Visual-vestibular interaction in the flocculus of the alert monkey

Neuronal activity in the flocculus of alert Rhesus monkeys was recorded during vestibular stimulation (rotation of the monkey about a vertical axis in complete darkness), optokinetic stimulation (rotation of the visual surround around the stationary monkey), combined visual-vestibular stimulation (rotation of the monkey inside the stationary surround in light), and conflicting visual-vestibular stimulation (rotation of the monkey together with the visual surround in the same direction). The input to the flocculus was recorded as non-Purkinje cell (non-P-cell) activity. Ninety per cent of the non-P-cells which were modulated during our stimulation paradigms carry information similar to that in the neurons of vestibular nuclei. This suggests that the main mossy fiber input to the flocculus originates in the vestibular nuclei. A second input of unknown origin conveys visual information about retinal slip. Thus, part of the flocculus -- as further discussed elsewhere (Waespe and Henn 1981) -- may be specialized to subserve visual-vestibular interaction to improve the nystagmus response.     

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     

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     

Visual-vestibular interaction in the flocculus of the alert monkey

Summary The activity of Purkinje cells (P-cells) was recorded in the flocculus of alert Rhesus monkeys under different conditions of visual-vestibular stimulation. Stimulus conditions were vestibular, optokinetic, combined and conflicting. About 10–20% of all P-cells were activated in their simple spike activity during conflicting stimulation to the recording side (type I) and gave no response or much less during vestibular stimulation. About half of these P-cells were also activated during optokinetic stimulation to the recording side at velocities above 40–60 deg/s. Simple and complex spike activity behaved in a reciprocal way with overlapping but not identical working ranges. Simple spike modulation was unidirectional, complex spike activity always bidirectional. Modulation of simple spike activity cannot be related to one single parameter of the sensory input or the oculomotor output. The hypothesis is put forward that the vestibular nuclei and the flocculus behave in a complementary fashion in processing visual-vestibular information, the flocculus being specialized for high velocity optokinetic nystagmus and suppression of vestibular nystagmus.Supported by a grant from the Swiss National Foundation for Scientific Research 3.343-2.78     

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)     

Response properties of neurons in posterior parietal cortex of monkey during visual-vestibular stimulation. II. Optokinetic neurons

Recordings have been made from single neurons in area 7a or PG (11) in alert monkeys. Studies were limited to those neurons that were activated during optokinetic stimulation in a particular direction but not during foveal pursuit of a small moving target in the dark. Neurons responding in this way were called optokinetic. There was a considerable number of passive visual neurons, which responded to the movement of a visual stimulus during visual fixation but did not respond during optokinetic nystagmus (OKN). Most optokinetic neurons (46/51) also responded during suppression of OKN and usually displayed the same directional preference (43/46). Average discharge rates during constant-velocity optokinetic stimulation in the preferred direction increased monotonically with increases in stimulus velocity in the range 0-60 degrees/s (9/9), and most (7/9) tended to saturate at higher velocities. While the monkey fixated a stationary target light in the dark, most optokinetic neurons (20/24) responded to small moving visual stimuli, and more than half of them (13/20) had the same directional preferences as during OKN. When the chair in which the monkey was seated was oscillated sinusoidally in combination with optokinetic stimulation, most optokinetic neurons seemed to fall into one of two groups; one mainly responded when the animal was oscillated inside a stationary cylinder, and the other when the chair and the lighted cylinder were moved in synchrony together. The results suggest that some of the optokinetic neurons in area 7a or PG may receive extraretinal inputs similar to those that have been suggested to impinge on visual tracking neurons.     

Nystagmus induced by stimulation of the nucleus of the optic tract in the monkey

Summary 1. The nucleus of the optic tract (NOT) was electrically stimulated in alert rhesus monkeys. In darkness stimulation evoked horizontal nystagmus with ipsilateral slow phases, followed by after-nystagmus in the same direction. The rising time course of the slow phase velocity was similar to the slow rise in optokinetic nystagmus (OKN) and to the charge time of optokinetic after-nystagmus (OKAN). The maximum velocity of the steady state nystagmus was approximately the same as that of OKAN, and the falling time course of the after-nystagmus paralled OKAN. 2. Increases in frequency and duration of stimulation caused the rising and falling time constants of the nystagmus and after-nystagmus to become shorter. Changes in the falling time constant of the after-nystagmus were similar to changes in the time constant of OKAN produced by increases in the velocity or duration of optokinetic stimulation. 3. Stimulus-induced nystagmus was combined with OKN, OKAN and per- and post-rotatory nystagmus. The slow component of OKN as well as OKAN could be prolonged or blocked by stimulation, leaving the rapid component of OKN unaffected. Activity induced by electrical stimulation could also sum with activity arising in the semicircular canals to reduce or abolish post-rotatory nystagmus. 4. Positive stimulus sites for inducing nystagmus were located in the posterolateral pretectum. This included portions of NOT that lie in and around the brachium of the superior colliculus and adjacent regions of the dorsal terminal nucleus (DTN). 5. The data indicate that NOT stimulation had elicited the component of OKN which is responsible for the slow rise in slow phase velocity and for OKAN. The functional implication is that NOT, and possibly DTN, are major sources of visual information related to retinal slip in the animal's yaw plane for semicircular canal-related neurons in the vestibular nuclei. Analyzed in terms of a model of OKN and OKAN (Cohen et al. 1977; Waespe et al. 1983), the indirect pathway, which excites the velocity storage mechanism in the vestibular system to produce the slow component of OKN and OKAN, lies in NOT in the monkey, as it probably also does in cat, rat and rabbit. Pathways carrying activity for the rapid rise in slow phase velocity during OKN or for ocular pursuit appear to lie outside NOT.Supported by NIH grants EY02296, EY04148, EY01867 and PSC-CUNY FRAP award 6-63231     

Velocity storage in the vestibulo-ocular reflex arc (VOR)

Summary Vestibular and optokinetic nystagmus (OKN) of monkeys were induced by platform and visual surround rotation. Vision prolonged per-rotatory nystagmus and cancelled or reduced post-rotatory nystagmus recorded in darkness. Presumably, activity stored during OKN summed with activity arising in the semicircular canals. The limit of summation was about 120 °/s, the level of saturation of optokinetic after-nystagmus (OKAN). OKN and vestibular nystagmus, induced in the same or in opposite directions diminished or enhanced post-rotatory nystagmus up to 120 °/s. We postulate that a common storage mechanism is used for producing vestibular nystagmus, OKN, and OKAN. Evidence for this is the similar time course of vestibular nystagmus and OKAN and their summation. In addition, stored activity is lost in a similar way by viewing a stationary surround during either OKAN or vestibular nystagmus (fixation suppression).These responses were modelled using direct pathways and a non-ideal integrator coupled to the visual and peripheral vestibular systems. The direct pathways are responsible for rapid changes in eye velocity while the integrator stores activity and mediates slower changes. The integrator stabilizes eye velocity during whole field rotation and extends the time over which the vestibulo-ocular reflex can compensate for head movement.     

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     

Effects of kainic acid lesions of the nucleus reticularis tegmenti pontis on fast and slow phases of vestibulo-ocular and optokinetic reflexes in the pigmented rat

Summary The nucleus reticularis tegmenti pontis (NRTP) and adjacent pontine reticular formation were lesioned chemically using the neurotoxic agent kainic acid, and the effects of these lesions on horizontal ocular optokinetic and vestibular nystagmus were examined. Eye position was measured in the alert, NRTP-lesioned animals with the electromagnetic search coil technique. Optokinetic and vestibular stimuli consisted of steps of rotations or sinusoidal oscillations of a fullfield visual pattern surrounding the animal or of the animal in total darkness, respectively. In a first group of animals, small unilateral NRTP lesions were produced by placing a single kainic acid injection in the area of the left NRTP. In one third of the animals, ipsilateral quick phases of optokinetic and vestibular nystagmus were abolished. In the remaining animals, quick phases were deficient to various degrees or not affected at all. There were no changes in the characteristics of optokinetic step responses to ipsilateral pattern rotations which activate predominantly optokinetic pathways on the side of the brainstem lesion. In animals with ipsiversive quick phase deficits, contralateral pattern rotations elicited tonic eye deviations. In a second group of animals, large uni- or bilateral lesions were produced by injecting kainic acid into three separate rostral, middle and caudal levels of the right NRTP. These animals had uni- or bilateral quick phase deficits during optokinetic and vestibular nystagmus. Optokinetic nystagmus in response to velocity steps of pattern rotation towards the lesion side was strongly reduced in gain even in those animals that had no apparent deficits in the fast contraversive reset phases. In four out of six animals, responses to sinusoidal optokinetic pattern oscillations were reduced in gain and showed increased phase lags compared to controls. Vestibulo-ocular responses to velocity steps of head rotations were of normal gain but reduced in duration (measured from onset of stimulation to reversal of nystagmus). Sinusoidal vestibulo-ocular responses evoked by head oscillations exhibited reduced gain values and strongly increased phase leads in the frequency range below 0.5 Hz. The vestibular time constant was found to be around 4.5 s in animals with NRTP lesions compared to about 7.5 s in control animals. The present results show that large kainic acid lesions of the NRTP (and adjacent area) do not abolish optokinetic eye movements in the rat, in contrast to what has been reported after electrolytic lesions. The data suggest, however, that there is a failure of slow build-up of OKN slow phase velocity as well as a shortening of the vestibular time constant which correlates with the kainic acid lesions extending into rostromedial and caudal parts of the NRTP. The implications of these findings with respect to an involvement of these structures in velocity storage are discussed.Abbreviations CN cochlear nucleus - DpSC decussation, peduncle, superior, cerebellar - ip interpeduncular nucleus - MLF medial longitudinal fasciculus - NOT nucleus of optic tract - NRTPc nucleus reticularis tegmenti pontis, central subdivision - NRTPp nucleus reticularis tegmenti pontis, pericentral subdivision - p pontine nuclei - ph praepositus hypoglossi nucleus - pMC peduncle, middle cerebellar - pSC peduncle, superior cerebellar - Pyr pyramidal tract - Rcs raphe central superior - Rm raphe magnus - rpc reticular nucleus, pontine, caudal - rpo reticular nucleus, pontine, oral - TB trapezoid body - tM trapezoid nucleus, medial - tGd tegmental nucleus of von Gudden, dorsal - tGv tegmental nucleus of von Gudden, ventral - 5 trigeminal tract or trigeminal nerve - 5m mesencephalic trigeminal nucleus - 5mt motor trigeminal nucleus - 6n abducens nucleus - 7 facial nerve Prof. W. Precht died on March 12, 1985     

Resetting fast phases of head and eye and their linkage in the frog

Summary (1) Compensatory slow phase movements were evoked by optokinetic, vestibular and combined optokinetic and vestibular stimulation. Superimposed fast phases resetting the position of the head (in space) and of the eye (in head) were recorded with a magnetic field search coil in unrestrained and head fixed frogs, respectively. (2) Head fast phases recorded during optokinetic stimulation covaried in the frequency of their occurrence with slow phase head velocity. Their amplitude was large (average 18.9 ±8.9 °), maximal velocity increased with amplitude by 6.67 °/deg, and duration (average 230 ±33 ms) was almost independent on amplitude. (3) Ocular fast phases rarely occurred during sinusoidal stimulation and neither optokinetic after nystagmus nor postrotatory nystagmus were observed. Fast phases, evoked by constant velocity optokinetic or acceleratory stimuli, consisted of two components: a primary resetting fast phase and a smaller fast movement in the opposite direction. The primary fast phase had a small amplitude (average 2.2 ±1.3 °). In different stimulus conditions fast phase parameters were very similar. Maximal velocity increased by 6.5 °/s/deg. Duration (average 165 ±23.4 ms) was variable. (4) During ocular fast phases the vestibulo-collic and the optokinetic-collic reflexes were suppressed. The slow phase head velocity either became zero or a small head fast phase in the direction of the ocular fast phase occurred. Fast phase head movements were accompanied by an ocular fast phase or by a retraction of one or both eyes, depending on the amplitude of the head fast phase. At the end of a head fast phase eye position was always recentered.Supported by grants from Deutsche Forschungsgemeinschaft (Pr158/2) and Swiss National Science Foundation (3.505.79 and 3.616.80)     

Vestibular-related neuronal activity in the thalamus of the alert monkey during sinusoidal rotation in the dark

1. In the alert monkey neuronal activity was recorded in the ventro-posterior nucleus (VP) of the thalamus in the dark during sinusoidal rotation over a frequency range from 0.01-1 Hz. 2. From 57 neurons 38 (67%) were activated with rotation to the ipsilateral side (type I) and 19 (33%) to the contralateral side (type II). The spontaneous activity was low (average 10.1 imp/sec) and irregular. No activity changes were found with eye movements. 3. At 0.2-0.1 Hz neuronal activity showed a phase lead of 10-20 degrees relative to chair velocity. At the lowest frequency (0.01 Hz) the phase lead was only slightly higher (about 30 degrees). Accordingly the decrease in gain was only moderate. 4. At lower frequencies the simultaneously recorded eye movements (nystagmus) showed an increase in phase lead comparable to the values for the neuronal activity in the thalamus. For both neuronal activity in the thalamus and nystagmus a time constant between 25-35 sec was calculated. 5. The data are compared with vestibular nerve and nuclei recordings. It is argued that the time constants of vestibular neurons in the thalamus are very similar to the time constants of neurons in the vestibular nuclei in alert animals.     

The effect of muscimol micro-injections into the fastigial nucleus on the optokinetic response and the vestibulo-ocular reflex in the alert monkey

Eye movements of four macaque monkeys were investigated after unilateral micro-injections of the GABA agonist muscimol (1 g in 1 l NaCl) into the caudal fastigial nucleus, i.e. the fastigial oculomotor region. Spontaneous eye movements in the dark and in the light were tested, as well as those evoked by vestibular stimulation in the dark (sinusoidal: 0.1–0.2 Hz, ±40–100 deg/s, velocity trapezoid acceleration 40 deg/s², constant velocity 120 deg/s), optokinetic stimulation (sinusoidal: 0.1–0.2 Hz, ±40–100 deg/s, constant velocity 60–100 deg/s), and visual-vestibular conflict stimulation. With these stimuli, smooth pursuit mechanisms (fast build-up of optokinetic slow phase velocity), the vestibulo-ocular reflex (VOR) and the velocity storage mechanism were investigated. Muscimol injections consistently led to specific eye movement changes which were maximal 30–60 min after the injection and lasted 4–6 h. The fast initial rise of OKN slow phase velocity to the contralateral side decreased by 45% (range 24%–82%) of its pre-injection value, while it was virtually unaltered on the ipsilateral side (average decrease of 1%, range from a decrease of 20% to an increase of 32%). For conflict ramp stimulation, the suppression of vestibular nystagmus was less (decrease of 50%, range 12–82%) towards the contralateral side while it remained unchanged on the ipsilateral side. The VOR in the dark and the velocity storage mechanism were not altered. For the latter, the slow build-up of optokinetic nystagmus velocity, the optokinetic afternystagmus (OKAN) and the time constant of decay for the vestibular nystagmus were evaluated. There was no spontaneous nystagmus in the light or dark and no gazeholding deficit. These data support evidence that the fastigial oculomotor region contributes direction-specifically to smooth pursuit mechanisms, without affecting the VOR and the velocity storage mechanism.     

Role of the flocculus and paraflocculus in optokinetic nystagmus and visual-vestibular interactions: Effects of lesions

Optokinetic nystagmus (OKN), optokinetic after-nystagmus (OKAN), vestibular nystagmus and visual-vestibular interactions were studied in monkeys after surgical ablation of the flocculus and paraflocculus. After bilateral flocculectomy the initial rapid rise in slow phase eye velocity of horizontal and vertical OKN was severely attenuated, and maximum velocities fell to the preoperative saturation level of OKAN. There is generally little or no upward OKAN in the normal monkey, and upward OKN was lost after bilateral lesions. Unilateral flocculectomy affected the rapid rise in horizontal velocity to both sides. Consistent with the absence of a rapid response to steps of surround velocity, animals were unable to follow acceleration of the visual field with eye accelerations faster than about 3-5 degrees/s2. The slow rise in OKN slow phase velocity to a steady state level was prolonged after operation. However, rates of rise were approximately equal for the same initial retinal slips before and after operation. The similarity in the time course of OKN when adjusted for initial retinal slip, and in the gain, saturation level and time course of OKAN before and after flocculectomy indicates that the lesions had not significantly altered the coupling of the visual system to the velocity storage integrator or its associated time constant. When animals were rotated in a subject-stationary visual surround after flocculectomy, they could not suppress the initial jump in eye velocity at the onset of the step. Despite this, they could readily suppress the subsequent nystagmus. The time constant of decline in the conflict situations was almost as short as in the normal monkey and was in the range of the peripheral vestibular time constant. This suggests that although the animals were unable to suppress rapid changes in eye velocity due to activation of direct vestibulo-oculomotor pathways, they had retained their ability to discharge activity from the velocity storage mechanism. Consistent with this, animals had no difficulty in suppressing OKAN after flocculectomy. Visual-vestibular interactions utilizing the velocity storage mechanism were normal after flocculectomy, as was nystagmus induced by rotation about a vertical axis or about axes tilted from the vertical. Also unaffected were the discharge of nystagmus caused by tilting the head out of the plane of the response and visual suppression of nystagmus induced by off-vertical axis rotation. The flocculus does not appear to play an important role in mediating these responses. The data before and after flocculectomy were simulated by a model which is homeomorphic to that presented previously.(ABSTRACT TRUNCATED AT 400 WORDS)     

Transfer characteristics of neurons in vestibular nuclei of the alert monkey.

1. In the alert monkey, 74 neurons in the vestibular nuclei were investigated during sinusoidal rotation about a vertical axis at frequencies between 0.003 and 0.5 Hz. Phase and gain were determined by a fast Fourier analysis program. 2. Phase advance, relative to turntable velocity, was small between 0.05 and 0.5 Hz. At lower frequencies phase advance increased to 45 degrees at 0.007--0.02 Hz, and 90 degrees at 0.003--0.005 Hz. In agreement with the phase characteristics, a gain decrease of -3 dB was determined between 0.007 and 0.02 Hz. Assuming a linear system, time constants of 9.5, 11.9, and 24.5 s were calculated for three different monkeys. 3. Simultaneously recorded nystagmus exhibited similar time constants as the central vestibular neurons for each monkey. 4. Frequency responses of 11 neurons were recorded from the same monkeys while they were under general anesthesia and the time constants were reduced to 4--7 s. This is the range of time constants seen in the peripheral nerve. 5. The longer time constants in the alert state are due to an integration process, which provides a low-frequency compensation, and is thought to be achieved through a feedback loop involving the reticular formation. 6. In the alert and anesthetized state, monkeys were also exposed to velocity trapezoids. Time constants of decay of neuronal activity were in good agreement with the data obtained during sinusoidal stimulation. 7. A transfer function of the primary vestibular afferents is expanded to include the described low-frequency compensation found in central vestibular neurons in the alert animals.     

Role of irregular otolith afferents in the steady-state nystagmus during off-vertical axis rotation.

1. During constant velocity off-vertical axis rotations (OVAR) in the dark a compensatory ocular nystagmus is present throughout rotation despite the lack of a maintained signal from the semicircular canals. Lesion experiments and canal plugging have attributed the steady-state ocular nystagmus during OVAR to inputs from the otolith organs and have demonstrated that it depends on an intact velocity storage mechanism. 2. To test whether irregularly discharging otolith afferents play a crucial role in the generation of the steady-state eye nystagmus during OVAR, we have used anodal (inhibitory) currents bilaterally to selectively and reversibly block irregular vestibular afferent discharge. During delivery of DC anodal currents (100 microA) bilaterally to both ears, the slow phase eye velocity of the steady-state nystagmus during OVAR was reduced or completely abolished. The disruption of the steady-state nystagmus was transient and lasted only during the period of galvanic stimulation. 3. To distinguish a possible effect of ablation of the background discharge rates of irregular vestibular afferents on the velocity storage mechanism from specific contributions of the dynamic responses from irregular otolith afferents to the circuit responsible for the generation of the steady-state nystagmus, bilateral DC anodal galvanic stimulation was applied during optokinetic nystagmus (OKN) and optokinetic afternystagmus (OKAN). No change in OKN and OKAN was observed.(ABSTRACT TRUNCATED AT 250 WORDS)     

Nystagmus induced by electrical stimulation of the vestibular and prepositus hypoglossi nuclei in the monkey: evidence for site of induction of velocity storage

Summary Electrical stimulation of the vestibular nuclei (VN) and prepositus hypoglossi nuclei (PPH) of alert cynomolgus monkeys evoked nystagmus and eye deviation while they were in darkness. At some sites in VN, nystagmus and after-nystagmus were induced with characteristics suggesting that velocity storage had been excited. We analyzed these responses and compared them to the slow component of optokinetic nystagmus (OKN) and to optokinetic after-nystagmus (OKAN). We then recorded unit activity in VN and determined which types of nystagmus would be evoked from the sites of recording. Nystagmus and eye deviations were also elicited by electrical stimulation of PPH, and we characterized the responses where unit activity was recorded in PPH. Horizontal slow phase velocity of the VN storage responses was contralateral to the side of stimulation. The rising time constants and peak steady-state velocities were similar to those of OKN, and the falling time constants of the after-nystagmus and of OKAN were approximately equal. Both the induced after-nystagmus and OKAN were habituated by stimulation of the VN. When horizontal after-nystagmus was evoked with animals on their sides, it developed yaw and pitch components that tended to shift the vector of the slow phase velocity toward the spatial vertical. Similar cross-coupling occurs for horizontal OKAN or for vestibular post-rotatory nystagmus elicited in tilted positions. Thus, the storage component of nystagmus induced by VN stimulation had the same characteristics as the slow component of OKN and the VOR. Positive stimulus sites for inducing nystagmus with typical storage components were located in rostral portions of VN. They lay in caudal ventral superior vestibular nucleus (SVN), dorsal portions of central medial vestibular nucleus (MVN) caudal to the abducens nuclei and in adjacent lateral vestibular nucleus (LVN). More complex stimulus responses, but with contralateral after-nystagmus, were induced from surrounding regions of ventral MVN and LVN, rostral descending vestibular nucleus and the marginal zone between MVN and PPH. Vestibular-only (VO), vestibular plus saccade (VPS) and tonic vestibular pause (TVP) units were identified by extracellular recording. Stimulation near type I lateral and vertical canalrelated VO units elicited typical storage responses with after-nystagmus in 23 of 29 tracks (79%). Stimulus responses were more complex from the region of neurons with oculomotor-related signals, i.e., TVP or VPS cells, although after-nystagmus was also elicited from these sites. Effects of vestibular nerve and nucleus stimulation were compared. Nerve stimulation evoked nystagmus with both a rapid and slow component and after-nystagmus. There was a more prominent rapid rise in slow phase velocity, higher peak velocities, shorter latencies and a shorter falling time constant from nerve than from nucleus stimulation. This indicates more prominent activation of rapid pathways from nerve stimulation. From a comparison of nerve- and nucleus-induced nystagmus, we infer that there was predominant activation of the network responsible for velocity storage by electrical stimulation at many sites in the VN. Microstimulation at sites in PPH elicited nystagmus with ipsilateral slow phases or ipsilateral eye deviations. Slow phase eye velocity changed rapidly at the onset of nystagmus, and peak eye velocities were about 10–15°/s lower than from VN stimulation. The nystagmus had no slow component, and it was not followed by after-nystagmus. Only burst or burst-tonic neurons were recorded in PPH. Stimulation at sites of recording of these units induced either nystagmus with a rapid component or ipsilateral eye deviation. We conclude that the slow component of optokinetic and vestibular nystagmus, attributable to velocity storage is produced in the VN, not in the PPH. We postulate that VO neurons lying in caudal ventral portions of SVN, dorsal portions of MVN and adjacent LVN are part of the network that generates velocity storage.     

Discharge patterns of neurons in the pretectal nucleus of the optic tract (NOT) in the behaving primate

1. To determine the possible role of the primate pretectal nucleus of the optic tract (NOT) in the generation of optokinetic and smooth-pursuit eye movements, we recorded the activity of 155 single units in four behaving rhesus macaques. The monkeys were trained to fixate a stationary target spot during visual testing and to track a small moving spot in a variety of visual environments. 2. The majority (82%) of NOT neurons responded only to visual stimuli. Most units responded vigorously for large-field (70 x 50 degrees) moving visual stimuli and responded less, if at all, during smooth-pursuit eye movements in the dark; many of these units had large receptive fields (greater than 10 x 10 degrees) that included the fovea. The remaining visual units responded more vigorously during smooth-pursuit eye movements in the dark than during movement of large-field visual stimuli; all but one had small receptive fields (less than 10 x 10 degrees) that included the fovea. For all visual units that responded during smooth pursuit, extinction of the small moving target so briefly that pursuit continued caused the firing rates to drop to resting levels, confirming that the discharge was due to visual stimulation of receptive fields with foveal and perifoveal movement sensitivity and not to smooth-pursuit eye movements per se. 3. Eighteen percent of all NOT units ceased their tonic discharge in association with all saccades including the quick phases accompanying optokinetic or vestibular nystagmus. The pause in firing began after saccade onset, was unrelated to saccade duration, and occurred even in complete darkness. 4. Most (90%) of the visual NOT units were direction selective. They exhibited an increase in firing above resting during horizontal (ipsilateral) background movement and/or during smooth pursuit of a moving spot and a decrease in firing during contralateral movement. 5. The firing rates of NOT units were highly dependent on stimulus velocity. All had velocity thresholds of less than 1 degree/s and exhibited a monotonic increase in firing rate with visual stimulus velocity over part (n = 90%) or all (n = 10%) of the tested range (i.e., 1-200 degrees/s). Most NOT units exhibited velocity tuning with an average preferred velocity of 64 degrees/s.(ABSTRACT TRUNCATED AT 400 WORDS)     

Asymmetries of vertical vestibular nystagmus in the cat

Summary In the cat, the asymmetry of vertical nystagmus in response to a rotation around the Yaxis has been characterized by measuring the beat frequency and gain of vestibulo-ocular reflexes in each direction (upward and downward). Sinusoidal variations of head velocity or velocity steps have been applied under three visual conditions (a) in darkness (pure vestibular stimulation); (b) in the light (mixed vestibular and optokinetic stimulation); (c) with a mirror placed in front of the animal; since the mirror image moved with the head, the animal was provided with a stable visual cue (stabilized vision). In all three conditions, beat frequency and gain were greater for downward than for upward nystagmus (the direction refers to that of the quick phase). In darkness, the characteristics of postrotatory nystagmus suggested a greater time constant for downward than for upward vestibulo-ocular reflexes. In the light, both stimuli acted synergistically. In stabilized vision, upward vestibular nystagmus was preferentially suppressed, suggesting an algebraic summation of the effects arising from both kinds of stimuli.This project was supported by CNRS ATP internationale and Greco 17; J. López-Barneo (Sevilla, Spain) received an ETP training grant     

Characteristics of eye velocity storage during periods of suppression and reversal of eye velocity in monkeys

Summary An eye velocity storage mechanism has been postulated in the vestibulo-optokinetic system to account for the prolongation of vestibular nystagmus (VN) and the occurrence of optokinetic afternystagmus (OKAN). Presentation of a subject-stationary full-field surround during VN and OKAN (= full-field fixation) rapidly reduces activity related to eye velocity of the storage mechanism. If the subject-stationary full-field surround is presented for short periods during VN or OKAN, nystagmus resumes when the animal is again in darkness, but at a lesser velocity than would be predicted from a control response. This reduction in peak eye velocity after fixation reflects a decrease in activity of the storage mechanism due to full-field fixation. This decrease in activity occurs with a shorter time constant compared to that in control trials, it has been called dumping. We demonstrate that a subject-stationary small target light presented during VN or OKAN (= target fixation) also reduces activity of the storage mechanism with a time constant slightly greater than that for full-field fixation, but still considerably smaller than that in control trials. In 3 monkeys the time constant of discharge was reduced during the post-rotatory period from 20 s in control trials to 4.6 s by fixation of a single target light and to 2.9 s by fixation of a full-field. The time constant of discharge was reduced during OKAN from 13.2 s in control trials to 3.8 s by target fixation and to 2.6 s by full-field fixation. We report a second experimental paradigm with which the dynamics of visual-vestibular interaction involving the eye velocity storage mechanism is analysed by means of transient step responses. In this paradigm eye velocity due to activation of the storage mechanism (OKAN) is forced to reverse by a short exposure to a full-field moving in the opposite direction of the slow phases of nystagmus. Short periods of eye velocity reversal did not reduce activity of the storage mechanism more rapidly than fixation, i.e. suppression of eye velocity alone. Fixation of a full-field or of a single target light during vestibular or optokinetic stimulation reduces peak nystagmus velocity after stimulation when monkeys are in darkness. Suppression of OKN by target fixation during full-field stimulation reduces the initial eye velocity of OKAN to 15–20% compared to the OKAN velocity when OKN is allowed to occur. Fixation during vestibular or optokinetic stimulation obviously inhibits full activation of the eye velocity storage mechanism. The results are discussed in relation to current models of visual-vestibular interaction.Supported by Swiss National Foundation for Scientific Research (no. 3.593-0.84)