Neuronal activity in the vestibular nuclei of the alert monkey during vestibular and optokinetic stimulation

Summary Recordings from neurons of the vestibular nuclei were performed in alert monkeys. Type I and type II units were identified by rotating the monkey about a vertical axis. All neurons responded also when only the visual surround was rotated around the stationary monkey. The combination of visual and vestibular stimulation points towards non-algebraic summation characteristics for the two inputs, with each input dominating the response over a certain range.Supported by Swiss National Foundation for Scientific Research 3.044.76 and Emil-Barell-Foundation of Hoffmann-La Roche, Basel, Switzerland     

Vestibular nuclei activity in the alert monkey during suppression of vestibular and optokinetic nystagmus

Summary Single neurons were recorded in the vestibular nuclei of monkeys trained to suppress nystagmus by visual fixation during vestibular or optokinetic stimulation. During optokinetic nystagmus vestibular nuclei neurons exhibit frequency changes. With the suppression of optokinetic nystagmus this neuronal activity on average is attenuated by 40% at stimulus velocities of 40 °/s. At a stimulus velocity of 5 °/s responses are, under both conditions, close to threshold. For steps in velocity, suppression of vestibular nystagmus shortens the time constants of the decay of neuronal activity from 15–35 s to 5–9 s, while the amplitude of the response remains unchanged. The results are discussed in relation to current models of visual-vestibular interaction. These models use a feedback mechanism which normally operates during vestibular and optokinetic nystagmus. Nystagmus suppression interrupts this feedback loop.Supported by the Swiss National Foundation for Scientific Research (SNF 3.233.77) and the Deutsche Forschungsgemeinschaft (U.W. Buettner, Bue 379/2)     

Vestibular nuclei activity and eye movements in the alert monkey during sinusoidal optokinetic stimulation

Summary In the alert monkey (Macaca fascicularis) vestibular nuclei neurons and eye movements were recorded during sinusoidal optokinetic stimulation in the horizontal plane at frequencies between 0.02–3.3 Hz. Maximal stimulus velocity was generally kept constant at 40 deg/s, except for frequencies above 1 Hz. Eye movements showed a nystagmuslike pattern up to 0.2 Hz with a gain (change in eye position/change in cylinder position) greater than 0.8; at frequencies above 1 Hz the gain dropped to 0.35 at 3.3 Hz. A decrease in gain was accompanied by an increasing phase lag. Recordings in the vestibular nuclei were obtained from vestibular only and vestibular plus saccade neurons. Neurons with a strong eye position signal (vestibular plus position) were excluded. The vast majority (87%) of neurons were not modulated at 0.2 Hz or higher frequencies of sinusoidal optokinetic stimulation, and were classified as low-frequency type neurons. Compared to the response at constant stimulus velocity, sensitivity (imp·s^-1/deg·s^-1) dropped to 72% at 0.03 Hz and 16% at 0.1 Hz. A few neurons (13%) responding at 0.2 Hz (sensitivity on average 65% of the constant velocity response) were classified as high-frequency type neurons. They did not respond above 1.0 Hz and showed no modulation with individual eye movements. The results suggest that the activity in the groups of vestibular nuclei neurons tested here is insufficient to account for the eye movements in response to sinusoidal optokinetic stimulation at frequencies above 0.1 Hz. Thus additional neuronal mechanisms have to be involved in the generation of high frequency optokinetic responses, a likely structure being the flocculus in the cerebellum. Whether the high-frequency type vestibular nuclei neurons play a role for this response has yet to be determined.Supported by Deutsche Forschungsgemeinschaft SFB 200 A 2R.B. was a Alexander v. Humboldt fellow.     

Vestibular nerve activity in the alert monkey during vestibular and optokinetic nystagmus

Summary Activity of vestibular nerve fibers and eye movements were recorded in the alert monkey during natural stimulation. The animal was rotated about a vertical axis in the dark with velocity trapezoids (vestibular), or a striped cylinder was rotated around the stationary monkey (optokinetic), or these stimuli were combined.After velocity steps in the dark, neuronal activity declined with a dominant time constant of 5–6 s. The time constant of nystagmus recorded simultaneously was always longer, on average 23 s. Vestibular nerve activity was not influenced by optokinetic patterns or additional visual stimuli during combined visualvestibular stimulation. Thus, in contrast to vestibular nuclei neurons, vestibular nerve activity in the alert monkey is only determined by head acceleration and cannot be related to the nystagmus response or visual stimuli.Supported by a grant from the Swiss National Foundation for Scientific Research 3.343-2.78     

Behavior of horizontal semicircular canal afferents in alert monkey during vestibular and optokinetic stimulation

Summary The behavior of single vestibular nerve fibers from the lateral semicircular canal was recorded during sinusoidal oscillations of the head, during optokinetic stimulation with the head stationary, and during spontaneous oculomotor behavior in the alert monkey. The response of similar fibers to adequate vestibular stimulation was also studied in some of the animals under deeply anesthetized conditions. In the alert animals all units were spontaneously active and their discharge was modulated only by adequate vestibular stimulation. Ipsilateral horizontal rotations of the head were excitatory for all units. No modification of this basic vestibular response by visual stimulation including full-field striped drum rotation was observed. Furthermore no correlation of unit activity with oculomotor function including voluntary saccadic and pursuit eye movements was found in any of the units. The regularity of spontaneous discharge was the most consistent characteristic that differentiated the unit response into types. Most units were very regular in discharge, but a few were very irregular. The averaging of unit discharge over several cycles of oscillatory head rotation showed that the irregular type units were also consistently modulated by adequate vestibular stimulation. Both regular and irregular type units were found in the anesthetized animals. Unimodal distributions of the quantitative values for unit resting discharge rate, sensitivity, and phase relationship were found. The distributions for these three parameters were similar in the units recorded in the anesthetized animals. Thus at least these characteristics of semicircular canal response seem not to be affected by the vestibular efferent system which should be altered or eliminated in the case of the anesthetized animals.Research supported by NIH Grant EY0995-04.     

Linear addition of optokinetic and vestibular signals in the vestibular nucleus

Summary A simple model of the vestibuloocular reflex and the optokinetic system was used to simulate recent data on visual and vestibular responses of neurons in the vestibular nucleus. Contrary to a previous interpretation, the results support the hypothesis that the optokinetic and semicircular canal signals are combined simply by linear addition on the cells of the vestibular nucleus.     

Visual-vestibular interactions in the vestibular nuclei of the goldfish

Summary The responses of vestibular nuclei neurons of relaxed unaesthetized goldfish have been examined with trapezoid velocity stimuli under three conditions. Responses to horizontal body rotation in the dark (pure vestibular stimulation) resemble those observed in vestibular nerve afferents. Optokinetic responses to exclusive visual surround-motion are also direction-specific and, in contrast to vestibular responses, exhibit a tonic response to constant velocity. They show three different response profiles, classified A, B or C, based on the neuron's discharge rate: either increasing, decreasing or remaining constant once surround motion is maintained at constant velocity. Following these dynamic effects, optokinetic responses have a maintained modulation of resting discharge until deceleration commences. The time constants associated with the dynamic effects vary between 1 and 11 seconds. Steady-state modulation of optokinetic responses shows a weak relation to stimulus velocities exceeding 10 deg/sec. Responses to body rotation in the light were found to linearly combine the weighted vestibular and optokinetic responses so that accurate velocity information is available for sensory and motor functions independent of the neuron's vestibular (I, II) or optokinetic (A, B, C) response type. The principle of this visual-vestibular interaction is discussed with respect to multisensory processing within the vestibular nuclei.     

The optokinetic response under open and closed loop conditions in the monkey

Summary The spatial and temporal characteristics of optokinetic nystagmus (OKN) were investigated in the alert rhesus monkey under open and closed-loop conditions. One eye of each animal was immobilized by transection of the 3rd, 4th and 6th nerve intracranially. On optokinetic stimulation of the paralytic eye (open-loop) with the monkey's head restrained, eye movement records of the occluded, moving eye demonstrate a gradually increasing OKN, its slow phase reaching angular velocities much faster than pattern speed. This runaway effect is discussed in terms of the corollary discharge concept. Similarities of optokinetic and post-rotatory vestibular after-nystagmus are discussed. Investigation of the spatial parameters shows that the size of perifoveal areas successfully stimulated to elicit optokinetic nystagmus is relatively small under open-loop conditions and that this size depends on the distance of the stimulated area from the fovea, the minimum field diameter being an exponential function of excentricity. The preparation is shown to be useful for objective measurements of visual functions in the experimental monkey.This research was supported in part by NSF Grant GB-17047, Foundation Fund of Research in Psychiatry Grant G 69-447 and NASA Grant NGL 22-009-308.     

Effects of lesions of the nucleus of the optic tract on optokinetic nystagmus and after-nystagmus in the monkey

Summary 1. The nucleus of the optic tract (NOT) and the dorsal terminal nucleus (DTN) of the accessory optic system were lesioned electrolytically or with kainic acid in rhesus monkeys. When lesions involved NOT and DTN, peak velocities of optokinetic nystagmus (OKN) with slow phases toward the side of the lesion were reduced, and optokinetic after-nystagmus (OKAN) was reduced or abolished. The jump in slow phase eye velocity at the onset of OKN was smaller in most animals, but was not lost. Initially, there was spontaneous nystagmus with contralateral slow phases. OKN and OKAN with contralateral slow phases were unaffected. 2. Damage to adjacent regions had no effect on OKN or OKAN with two exceptions: 1. A vascular lesion in the MRF, medial to NOT and adjacent to the central gray matter, caused a transient loss of the initial jump in OKN. The slow rise in slow phase velocity was prolonged, but the gain of OKAN was unaffected. There was no effect after a kainic acid lesion in this region in another animal. 2. Lesions of the fiber tract in the pulvinar that inputs to the brachium of the superior colliculus caused a transient reduction in the buildup and peak velocity of OKN and OKAN. 3. In terms of a previous model (Cohen et al. 1977; Waespe et al. 1983), the findings suggest that the indirect pathway that activates the velocity storage integrator in the vestibular system to produce the slow rise in ipsilateral OKN and OKAN, lies in NOT and DTN. Activity for the rapid rise in OKN, carried in the direct pathway, is probably transmitted to the pontine nuclei and flocculus via an anatomically separate fiber path-way that lies in the MRF. A fiber tract in the pulvinar that inputs to the brachium of the superior colliculus appears to carry activity related to retinal slip from the visual cortex to NOT and DTN.Abbreviations used in Figures BIC brachium of the inferior colliculus - BSC brachium of the superior colliculus - C caudate nucleus - CG central gray - CL Centralis lateralis - dbc decussation of the brachium conjunctivum - DTN dorsal terminal nucleus of the accessory optic system - IC inferior colliculus - Hb habenular nucleus - hc habenular commissure - LD lateralis dorsalis - LGn lateral geniculate nucleus - MD medialis dorsalis - MGn medial geniculate nucleus - MLF median longitudinal fasciculus - MRF mesencephalic reticular formation - cMRF central mesencephalic reticular formation - NL nucleus limitans - NLL nucleus of the lateral lemniscus - NOT nucleus of the optic tract - PB parabigeminal nucleus - pc posterior commissure - Pi pineal gland - PON pretectal olivary nucleus - Pt pretectum - Pulv pulvinar - R nucleus reticularis - RN red nucleus - RpN raphe nucleus - RTP nucleus reticularis tegmenti pontis - SC superior colliculus - SCpit superior cerebellar peduncle - VPL ventralis postero-lateralis - VPM ventralis posteromedialis - III oculomotor nucleus - IV trochlear nucleus - IVn trochlear nerve - Vm mesencephalic trigeminal nucleus     

Visual sensory substitution in vestibular compensation: neuronal substrates in the alert cat

The purpose of this study was to investigate adaptive changes in the activity of vestibular nuclei neurons unilaterally deprived of their primary afferent inputs when influenced by visual motion cues. These neuronal changes might account for the established role that vision plays in the compensation for posturo-kinetic deficits after the loss of vestibular inputs. Neuronal recordings were made in alert, non-paralysed cats that had undergone unilateral vestibular nerve sections. The unit responses collected in both Deiters' nuclei were compared to those previously recorded in intact cats. We analysed the extracellular activity of Deiters' nucleus neurons, as well as the optokinetic reflex (OKR) evoked during sinusoidal translation of a whole-field optokinetic stimulus in the vertical plane. In intact cats, we found the unit firing rate closely correlated with the visual surround translation velocity, and the relationship between the discharge rate and the motion frequency was tuned around an optimal frequency. The maximum firing rate modulation was generally below the 0.25 Hz stimulus frequency; unit responses were weak or even absent above 0.25 Hz. From the 4th day to the end of the 3rd week after ipsilateral deafferentation, a majority of cells was found to display maximum discharge modulation during vertical visual stimulation at 0.50 Hz, and even at 0.75 Hz, indicating that the frequency bandwidth of the visually induced responses of deafferented vestibular nuclei neurons had been extended. Consequently, the frequency-dependent attenuation in the sensitivity of vestibular neurons to visual inputs was much less pronounced. After the first 3 weeks postlesion, the unit response characteristics were very similar to those observed prior to the deafferentation. On the nucleus contralateral to the neurectomy, the maximum modulation of most cells was tuned to the low frequencies of optokinetic stimulation, as also seen prior to the lesion. We found, however, a subgroup of cells displaying well-developed responses above 0.50 Hz. Under all experimental conditions, the neuronal response phase still remained closely correlated with the motion velocity of the vertical sinusoidal visual pattern. We hypothesize that Deiters' neurons deprived of their primary afferents may transiently acquire the ability to code fast head movements on the basis of visual messages, thus compensating, at least partially, for the loss of dynamic vestibular inputs during the early stages of the recovery process. Since the overall vertical OKR gain was not significantly altered within the 0.0125 Hz–1 Hz range of stimulation after the unilateral neurectomy, it can be postulated that the increased sensitivity of deafferented vestibular neurons to visual motion cues was accounted for by plasticity mechanisms operating within the deafferented Deiters' nucleus. The neuroplasticity mechanisms underlying this rapid and temporary increase in neuronal sensitivity are discussed.     

Purkinje cell activity in the flocculus of vestibular neurectomized and normal monkeys during optokinetic nystagmus (OKN) and smooth pursuit eye movements

Summary 1. Single unit activity was recorded in the primate flocculus after the vestibular nerves were cut (bilateral vestibular neurectomy) during optokinetic nystagmus (OKN), smooth pursuit eye movements (SP) and whole field visual stimulation with gaze fixed on a stationary target light (OKN-suppression). Following vestibular neurectomy monkeys had no vestibular responses and no optokinetic after-nystagmus (OKAN) in the horizontal plane. However, OKN slow phases still reached steady state velocities of up to 100 deg/s. 2. After neurectomy, simple spike (SS) activity of Purkinje cells (P-cells) was modulated in relation to eye velocity, regardless of whether eye velocity was induced by a small target light moving in darkness (SP) or by a moving visual surround (OKN). In over 90% of the P-cells firing rate increased with eye velocity to the ipsilateral side and decreased with velocities to the contralateral side. Modulation in firing rate increased monotonically with increasing eye velocity. The strength of modulation was similar during SP and OKN for the same eye velocity. 3. The change in firing rate of P-cells in response to a sudden change in optokinetic stimulus velocity contained a component related to eye velocity and a component related to eye acceleration. Only a few P-cells were also modulated with image slip velocity during OKN-suppression. 4. The modulation of P-cells during SP and OKN was compared in normal and vestibular neurectomized monkeys. The sensitivity of floccular P-cells to eye velocity during SP was 1.14 imp·s^–1/deg·s^–1 in normal monkey and 1.28 imp·s^–1/deg·s^–1 after neurectomy. The similarity of eye velocity sensitivities demonstrates that neurectomy does not change the characteristics of floccular P-cell modulation during SP. In contrast, during OKN modulation of P-cells is quite different in normal and neurectomized monkey. In normal monkey, P-cells are modulated during steady state OKN for eye velocities above 40–60 deg/s only. This threshold velocity corresponds approximately to the maximal initial OKAN velocity (i.e. OKAN saturation velocity). After neurectomy, the threshold velocity is 0 deg/s and P-cells are modulated during steady state OKN also over ranges of eye velocities that do not cause a response in normal monkey. Sensitivities of P-cells to eye velocity during OKN for eye velocities above the threshold velocity are 1.0 imp·s^–1/deg·s^–1 in neurectomized monkey and 1.43 imp·s^–1/deg·s^–1 in normal monkey. 5. The hypothesis has been put forward that OKN slow phase velocity in normal monkey has two dynamically different components, a fast and a slow component. The results strongly suggest that the two components depend on different neuronal populations. Firing rate of floccular P-cells is modulated in relation to the fast component only. The results furthermore support the idea that it is the smooth pursuit system which may generate the fast component in the OKN slow phase velocity response.Supported by Swiss National Foundation for Scientific Research (Nr. 3.718-0.80 and 3.593-0.84)     

Eye movements during combined pursuit, optokinetic and vestibular stimulation in macaque monkey

 During natural behaviour in a visual environment, smooth pursuit eye movements (SP) usually override the vestibular-ocular reflex (VOR) and the optokinetic reflex (OKR), which stem from head-in-space and scene-relative-to-eye motion, respectively. We investigated the interaction of SP, VOR, and OKR, which is not fully understood to date. Eye movements were recorded in two macaque monkeys while applying various combinations of smooth eye pursuit, vestibular and optokinetic stimuli (sinusoidal horizontal rotations of visual target, chair and optokinetic pattern, respectively, at 0.025, 0.05, 0.1, 0.2, 0.4, and 0.8 Hz, corresponding to peak stimulus velocities of 1.25–40°/s for a standard stimulus of ±8°). Slow eye responses were analysed in terms of gain and phase. During SP at mid-frequencies, the eyes were almost perfectly on target (gain 0.98 at 0.1 Hz), independently of a concurrent vestibular or optokinetic stimulus. Pursuit gain at lower frequencies, although being almost ideal (0.98 at 0.025 Hz with pursuit-only stimulation), became modified by the optokinetic input (gain increase above unity when optokinetic stimulus had the same direction as target, decrease with opposite direction). At higher stimulus frequencies, pursuit gain decreased (down to 0.69 at 0.8 Hz), and the pursuit response became modified by vestibular input (gain increase during functionally synergistic combinations, decrease in antagonistic combinations).Thus, the pursuit system in monkey dominates during SP-OKR-VOR interaction, but it does so effectively only in the mid-frequency range. The results can be described in the form of a simple dynamic model in which it is assumed that the three systems interact by linear summation. In the model SP and OKR dominate VOR in the low- to mid-frequency/velocity range, because they represent closed loop systems with high internal gain values (>>1) at these frequencies/velocities, whereas the VOR represents an open loop system with about unity-gain (up to very high frequencies). SP dominance over OKR is obtained by allowing an ’attentional/volitional’ mechanism to boost SP gain and a predictive mechanism to improve its dynamics. Received: 27 November 1998 / Accepted: 8 March 1999     

The velocity response of vestibular nucleus neurons during vestibular,visual, and combined angular acceleration

Summary In alert Rhesus monkeys neuronal activity in the vestibular nuclei was measured during horizontal angular acceleration in darkness, acceleration of an optokinetic stimulus, and combined visual-vestibular stimulation. The working ranges for visual input velocity and acceleration extend up to 60 °/s and 5 °/s². The corresponding working range for vestibular input acceleration is wider and time-dependent. During combined stimulation, that is acceleration of the monkey in the light, a linear relation between neuronal activity and velocity could be established for all neurons. Type I vestibular plus eye movement neurons displayed the greatest sensitivity and had a small linear range of operation. Other vestibular neurons were less sensitive but had a larger range of linear response to different values of acceleration. Accelerating the animal and visual surround, simultaneously but in opposite directions, results in neuronal activity proportional to relative velocity over a limited range.Supported by a grant from the Swiss National Foundation for Scientific Research 3.672-0.77     

Purkinje cell activity in the primate flocculus during optokinetic stimulation,smooth pursuit eye movements and VOR-suppression

Summary Purkinje cell (PC), activity in the flocculus of trained monkeys was recorded during: 1) Vestibular stimulation in darkness. 2) Suppression of the vestibulo-ocular reflex (VOR-supp) by fixation of a small light spot stationary with respect to the monkey. 3) Visual-vestibular conflict (i.e. the visual surround moves together with the monkey during vestibular stimulation), which leads to attenuation or suppression of vestibular nystagmus. 4) Smooth pursuit eye movements. 5) Optokinetic nystagmus (OKN). 6) Suppression of nystagmus during optokinetic stimulation (OKN-supp) by fixation of a small light spot; whereby stimulus velocity corresponds then to image slip velocity.Results were obtained from PCs, which were activated with VOR-supp during rotation to the ipsilateral side. The same PCs were also modulated during smooth pursuit and visual-vestibular conflict. No tonic modulation during constant velocity OKN occurred with slow-phase nystagmus velocities below 40–60 deg/s. Tonic responses were only seen at higher nystagmus velocities. Transient activity changes appeared at the beginning and end of optokinetic stimulation. PCs were not modulated by image slip velocity during OKN-supp.The results show that in primates the same population of floccular PCs is involved in different mechanisms of visual-vestibular interaction and that smooth pursuit and certain components of OKN slow-phase velocity share the same neural pathway. It is argued that the activity of these neurons can neither be related strictly to gaze, eye or image slip velocity; instead, their activity pattern can be best interpreted by assuming a modulation, which is complementary to that of central vestibular neurons of the vestibular nuclei, in the control of slow eye movements.Supported by Swiss National Foundation for Scientific Research 3.343-2.78, and Deutsche Forschungsgemeinschaft, SFB 200, A2     

A comparison of the horizontal and vertical optokinetic reflexes of the rabbit

Summary The horizontal and vertical monocular optokinetic reflexes of the rabbit were measured under closed-loop and open-loop conditions. A random noise, optokinetic stimulus subtending 70×70 deg was presented to the left eye of rabbits placed in front of a rear projection tangent screen. The position of the right eye (nonstimulated) was measured using an infrared light projection technique. During open-loop optokinetic stimulation the eye position signal was fed back to sum with a time-integrated velocity command signal driving the optokinetic stimulus. The dynamics of eye movements evoked by horizontal and vertical optokinetic stimulation were different. Horizontally evoked eye movements never exceeded a deviation of 15 deg before being interrupted by resetting saccades, which returned the eye past the primary position. By contrast, vertical eye deviations greater than 20 deg were often maintained for intervals exceeding 10 s without resetting. The closed-loop gain of optokinetically evoked horizontal eye movements was higher for monocular posterior-anterior optokinetic stimulation than for anterior-posterior stimulation. The vertical optokinetic gain for up-down stimulation was slightly greater than the gain for down-up stimulation. The vertical up-down, open-loop optokinetic gain was greater than the down-up gain over a range of retinal slip velocities of 0.5–5.0 deg/s. Measurement of the horizontal vestibulo-ocular reflex during simultaneous horizontal optokinetic stimulation demonstrated that visual and vestibular information combine linearly to produce reflex eye movements. These data suggest that the higher gain of the horizontal optokinetic reflex may compensate in part for the reduced gain of the horizontal vestibulo-ocular reflex at lower angular accelerations of the head. An equivalent vertical optokinetic gain would be obviated by the contribution of the utricular otoliths to the vertical vestibulo-ocular reflex at low frequencies of head movement.This research was supported by the National Institutes of Health Grant EY00848 and the Oregon Lions Sight and Hearing Foundation     

Optokinetic nystagmus (OKN) and optokinetic after-responses after bilateral vestibular neurectomy in the monkey

Summary The superior branch of the vestibular nerve containing peripheral axons of primary afférents originating in the lateral and anterior semicircular canals was cut bilaterally in three monkeys (vestibular neurectomy). Vertical and horizontal components of eye position were monitored by electro-oculography (EOG) during different stimulus and behavioral paradigms. Postoperatively, monkeys were unable to hold their eyes in eccentric lateral positions in complete darkness. The eyes drifted slowly back to the primary position where eye drift was minimal (null-zone). After vestibular neurectomy the time constant of the eye position integrator in darkness was 4–8 s. Constant velocity optokinetic stimuli produced peak velocities of horizontal OKN that were similar to those before operation. Consistent optokinetic after-responses could not be observed after neurectomy for stimulus durations of less than 60 s. However, with stimulus periods greater than 60–120 s a drift near the primary position of the eyes appeared in darkness which had the same direction as the slow phases of the preceding OKN. Drift velocity was too high to be explained by drift due to the imperfect eye position integrator alone. We assume that drift after prolonged optokinetic stimulation is a combination of an after-response similar as it can be observed after smooth pursuit and of drift due to an imperfect eye position integrator. Secondary optokinetic after-nystagmus was not observed after neurectomy.Supported by Swiss National Foundation for Scientific Research (Nr. 3.718-0.80 and 3.593-0.84)     

Neuronal activity in the flocculus of the alert monkey during sinusoidal optokinetic stimulation

Summary 1. Activity of single units was recorded in the flocculus of alert, behaving monkeys during sinusoidal optokinetic (0.02–5.0 Hz), constant velocity optokinetic, vestibular and visual-vestibular conflict stimulation. The maximal stimulus velocity for sinusoidal optokinetic stimulation at different frequencies was 40 deg/s or less (at frequencies above 1 Hz). For an amplitude series at 0.2 Hz, stimulus velocity was varied between ±10 to ±80 deg/s. In one trained monkey activity was also investigated during smooth pursuit eye movements and suppression of the vestibulo-ocular reflex by visual fixation (VOR-supp.). Only neurons which responded to 0.2 Hz (±40 deg/s) optokinetic stimulation were included in the study. 2. The majority of neurons (44 out of 59) were type I Purkinje cells (PCs), which increased their simple spike activity during optokinetic cylinder rotation to the ipsilateral recording side. The responses during other, vestibular related, paradigms allowed all these neurons to be classified as so called gaze velocity PCs. Three type II PCs were encountered, which responded similarly, but were only weakly modulated. 3. All type I PCs were modulated at frequencies of sinusoidal optokinetic stimulation between 0.05 and 2.5 Hz. PC's showed little or no modulation at 0.03 and 0.02 Hz. About half of the PC's still responded at 5.0 Hz. 4. Relative to eye velocity, the PC activity had a phase advance of about 30 deg between 0.1 and 2 Hz. It became larger at lower, and smaller at higher, frequencies. Eye velocity related sensitivity (imp/s/deg/s) was small at low stimulus frequencies and increased monotonically, on average from 0.16 at 0.02 Hz to 2.0 at 3.3 Hz. 5. Ten (out of 12) mossy fiber related input neurons were classified as visual neurons, since their activity could be related to the amount of retinal slip in all conditions. Neurons were clearly modulated at sinusoidal optokinetic stimulation up to 5 Hz. One input neuron, investigated during sinusoidal OKN, smooth pursuit eye movements, VOR and VOR-supp., behaved qualitatively like a gaze velocity PC. The remaining input neuron encoded eye velocity at 0.2 Hz optokinetic, vestibular and visual-vestibular conflict stimulation. 6. The results show that during sinusoidal and constant velocity optokinetic stimulation gaze velocity PC's do not encode eye velocity and/or eye acceleration. 7. The vestibular nuclei-flocculus complementary hypothesis (Waespe and Henn 1981) can explain PC responses to a large extent. However, a direct comparison shows that at low frequencies (particularly around 0.05 Hz) the complementary responses of most velocity storage encoding vestibular nuclei neurons and floccular PC's appears insufficient to account fully for the oculomotor response.Supported by Deutsche Forschungsgemeinschaft SFB 220, D7R.B. was a Alexander v. Humboldt fellow.     

Conflicting visual-vestibular stimulation and vestibular nucleus activity in alert monkeys

Summary In alert Rhesus monkeys (Macaca mulatta) neuronal activity of vestibular nuclei was recorded during pure vestibular and conflicting visual-vestibular stimulation. Pure vestibular stimulation consisted of rotating the monkey about the vertical axis in complete darkness. During conflicting visual-vestibular stimulation the monkeys were rotated in the light within a vertically striped cylinder mechanically coupled to the turntable. The conflict is that although the monkey is accelerated, there is no relative movement between visual surrounding and the animal. In the conflict situation thresholds of neuronal modulation and of nystagmus were raised compared with those during pure vestibular stimulation. Nystagmus slow-phase velocity could always be dissociated from the neuronal activity, the nystagmus often being totally suppressed whereas the neuronal activity was only attenuated. This suggests a further information processing between vestibular and oculomotor nuclei in the generation of nystagmus.Supported in part by Swiss National Foundation for Scientific Research 3.672-0.77, and Emil Barell-Foundation of Hoffmann-La Roche, Basel, Switzerland     

Firing characteristics of vestibular nuclei neurons in the alert monkey after bilateral vestibular neurectomy

Summary After destruction of the peripheral vestibular system which is not activated by moving large-field visual stimulation, not only labyrinthine-ocular reflexes but also optokinetic-ocular responses related to the velocity storage mechanism are abolished. In the normal monkey optokinetic-ocular responses are reflected in sustained activity changes of central vestibular neurons within the vestibular nuclei. To account for the loss of optokinetic responses after labyrinthectomy, inactivation of central vestibular neurons consequent on the loss of primary vestibular activity is assumed to be of major importance. To test this hypothesis we recorded the neural activity within the vestibular nuclear complex in two chronically prepared Rhesus monkeys during a period from one up to 9 and 12 months after both vestibular nerves had been cut. The discharge characteristics of 829 cells were studied in relation to eye fixation, and to a moving small and large (optokinetic) visual stimulus producing smooth pursuit (SP) eye movements and optokinetic nystagmus (OKN). Units were grouped into different subclasses.After chronic bilateral vestibular neurectomy (BVN) we have found: (1) a rich variety of spontaneously active cells within the vestibular nuclear complex, which — as far as comparison before and after BVN is possible — belong to all subclasses of neurons functionally defined in normal monkey; and (2) no sustained activity changes which are related to the activation of the velocity storage mechanism; this is especially true for pure-vestibular, vestibular-pause and tonic-vestibular-pause cells in normal monkey which show a pure, pause and tonic-pause firing pattern after BVN. Neurons which are modulated by eye position are, however, modulated with the velocity of slow eye movements with comparable sensitivity during SP and OKN. Retinal slip is extremely rarely encoded. The results of the present study do not directly answer the question why the velocity storage mechanism is abolished after BVN but they suggest that only a small number of central vestibular cells may be inactivated by neurectomy.Supported by SNF grant no. 3.510-0.86