Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth-pursuit eye movements and passive head rotation

1978 ◽  
Vol 41 (3) ◽  
pp. 733-763 ◽  
Author(s):  
S. G. Lisberger ◽  
A. F. Fuchs
Keyword(s):  
Eye Movements ◽  
Firing Rate ◽  
Eye Movement ◽  
Smooth Pursuit ◽  
Head Rotation ◽  
Head Velocity ◽  
Rate Modulation ◽  
Cell Firing ◽  
Eye Velocity ◽  
P Cells

1. Extracellular recordings were obtained from 124 Purkinje cells (P-cells) in the flocculus of alert monkeys. P-cell simple spike-firing rate was analyzed quantitatively during various combinations of smooth-pursuit eye movement and passive head rotation. 2. During sinusoidal smooth eye movements, 80% of the P-cells displayed increased firing rate during ipsilateral and 20% during contralateral eye movement. Over the frequency range 0.3--1.4 Hz, firing-rate modulation was proportional to and in phase with maximum eye velocity. During the steady state of triangle-wave tracking, firing rate increased monotonically as a function of eye velocity. Since firing rate was uncorrelated with retinal-error velocity, one component of P-cell firing rate was related to eye velocity. 3. During the transient phase of triangle-wave tracking, when an instantaneous change in the direction of target movement caused a large retinal-error velocity, 40% of the P-cells were related only to eye velocity. Sixty percent of the P-cells displayed an overshoot or undershoot in firing rate, indicating a relationship to either retinal-error velocity or eye acceleration as well as to eye velocity. 4. During the vestibuloocular reflex (VOR), evoked by head rotation in the dark, P-cell firing rate was only weakly modulated. In contrast, when the monkey suppressed the VOR by fixating a target that rotated with him, P-cell rate was deeply modulated. Since the modulation was proportional to and in phase with maximum head velocity, another component of P-cell firing rate was related to head velocity. 5. Of 36 P-cells tested, 35 displayed firing-rate modulation during both suppression of the VOR and smooth-pursuit eye movement. P-cells that reached peak firing rate during ipsilateral head rotation also reached peak firing rate during ipsilateral smooth eye rotation. Average population sensitivitites to head velocity and eye velocity were equal. In three conditions in which eye and head velocity were elicited simultaneously, P-cell firing rate could be predicted by the linear, vector addition of the separate eye and head velocity components of firing rate. Therefore, the relatively weak modulation of P-cell firing rate during the VOR in the dark can be accounted for by the cancellation of equal but opposite head and eye velocity components. 6. The connections of flocculus P-cells to interneurons in the brain stem VOR pathways have been established in other mammals. In the context of those connections, P-cell firing patterns were appropriate to facilitate the eye movements the monkey was required to make. We conclude that the flocculus is important for sustaining any smooth eye movements that are different from those evoked by head rotation in the dark. The eye velocity component may represent an efference copy signal that sustains ongoing eye velocity during smooth pursuit.

Quantitative Analysis of Abducens Neuron Discharge Dynamics During Saccadic and Slow Eye Movements

1999 ◽  
Vol 82 (5) ◽  
pp. 2612-2632 ◽  
Author(s):  
Pierre A. Sylvestre ◽  
Kathleen E. Cullen
Keyword(s):  
Eye Movements ◽  
Firing Rate ◽  
Eye Movement ◽  
Neuronal Activity ◽  
Smooth Pursuit ◽  
Slow Phase ◽  
Vestibular Nystagmus ◽  
Firing Rates ◽  
Rapid Eye Movements ◽  
Eye Velocity

The mechanics of the eyeball and its surrounding tissues, which together form the oculomotor plant, have been shown to be the same for smooth pursuit and saccadic eye movements. Hence it was postulated that similar signals would be carried by motoneurons during slow and rapid eye movements. In the present study, we directly addressed this proposal by determining which eye movement–based models best describe the discharge dynamics of primate abducens neurons during a variety of eye movement behaviors. We first characterized abducens neuron spike trains, as has been classically done, during fixation and sinusoidal smooth pursuit. We then systematically analyzed the discharge dynamics of abducens neurons during and following saccades, during step-ramp pursuit and during high velocity slow-phase vestibular nystagmus. We found that the commonly utilized first-order description of abducens neuron firing rates (FR = b + kE + rE˙, where FR is firing rate, E and E˙ are eye position and velocity, respectively, and b, k, and r are constants) provided an adequate model of neuronal activity during saccades, smooth pursuit, and slow phase vestibular nystagmus. However, the use of a second-order model, which included an exponentially decaying term or “slide” (FR = b + kE + rE˙ + uË − c[Formula: see text]), notably improved our ability to describe neuronal activity when the eye was moving and also enabled us to model abducens neuron discharges during the postsaccadic interval. We also found that, for a given model, a single set of parameters could not be used to describe neuronal firing rates during both slow and rapid eye movements. Specifically, the eye velocity and position coefficients ( r and k in the above models, respectively) consistently decreased as a function of the mean (and peak) eye velocity that was generated. In contrast, the bias ( b, firing rate when looking straight ahead) invariably increased with eye velocity. Although these trends are likely to reflect, in part, nonlinearities that are intrinsic to the extraocular muscles, we propose that these results can also be explained by considering the time-varying resistance to movement that is generated by the antagonist muscle. We conclude that to create realistic and meaningful models of the neural control of horizontal eye movements, it is essential to consider the activation of the antagonist, as well as agonist motoneuron pools.

Discharge patterns in nucleus prepositus hypoglossi and adjacent medial vestibular nucleus during horizontal eye movement in behaving macaques

1992 ◽  
Vol 68 (1) ◽  
pp. 319-332 ◽  
Author(s):  
J. L. McFarland ◽  
A. F. Fuchs
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
Smooth Pursuit ◽  
Vestibular Nucleus ◽  
Medial Vestibular Nucleus ◽  
Eye Position ◽  
Head Velocity ◽  
Firing Rates ◽  
Prepositus Hypoglossi ◽  
Eye Velocity

1. Monkeys were trained to perform a variety of horizontal eye tracking tasks designed to reveal possible eye movement and vestibular sensitivities of neurons in the medulla. To test eye movement sensitivity, we required stationary monkeys to track a small spot that moved horizontally. To test vestibular sensitivity, we rotated the monkeys about a vertical axis and required them to fixate a target rotating with them to suppress the vestibuloocular reflex (VOR). 2. All of the 100 units described in our study were recorded from regions of the medulla that were prominently labeled after injections of horseradish peroxidase into the abducens nucleus. These regions include the nucleus prepositus hypoglossi (NPH), the medial vestibular nucleus (MVN), and their common border (the “marginal zone”). We report here the activities of three different types of neurons recorded in these regions. 3. Two types responded only during eye movements per se. Their firing rates increased with eye position; 86% had ipsilateral “on” directions. Almost three quarters (73%) of these medullary neurons exhibited a burst-tonic discharge pattern that is qualitatively similar to that of abducens motoneurons. There were, however, quantitative differences in that these medullary burst-position neurons were less sensitive to eye position than were abducens motoneurons and often did not pause completely for saccades in the off direction. The burst of medullary burst position neurons preceded the saccade by an average of 7.6 +/- 1.7 (SD) ms and, on average, lasted the duration of the saccade. The number of spikes in the burst was well correlated with saccade size. The second type of eye movement neuron displayed either no discernible burst or an inconsistent one for on-direction saccades and will be referred to as medullary position neurons. Neither the burst-position nor the position neurons responded when the animals suppressed the VOR; hence, they displayed no vestibular sensitivity. 4. The third type of neuron was sensitive to both eye movement and vestibular stimulation. These neurons increased their firing rates during horizontal head rotation and smooth pursuit eye movements in the same direction; most (76%) preferred ipsilateral head and eye movements. Their firing rates were approximately in phase with eye velocity during sinusoidal smooth pursuit and with head velocity during VOR suppression; on average, their eye velocity sensitivity was 50% greater than their vestibular sensitivity. Sixty percent of these eye/head velocity cells were also sensitive to eye position. 5. The NPH/MVN region contains many neurons that could provide an eye position signal to abducens neurons.(ABSTRACT TRUNCATED AT 400 WORDS)

Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. II. Mossy fiber firing patterns during horizontal head rotation and eye movement

1978 ◽  
Vol 41 (3) ◽  
pp. 764-777 ◽  
Author(s):  
S. G. Lisberger ◽  
A. F. Fuchs
Keyword(s):  
Firing Rate ◽  
Eye Movement ◽  
Head Rotation ◽  
Quantitative Comparison ◽  
Eye Position ◽  
Head Velocity ◽  
Firing Rates ◽  
Steady Fixation ◽  
Discharge Patterns ◽  
P Cells

1. Extracellular recordings were obtained from 113 mossu fibers (MFs) in the flocculus of alert monkeys trained to perform a visual tracking task during sinusoidal, horizontal head rotation. The analysis of MF discharge patterns was designed to allow quantitative comparison of the discharge properties of flocculus MFs with brain stem cell populations from which the MFs might originate and with flocculus Purkinje cells (P-cells). Based on their firing patterns, MFs were divided into two classes. Vestibular MFs discharged in relation to head velocity and, in some cases, also in relation to eye movement. Eye movement MFs discharged only in relation to one or more components of eye movement. 2. Vestibular MFs were subdivided into three classes. Vestibular-only MFs (n = 15) displayed a modulation in firing rate during head rotation but exhibited no relationship to spontaneous eye movements. Vestibular-plus-saccade MFs (n = 14) displayed a modulation in firing rate during head rotation that quantitatively resembled the modulation in vestibular-only MFs. In addition, a pause in firing rate interrupted the vestibular modulation during saccades in one or more directions. Vestibular-plus-position MFs (n = 4) exhibited steady firing rates that were linearly related to horizontal eye position in the absence of vestibular stimulation. Sinusoidal head rotation evoked a modulation ofiring rate above and below the firing rate set by the eye position. 3. during sinusoidal head rotation, vestibular MF firing rate led head velocity by an average of 24 degrees. The amplitude of MF firing-rate modulation increased as a function of the frequency of head rotation and, hence, maximum head velocity. Since these characteristics are similar to those displayed by P-cells during suppression of the VOR, vestibular MFs probably transmit the head velocity component of P-cell firing rate to the flocculus. Based on evidence from other mammals and a quantitative comparison of population discharge characteristics, it is likely that vestibular MFs originate from the vestibular nerve and from cells in the medial vestibular nucleus. 4. Based on their discharge patterns, eye movement MFs were also subdivided into three classes. Burst MFs (n = 14) emitted a high-frequency burst of spikes prior to and during saccades in one or more direction, but were silent during steady fixation. Burst-tonic MFs (n = 53) emitted a burst of spikes prior to saccades in a preferred ("on") direction, ceased firing during saccades in the opposite ("off") direction, and exhibited steady firing rates that increased as steady gaze shifted in the on direction. Tonic MFs (n = 13) displayed steady firing rates that increased as the position of steady gaze shifted in the on direction, and either paused or exhibited step changes in firing rate during saccades. 5. During steady fixation, 64% of tonic and burst-tonic MFs were recruited into maintained firing within +/- 10 degrees of the primary direction of gaze...

Purkinje Cells of the Cerebellar Dorsal Vermis: Simple-Spike Activity During Pursuit and Passive Whole-Body Rotation

2002 ◽  
Vol 87 (4) ◽  
pp. 1836-1849 ◽  
Author(s):  
Yasuhiro Shinmei ◽  
Takanobu Yamanobe ◽  
Junko Fukushima ◽  
Kikuro Fukushima
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Spike Activity ◽  
Whole Body ◽  
Body Rotation ◽  
Head Velocity ◽  
Simple Spike ◽  
Group I ◽  
Eye Velocity ◽  
P Cells

To track a slowly moving object during whole body rotation, smooth-pursuit and vestibularly induced eye movements must interact to maintain the accuracy of eye movements in space (i.e., gaze), and gaze movement signals must eventually be converted into eye movement signals in the orbit. To understand the role played by the cerebellar vermis in pursuit-vestibular interactions, in particular whether the output of the vermis codes gaze-velocity or eye-velocity, we examined simple-spike activity of 58 Purkinje (P-) cells in lobules VI–VII of head-stabilized Japanese monkeys that were trained to elicit smooth-pursuit eye movements and cancel their vestibuloocular reflex (VOR) during passive whole body rotation around horizontal, vertical, or oblique axes. All pursuit-sensitive vermal P-cells also responded during VOR cancellation, and the majority of them had peak modulation near peak stimulus velocity. The directions of maximum modulation during these two tasks were distributed in all directions with a downward preponderance. Using standard criteria, 40% of pursuit-sensitive vermal P-cells were classified as gaze-velocity. Other P-cells were classified either as eye/head-velocity group I (36%) that had similar preferred directions during pursuit and VOR cancellation but that had larger responses during VOR ×1 when gaze remained stationary, or as eye/head-velocity group II (24%) that had oppositely directed or orthogonal eye and head movement sensitivity during pursuit and VOR cancellation. Eye/head-velocity group I P-cells contained cells whose activity was correlated with eye velocity. Modulation of many P-cells of the three groups during VOR ×1 could be accounted for by the linear addition of their modulations during pursuit and VOR cancellation. When monkeys fixated a stationary target, over half of the P-cells tested, including gaze-velocity P-cells, discharged in proportion to the velocity of retinal motion of a second spot. These observations are in a striking contrast to our previous results for floccular vertical P-cells. Because we used identical tasks, these differences suggest that the two cerebellar regions are involved in very different kinds of processing of pursuit-vestibular interactions.

Precerebellar Hindbrain Neurons Encoding Eye Velocity During Vestibular and Optokinetic Behavior in the Goldfish

2006 ◽  
Vol 96 (3) ◽  
pp. 1370-1382 ◽  
Author(s):  
James C. Beck ◽  
Paul Rothnie ◽  
Hans Straka ◽  
Susan L. Wearne ◽  
Robert Baker
Keyword(s):  
Firing Rate ◽  
Eye Movement ◽  
Time Course ◽  
Mossy Fiber ◽  
Vestibular Stimulation ◽  
Neuronal Firing ◽  
Velocity Storage ◽  
Head Velocity ◽  
Motor Error ◽  
Eye Velocity

Elucidating the causal role of head and eye movement signaling during cerebellar-dependent oculomotor behavior and plasticity is contingent on knowledge of precerebellar structure and function. To address this question, single-unit extracellular recordings were made from hindbrain Area II neurons that provide a major mossy fiber projection to the goldfish vestibulolateral cerebellum. During spontaneous behavior, Area II neurons exhibited minimal eye position and saccadic sensitivity. Sinusoidal visual and vestibular stimulation over a broad frequency range (0.1–4.0 Hz) demonstrated that firing rate mirrored the amplitude and phase of eye or head velocity, respectively. Table frequencies >1.0 Hz resulted in decreased firing rate relative to eye velocity gain, while phase was unchanged. During visual steps, neuronal discharge paralleled eye velocity latency (∼90 ms) and matched both the build-up and the time course of the decay (∼19 s) in eye velocity storage. Latency of neuronal discharge to table steps (40 ms) was significantly longer than for eye movement (17 ms), but firing rate rose faster than eye velocity to steady-state levels. The velocity sensitivity of Area II neurons was shown to equal (±10%) the sum of eye- and head-velocity firing rates as has been observed in cerebellar Purkinje cells. These results demonstrate that Area II neuronal firing closely emulates oculomotor performance. Conjoint signaling of head and eye velocity together with the termination pattern of each Area II neuron in the vestibulolateral lobe presents a unique eye-velocity brain stem-cerebellar pathway, eliminating the conceptual requirement of motor error signaling.

Eye Movements in Cerebellar and Combined Cerebellobrainstem Diseases

1983 ◽  
Vol 92 (2) ◽  
pp. 165-171 ◽  
Author(s):  
Carsten Wennmo ◽  
Bengt Hindfelt ◽  
Ilmari Pyykkö
Keyword(s):  
Quantitative Analysis ◽  
Eye Movements ◽  
Eye Movement ◽  
Smooth Pursuit ◽  
Optokinetic Nystagmus ◽  
Vestibular Nystagmus ◽  
Full Field ◽  
Eye Velocity ◽  
Voluntary Saccades ◽  
Cerebellar Disorders

We report a quantitative analysis of eye movement disturbances in patients with isolated cerebellar disorders and patients with cerebellar disorders and concomitant brainstem involvement. The most characteristic abnormalities in the exclusively cerebellar patients were increased velocities of the slow phases of vestibular nystagmus induced by rotation in the dark and increased peak velocities of the fast phases of optokinetic nystagmus induced by full-field optokinetic stimuli. Dysmetria of saccades was found in three of six cerebellar patients and gaze nystagmus in all six patients. The typical findings in the combined cerebellobrainstem group were reduced peak velocities of voluntary saccades, defective smooth pursuit and reduced peak velocities of the fast component of nystagmus during rotation in both the dark and light. All patients with combined cerebellobrainstem disorder had dysmetric voluntary saccades and gaze nystagmus. The numbers of superimposed saccades during smooth pursuit were uniformly increased. Release of inhibition in cerebellar disorders may explain the hyperresponsiveness and inaccuracy of eye movements found in this study. In addition, when lesions also involve the brainstem, however, integrative centers coding eye velocity are affected, leading to slow and inaccurate eye movements. These features elicited clinically may be useful in the diagnosis of cerebellar and brainstem disorders.

Dynamic properties of medial rectus motoneurons during vergence eye movements

1992 ◽  
Vol 67 (1) ◽  
pp. 64-74 ◽  
Author(s):  
P. D. Gamlin ◽  
L. E. Mays
Keyword(s):  
Eye Movements ◽  
Firing Rate ◽  
Smooth Pursuit ◽  
Dynamic Properties ◽  
Medial Rectus ◽  
Velocity Signal ◽  
Velocity Sensitivity ◽  
The Difference ◽  
Eye Velocity ◽  
The Relationship

1. An early study by Keller reported that medial rectus motoneurons display a step change in firing rate during accommodative vergence movements. However, a later study by Mays and Porter reported gradual changes in firing rate during symmetrical vergence movements. Furthermore, subsequent inspection of the activity of individual medial rectus motoneurons during vergence movements indicated transient changes in their firing rate that had not been noted by Mays and Porter. For conjugate eye movements, in addition to a position signal, motoneurons display an eye velocity signal that compensates for the characteristics of the oculomotor plant. This suggested that the transient change in firing rate seen during vergence movements represented a velocity signal. Therefore the present study used single-unit recording techniques in alert rhesus monkeys to examine the dynamic behavior of medial rectus motoneurons during vergence eye movements. 2. The relationship between firing rate and eye velocity was first studied for vergence responses to step changes in binocular disparity and accommodative demand. Inspection of single trials showed that medial rectus motoneurons display transient changes in firing rate during vergence eye movements. To better visualize the dynamic signal during vergence movements, an expected firing rate (eye position multiplied by position sensitivity of the cell plus its baseline firing rate) was subtracted from the actual firing rate to yield a difference firing rate, which was displayed along with the eye velocity trace for individual trials. During all smooth symmetrical vergence movements, the profile of the difference firing rate very closely resembled the velocity profile. 3. To quantify the relationship between eye velocity and firing rate, two approaches were taken. In one, peak eye velocity was plotted against the difference firing rate. This plot yielded a measure of the velocity sensitivity of the cell (prv). In the other, a scatter plot was produced in which horizontal eye velocity throughout the vergence eye movement was plotted against the difference firing rate. This plot yielded a second measure of the velocity sensitivity of the cell (rv). 4. The behavior of 10 cells was studied during both sinusoidal vergence tracking and conjugate smooth pursuit over a range of frequencies from 0.125 to 1.0 Hz. This enabled the frequency sensitivity of the medial rectus motoneurons to be assessed for both types of movements. Both vergence velocity sensitivity and smooth pursuit velocity sensitivity decreased with increasing frequency. This is similar to a finding by Fuchs and co-workers for lateral rectus motoneurons during smooth pursuit eye movements.(ABSTRACT TRUNCATED AT 400 WORDS)

Responses during eye movements of brain stem neurons that receive monosynaptic inhibition from the flocculus and ventral paraflocculus in monkeys

1994 ◽  
Vol 72 (2) ◽  
pp. 909-927 ◽  
Author(s):  
S. G. Lisberger ◽  
T. A. Pavelko ◽  
D. M. Broussard
Keyword(s):  
Eye Movements ◽  
Firing Rate ◽  
Brain Stem ◽  
Eye Movement ◽  
Head Rotation ◽  
Eye Position ◽  
Eye Motion ◽  
Ventral Paraflocculus ◽  
Straight Ahead ◽  
Stimulation Of

1. We have identified a group of brain stem cells called “flocculus target neurons” (or FTNs) because they are inhibited at monosynaptic latencies by stimulation of the flocculus and the ventral paraflocculus with single electrical pulses. We report the responses of FTNs, as well as those of other brain stem cells, during horizontal eye movements with the head stationary and during natural vestibular stimulation in monkeys. 2. FTNs discharged primarily in relation to eye movements. The majority (71%) showed increased firing for eye movement away from the side of the recording (“contraversive”), which is consistent with their inhibition by Purkinje cells that show increased firing for eye movement toward the side of recording. However, a significant and surprisingly large percentage (29%) of FTNs showed increased firing for eye movement toward the side of recording (“ipsiversive”). 3. The firing rate of FTNs showed strong modulation during pursuit of sinusoidal target motion with the head stationary and during the compensatory eye movements evoked by fixation of an earth-stationary target with sinusoidal head rotation. In addition, firing rate was related to eye position during steady fixation at different positions. Of the FTNs that showed increased firing for contraversive eye motion during pursuit with the head stationary, most had an infection in the relationship between firing rate and eye position so that the sensitivity to eye position was low for eye positions ipsilateral to straight-ahead gaze and high for eye positions contralateral to straight-ahead gaze. 4. When the monkey canceled the vestibuloocular reflex (VOR) by tracking a target that moved exactly with him during sinusoidal head rotation, the firing rate of FTNs was modulated much less strongly than during pursuit with the head stationary. In the FTNs that showed increased firing for contraversive eye motion during pursuit, firing rate during cancellation of the VOR increased for contraversive head motion during sinusoidal vestibular rotation at 0.4 Hz but was only weakly modulated during rotation at 0.2 Hz. 5. The position-vestibular-pause cells (PVP-cells), previously identified as interneurons in the disynaptic VOR pathways, were not inhibited by stimulation of the flocculus and ventral paraflocculus and had response properties that were different from FTNs. The majority (69%) showed increased firing for contraversive eye motion during pursuit and for ipsiversive head motion during cancellation of the VOR, whereas some (31%) showed the opposite direction preferences under both conditions.(ABSTRACT TRUNCATED AT 250 WORDS)

Discharge properties of brain stem neurons projecting to the flocculus in the alert cat. I. Medical vestibular nucleus

1996 ◽  
Vol 76 (3) ◽  
pp. 1759-1774 ◽  
Author(s):  
G. Cheron ◽  
M. Escudero ◽  
E. Godaux
Keyword(s):  
Eye Movements ◽  
Firing Rate ◽  
Vestibular Nucleus ◽  
Eye Position ◽  
Type I ◽  
Middle Zone ◽  
Head Velocity ◽  
Phase Lead ◽  
Stimulating Electrodes ◽  
Eye Velocity

1. The aim of this study was to characterize the signals transmitted by neurons of the medial vestibular nucleus (MVN) to the middle zone of the flocculus in alert cats. 2. Bipolar stimulating electrodes were implanted into the middle zone of each flocculus, because this zone is known to be involved in the control of horizontal eye movements. Correct implantation of the stimulating electrodes was ensured by 1) recording of Purkinje cells whose activity was related to horizontal eye movements and 2) elicitation of slow abduction of the ipsilateral eye upon electrical stimulation. 3. The rostral two-thirds of the MVN were investigated by microelectrodes during stimulation of both flocculi. Antidromically activated neurons were found only in the central part of the explored area. Forty-four units were activated from the contralateral, eight from the ipsilateral flocculus. Neurons could never be activated from both flocculi. 4. Neurons included in this study were MVN neurons that had 1) to be antidromically activated from one flocculus and 2) to modulate their firing rate during the horizontal vestibuloocular reflex (VOR) elicited by sinusoidal stimulation (0.1 Hz; 10, 20, 30 or 40 degrees). The 39 neurons matching both criteria were classified in 2 groups: 22 neurons changed their firing rate during spontaneous horizontal eye movements (EM-neurons), 17 modulated their activity only during head rotation and were labeled vestibular-only neurons (VO-neurons). 5. Sufficient data were obtained from 13 EM-neurons to allow a quantitative analysis. Among those, 12 were activated from the contralateral and 1 from the ipsilateral flocculus. Their sensitivity to horizontal eye position during intersaccadic fixation was 3.54 +/- 2.75 (SD) spikes.s-1/deg. Eight EM-neurons behaved as type I neurons, five as type II neurons. During the slow phases of the VOR, all of these neurons combined some head-velocity sensitivity (1.50 +/- 0.43 spikes.s-1/deg.s-1) with some horizontal eye-position sensitivity (3.61 +/- 2.45 spikes.s-1/deg). Additionally, seven of these neurons presented a sensitivity to eye velocity (1.34 +/- 0.55 spikes.s-1/deg.s-1). The phase difference between the modulation of firing rate and eye position varied substantially between neurons. The observed phase lead with respect to eye position ranged from 2 to 110 degrees (41.9 +/- 31.8 degrees). 6. Sufficient data were obtained from 10 VO-neurons to allow a quantitative analysis. Among those, nine were activated from the contralateral and one from the ipsilateral flocculus. All of these neurons behaved as type I neurons. The sensitivity to head velocity was 1.64 +/- 1.07 spikes.s-1/deg.s-1. The phase lead of the modulation of spike activity with respect to head velocity ranged from 4.5 to 30.5 degrees (16.4 +/- 8.9 degrees). 7. We conclude that the MVN provides the horizontal zone of the flocculus (with a strong contralateral preference) with information about head velocity (through VO-neurons and EM-neurons) and about eye velocity and position (through EM-neurons).

Dynamics of rabbit vestibular nucleus neurons and the influence of the flocculus

1995 ◽  
Vol 73 (4) ◽  
pp. 1396-1413 ◽  
Author(s):  
J. S. Stahl ◽  
J. I. Simpson
Keyword(s):  
Eye Movements ◽  
Transfer Function ◽  
Firing Rate ◽  
Eye Movement ◽  
Vestibular Nucleus ◽  
Head Rotation ◽  
Medial Vestibular Nucleus ◽  
Eye Position ◽  
Abducens Nucleus ◽  
Nucleus Neuron

1. We recorded single vestibular nucleus neurons shown by electrical stimulation to receive floccular inhibition [flocculus receiving neurons (FRNs)] and/or to project toward midbrain motoneuronal pools [midbrain projecting neurons (MPNs)] in awake, head-fixed rabbits during compensatory eye movements. Stimuli included head rotation in the light, head rotation in the dark, and rotation of an optokinetic drum about the animal. We employed sinusoidal and triangular position profiles in the 0.05- to 0.8-Hz frequency band. We also examined transient responses to step changes in eye position. 2. We found identified vestibular nucleus cells (i.e., FRN/non-MPNs, FRN/MPNs, and non-FRN/MPNs) in the parvocellular and magnocellular portions of the medial vestibular nucleus, at the rostrocaudal level of the dorsal acoustic stria. 3. All identified vestibular nucleus neurons were excited during ipsilateral (relative to side of recording) head rotation and contralateral eye rotation. 4. The neuronal firing rates could be related to eye position and its time derivatives, and that relationship could be approximated by a two-pole, one-zero linear transfer function. As with abducens neurons, a more detailed approximation requires inclusion of two nonlinearities-a hysteresis and a variable sensitivity term that increases as eye movement amplitude decreases. 5. When the vestibuloocular reflex is suppressed by a conflicting full-field visual stimulus [visual vestibular conflict condition (VVC)], vestibular nucleus neuron modulation is largely suppressed. The remaining modulation is motoric in nature, because it can be related to the residual eye movements. Cells with "sensory vestibular signals," i.e., cells whose modulation during VVC correlates better with head rotation than eye movement, were not encountered. 6. We examined the dependence of firing rate parameters on stimulus modality. All neurons exhibited increased phase lead with respect to abducens nucleus neurons during stimuli involving head rotation. This finding could indicate that vestibular-derived inputs are inhomogeneously distributed on premotor neurons and that the studied premotor population receives a stronger vestibular input than another premotor group, not recorded in the current experiments. 7. FRNs and non-FRNs were similar in their qualitative response to the fast phases, the applicability of the two-pole, one-zero transfer function, hysteresis, and the amplitude nonlinearity. 8. FRNs differed from non-FRNs in having a phase advanced firing rate at all stimulus frequencies during visual and vestibular stimuli. The phase difference suggests that one role of the rabbit flocculus is to regulate phase of the net premotor signal.

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