 degrees/sec. Even at 200 degrees/sec., visual movement still induces a discernable OKN response (gain .0.07). Secondary OKAN, always present in the cat, was observed in only 43% of ferret records. Taken together with other considerations, these findings recommend the ferret as an alternative to the cat for the study of OKN and of other visuo-motor capacities in carnivores.

Horizontal optokinetic responses under stroboscopic illumination in cat, monkey and man.

The horizontal optokinetic reflex (OKN) was studied in cat, monkey and man under conditions of steady or stroboscopic illumination. In all species, there was an abrupt decrease in OKN gain for a given spatial displacement of the stimulus between two consecutive stroboscopic flashes. The upper limit of spatial displacement which preserved optimal OKN gain was independent of stimulus velocity and flash frequency. The value of this limit differed in the three species studied. In the cat, OKN gain was affected when the spatial displacement between two stimuli exceeded 0.55 degrees of visual angle. In monkey and man, these limits were 1.48 degrees and 2.87 degrees, respectively. When human subjects were asked to volontary track the stimulus, the limit value reached 4.3 degrees. This result is discussed in the context of the evolution of the smooth pursuit system and its contribution to optokinetic response.

Latent defect in monocular optokinetic nystagmus after neonatal removal of the lateral suprasylvian area in the cat.

Three kittens underwent unilateral removal of the lateral suprasylvian area of cortex at the age of 1 month. After normal rearing for two years, their monocular optokinetic nystagmus was studied. During the experiment one eye was 'seeing' the optokinetic stimulus, but the other eye was 'covered'; by implanting scleral coils on both eyes, we measured movements not only in the 'seeing' eye, but also in the 'covered' eye. The stimulus was moved at a velocity between 1 and 40 degrees/s. Additionally, movements of the both eyes were simultaneously recorded in a normal cat. The previous results on movements of both eyes in normal cats which had been derived from the recordings by one coil (Vision Res., 26: 1311-1314, 1986) were confirmed by this experiment and were compared with the results of the lesioned cats. The gains (slow phase velocity/stimulus velocity) of the 'seeing' eye were not significantly different from the normal values. However, the gains of the 'covered' eye were significantly higher than the normal values when the stimulus was presented in the temporonasal direction, at the velocities between 1 and 40 degrees/s to the eye ipsilateral to the lesion and at the velocity of 40 degrees/s to the eye contralateral to the lesion; in the other conditions of stimulation the gains were not significantly different from the normal values.

Cross-coupled effects of repeated vestibular and optokinetic stimulations on the dynamics of the vestibulo-ocular and optokinetic reflexes in the cat.

Cats were submitted to repeated step stimulations either vestibular or optokinetic. Regardless of which of the two stimuli was used, dynamic modifications were observed in both vestibulo-ocular response and optokinetic after-nystagmus (OKAN). The progressive changes in post-rotational nystagmus and OKAN were quantified by measuring the duration of their primary phase. A parallel evolution of these two parameters was found. When repeated unidirectional vestibular stimulations were used, the same asymmetry was induced in both vestibuloocular responses and OKAN. These results support the hypothesis that the vestibulo-ocular and the optokinetic reflex share a common velocity storage mechanism, although alternative hypotheses cannot be excluded.

In search for the egocentric reference. A neurophysiological hypothesis.

Unilateral lesions of the middle suprasylvian gyrus in the cat parietal cortex produce an asymmetrical vestibulo-ocular reflex such that responses to head rotation toward the side opposite to the lesion become weaker. Unilateral lesions of the superior colliculus in the cat also produce the same effect. In either case symmetrical responses are recovered within 2-3 weeks. These results are discussed in terms of displacement, by the unilateral lesion, of an internal reference used for directing behaviour within extrapersonal space. Relevance of this hypothesis to clinical symptoms observed in man after unilateral posterior parietal lesions is discussed, with particular emphasis on the unilateral neglect phenomenon.

Effects of unilateral flocculus lesions on vestibulo-ocular responses in the cat.

Unilateral lesions of the cerebellar flocculus were performed in three chronically-implanted adult cats. Following the lesion a spontaneous nystagmus was observed in the dark, with the fast phase directed to the lesioned side. Vestibulo-ocular responses in the dark became asymmetrical. Responses to velocity steps exciting the labyrinth ipsilateral to the lesion were strongly increased. A decrease, although less marked, was observed in the opposite direction. Responses to sinusoidal oscillations in the dark were also asymmetric with respect to both the cumulative eye displacement during rotation in the two directions and the interval between two consecutive reversals of eye movement. These differences were greater at the lower tested frequencies (0.01 HZ) than at the higher (0.1 HZ). Spontaneous nystagmus disappeared in about 10 days and a complete symmetry of the vestibulo-ocular responses was restored in about 3 weeks. It is concluded that a unilateral lesion of the flocculus leads to two separate, but interacting, effects upon vestibulo-ocular responses.

Possible visual pathways to the cat vestibular nuclei involving the nucleus prepositus hypoglossi.

Non-cerebellar afferents from visual relays to the vestibular nuclei (VN) of the cat have been re-evaluated with the use of the horseradish peroxidase technique. From our data it can be concluded that: (1) A monosynaptic projection from the nucleus reticularis tegmenti pontis to the VN can be excluded. (2) Monosynaptic projections from the superior colliculus and some of the pretectal nuclei (nucleus of the optic tract, olivary pretectal nucleus) to the nucleus prepositus hypoglossi may constitute polysynaptic visual afferents to the VN, which would account for the residual visual sensitivity of the VN neurons after cerebellar or inferior olivary lesions.

The role of the flocculus in vestibular compensation after hemilabyrinthectomy.

Unilateral lesions of the cerebellar flocculus were made in two groups of cats chronically implanted for eye-movement recording. In the first group (3 cats), the floccular lesion preceded by 40-70 days a unilateral labyrinthectomy on the contralateral side. In the second group (5 cats), the serial order of the two lesions was reverted, the unilateral flocculectomy following unilateral labyrinthectomy by about 60 days in 2 animals and by 16-27 months in the other 3. The effects of the unilateral labyrinthectomy on the vestibulo-ocular reflex (spontaneous nystagmus and asymmetrical responses) were extensively tested by using natural vestibular stimulations. It was found that recovery from these effects was severely delayed in animals from the first group (flocculectomy prior to labyrinthectomy), although in animals from the second group the flocculectomy secondary to the labyrinthectomy only produced a transient asymmetry of vestibulo-ocular responses. It is concluded that the flocculus is required for initiating (not for maintaining), the compensatory process following peripheral lesions of the vestibular system.

Vestibulo-ocular reflex and optokinetic nystagmus in adult cats reared in stroboscopic illumination.

Cats reared in stroboscopic illumination (strobe reared cats) have been found to have abnormal eye movements. Visual and vestibular evoked compensatory eye movements were inefficient. Vestibulo-ocular reflex in the dark had a maximum gain of 0.6 (1.0 in normal animals). Optokinetic nystagmus had a mean gain which approached unity only at stimulus velocities around 7 degrees/S (up to 30 degrees/S in normal animals). The asymmetry of the optokinetic nystagmus resulting from monocular stimulation was more pronounced in strobe reared cat than in normal animals. Interaction between vestibulo-ocular reflex and optokinetic nystagmus to give adequate compensatory eye movements was absent in strobe reared cats: visual suppression of vestibulo-ocular reflex was absent when the animal was rotated in an illuminated environment which remained stationary with respect to the head. Optokinetic nystagmus failed to improve the gain of the vestibulo-ocular reflex when the animal was rotated in a normally lit environment. The deprived animals showed no signs of recovery after 5 months exposure to normal lighting.

Effects of unilateral superior colliculus ablation on oculomotor and vestibulo-ocular responses in the cat.

1. Unilateral lesions of the superior colliculus were made in normal cats. Following the operation, animals exhibited a typical neglect for contralateral visual space and forced circling toward the ipsilateral side. Optokinetic nystagmus was decreased for a stimulus moving toward the ipsilateral side, particularly in the temporal-to-nasal direction when the eye contralateral to the lesion was stimulated alone. -- 2. When tested in the dark, animals exhibited a strong imbalance of their vestibulo-ocular responses (VOR) to velocity steps or to sinusoidal oscillations. Rotation of the animal toward the ipsilateral side produced a VOR with a higher gain, and a shorter phase-lead than in pre-operative controls. VOR was decreased in the opposite direction to a smaller extent, however, the overall asymmetry between the two sides at the post-operative stage was about 40%. -- 3. In two animals, spontaneous nystagmus was present in the dark with the fast phase toward the ipsilateral side. -- 4. Visual suppression of VOR was abolished during ipsiversive rotation and was still present during contraversive rotation. -- 5. The effects of unilateral colliculectomy on VOR were transient. Spontaneous nystagmus disappeared in 3 days. VOR asymmetry in the dark was no longer present after 2-3 weeks. Loss of visual VOR suppression persisted for a few more days. -- 6. Superior colliculus exerts a tonic control on static and dynamic components of VOR. This control may mediate part of VOR visual modulation and provide a substitutive input for compensation of pathological VOR asymmetry.

Afferent visual pathways and receptive field properties of superior colliculus neurons in stroboscopically reared cats.

Unit recordings were made in the superior colliculus of strobe-reared cats. Receptive field properties were studied and electrical stimulation in the chiasma and optic tract made it possible to characterize the visual input. The retinal Y-cell input and the cortical input were found to be deficient. The principal response deficit was the decrease of selective response to direction of movement, also shown to be largely absent in the corticotectal pathway. These results are compared to similar findings in dark-reared animals and discussed in connection with the importance of visual movement to the developing visual system.

Development of vestibulo-ocular response in the kitten.

Vestibulo-ocular response (VOR) has been recorded in kittens aged between 10 and 61 postnatal days. Responses to velocity steps and to sinusoidal oscillations are present on the earliest recordings, though they are limited to a low gain slow compensatory gaze displacement. Vestibular-induced saccades appear only around postnatal day 30, but adult-like responses with a high gain are not displayed before the end of the second month. Optokinetic nystagmus (OKN) appears earlier (around postnatal day 25) and maturates faster.

Vestibulo-ocular responses during the states of sleep in the cat.

The vestibulo-ocular response (VOR) was recorded during natural sleep in cats with chronically implanted electrodes. By using a small amplitude sinusoidal head rotation (11 degrees) peak-to-peak at 0.4 Hz) which elicited only slow compensatory eye movements, the VOR amplitude was found to decrease steeply (down to 40% or less) during slow-wave sleep. The phase of the VOR with respect to head position remained approximately constant. With a larger amplitude of sinusoidal rotation (320 degrees peak-to-peak at 0.05 Hz) the VOR response included nystagmus. During slow-wave sleep, nystagmus disappeared and the overall amplitude of the response decreased. Simultaneously, the phase of the eye response with respect to head position shifted by up to 90 degrees in advance. During paradoxical sleep, VOR disappeared in all cases and was replaced by randomly occurring bursts of rapid eye movements. These results are discussed in terms of a parametric control model of VOR.