Effects of Viewing Distance on the Responses of Horizontal Canal–Related Secondary Vestibular Neurons During Angular Head Rotation

1999 ◽  
Vol 81 (5) ◽  
pp. 2517-2537 ◽  
Author(s):  
Chiju Chen-Huang ◽  
Robert A. McCrea
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
Head Rotation ◽  
Vestibular Nerve ◽  
Viewing Distance ◽  
Vestibuloocular Reflex ◽  
Horizontal Canal ◽  
Head Velocity ◽  
Firing Behavior ◽  
Vestibular Neurons

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

Effects of Viewing Distance on the Responses of Vestibular Neurons to Combined Angular and Linear Vestibular Stimulation

1999 ◽  
Vol 81 (5) ◽  
pp. 2538-2557 ◽  
Author(s):  
Chiju Chen-Huang ◽  
Robert A. McCrea
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
Vestibular Stimulation ◽  
The Other ◽  
Viewing Distance ◽  
Vestibuloocular Reflex ◽  
Horizontal Canal ◽  
Head Velocity ◽  
Vestibular Neurons ◽  
Axis Of Rotation

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

Effect of viewing distance and location of the axis of head rotation on the monkey's vestibuloocular reflex. I. Eye movement responses

1992 ◽  
Vol 67 (4) ◽  
pp. 861-874 ◽  
Author(s):  
L. H. Snyder ◽  
W. M. King
Keyword(s):  
Eye Movement ◽  
Visual Target ◽  
Head Rotation ◽  
Rotational Axis ◽  
Viewing Distance ◽  
Vestibuloocular Reflex ◽  
Velocity Signal ◽  
Head Velocity ◽  
Axis Of Rotation ◽  
Pure Delay

1. The vestibuloocular reflex (VOR) stabilizes images on the retina against movements of the head in space. Viewing distance, target eccentricity, and location of the axis of rotation may influence VOR responses because rotation of the head about most axes in space rotates and translates the eyes relative to visual targets. To study the VOR response to combined rotation and translation, monkeys were placed on a rate table and rotated briefly in the dark about a vertical axis that was located in front of or behind the eyes. The monkeys fixated a near or far visual target that was extinguished before the rotation. Eye movements were recorded from both eyes by the use of the search coil technique. 2. Peak eye velocity evoked by the VOR was linearly related to vergence angle for any axis of rotation. The percent change in the VOR with near target viewing relative to far target viewing at a vergence angle of 20 degrees was linearly related to the location of the axis of rotation. Axes located behind the eyes produced positive changes in VOR amplitude, and axes located in front of the eyes produced negative changes in VOR amplitude. An axis of rotation located in the coronal plane containing the centers of rotation of the eyes produced no modification of VOR amplitude. For any axis, the VOR compensated for approximately 90% of the translation of the eye relative to near targets. 3. The initial VOR response was not correct in magnitude but was refined by a series of three temporally delayed corrections of increasing complexity. The earliest VOR-evoked eye movement (10-20 ms after rotation onset) was independent of viewing distance and rotational axis location. In the next 100 ms, eye speed appeared to be sequentially modified three times: within 20 ms by viewing distance; within 30 ms by otolith translation; and within 100 ms by eye translation relative to the visual target. 4. These data suggest a formal model of the VOR consisting of four channels. Channel 1 conveys an unmodified head rotation signal with a pure delay of 10 ms. Channel 2 conveys an angular head velocity signal, modified by viewing distance with a pure delay of 20 ms, but invariant with respect to the location of the axis of rotation. Channel 3 conveys a linear head velocity signal, dependent on the location of the axis of rotation, that is modified by viewing distance with a pure delay of 30 ms.(ABSTRACT TRUNCATED AT 400 WORDS)

Firing Behavior of Vestibular Neurons During Active and Passive Head Movements: Vestibulo-Spinal and Other Non-Eye-Movement Related Neurons

1999 ◽  
Vol 82 (1) ◽  
pp. 416-428 ◽  
Author(s):  
Robert A. McCrea ◽  
Greg T. Gdowski ◽  
Richard Boyle ◽  
Timothy Belton
Keyword(s):  
Electrical Stimulation ◽  
Eye Movement ◽  
Head Rotation ◽  
Head Movements ◽  
Whole Body ◽  
Body Rotation ◽  
Firing Behavior ◽  
Vestibular Neurons ◽  
Gaze Saccades ◽  
Stimulation Of

The firing behavior of 51 non-eye movement related central vestibular neurons that were sensitive to passive head rotation in the plane of the horizontal semicircular canal was studied in three squirrel monkeys whose heads were free to move in the horizontal plane. Unit sensitivity to active head movements during spontaneous gaze saccades was compared with sensitivity to passive head rotation. Most units (29/35 tested) were activated at monosynaptic latencies following electrical stimulation of the ipsilateral vestibular nerve. Nine were vestibulo-spinal units that were antidromically activated following electrical stimulation of the ventromedial funiculi of the spinal cord at C1. All of the units were less sensitive to active head movements than to passive whole body rotation. In the majority of cells (37/51, 73%), including all nine identified vestibulo-spinal units, the vestibular signals related to active head movements were canceled. The remaining units ( n = 14, 27%) were sensitive to active head movements, but their responses were attenuated by 20–75%. Most units were nearly as sensitive to passive head-on-trunk rotation as they were to whole body rotation; this suggests that vestibular signals related to active head movements were cancelled primarily by subtraction of a head movement efference copy signal. The sensitivity of most units to passive whole body rotation was unchanged during gaze saccades. A fundamental feature of sensory processing is the ability to distinguish between self-generated and externally induced sensory events. Our observations suggest that the distinction is made at an early stage of processing in the vestibular system.

Integration of Vestibular and Head Movement Signals in the Vestibular Nuclei During Whole-Body Rotation

1999 ◽  
Vol 82 (1) ◽  
pp. 436-449 ◽  
Author(s):  
Greg T. Gdowski ◽  
Robert A. McCrea
Keyword(s):  
Eye Movement ◽  
Head Rotation ◽  
Vestibular Nuclei ◽  
Head Movements ◽  
Whole Body ◽  
Body Rotation ◽  
Horizontal Semicircular Canal ◽  
Head Velocity ◽  
Vestibular Neurons ◽  
Single Unit Recordings

Single-unit recordings were obtained from 107 horizontal semicircular canal-related central vestibular neurons in three alert squirrel monkeys during passive sinusoidal whole-body rotation (WBR) while the head was free to move in the yaw plane (2.3 Hz, 20°/s). Most of the units were identified as secondary vestibular neurons by electrical stimulation of the ipsilateral vestibular nerve (61/80 tested). Both non–eye-movement ( n = 52) and eye-movement–related ( n = 55) units were studied. Unit responses recorded when the head was free to move were compared with responses recorded when the head was restrained from moving. WBR in the absence of a visual target evoked a compensatory vestibulocollic reflex (VCR) that effectively reduced the head velocity in space by an average of 33 ± 14%. In 73 units, the compensatory head movements were sufficiently large to permit the effect of the VCR on vestibular signal processing to be assessed quantitatively. The VCR affected the rotational responses of different vestibular neurons in different ways. Approximately one-half of the units (34/73, 47%) had responses that decreased as head velocity decreased. However, the responses of many other units (24/73) showed little change. These cells had signals that were better correlated with trunk velocity than with head velocity. The remaining units had responses that were significantly larger (15/73, 21%) when the VCR produced a decrease in head velocity. Eye-movement–related units tended to have rotational responses that were correlated with head velocity. On the other hand, non–eye-movement units tended to have rotational responses that were better correlated with trunk velocity. We conclude that sensory vestibular signals are transformed from head-in-space coordinates to trunk-in-space coordinates on many secondary vestibular neurons in the vestibular nuclei by the addition of inputs related to head rotation on the trunk. This coordinate transformation is presumably important for controlling postural reflexes and constructing a central percept of body orientation and movement in space.

Neuronal activity in the ipsilateral vestibular nucleus following unilateral labyrinthectomy in the alert guinea pig

1995 ◽  
Vol 74 (5) ◽  
pp. 2087-2099 ◽  
Author(s):  
L. Ris ◽  
C. de Waele ◽  
M. Serafin ◽  
P. P. Vidal ◽  
E. Godaux
Keyword(s):  
Guinea Pig ◽  
Vestibular Nucleus ◽  
Head Rotation ◽  
Second Order ◽  
Vestibular Nerve ◽  
Control Group ◽  
Head Velocity ◽  
Vestibular Neurons ◽  
Unilateral Labyrinthectomy ◽  
Control State

1. Neuronal activity was investigated in the left superior vestibular nucleus (SVN), lateral vestibular nucleus (LVN), and rostral part of the medial vestibular nucleus (MVN) in the alert guinea pig after a unilateral (left) labyrinthectomy was performed. Vestibular neurons were recorded either immediately (just-postoperative group, n = 6) or 1 wk after labyrinthectomy (1-wk-postoperative group, n = 6) and compared with the activity recorded in intact animals (control group, n = 6). 2. Animals were prepared for extracellular recording of single-unit activity and for eye movement recording (scleral search coil technique). To enable stimulation of the left vestibular nerve, bipolar silver ball electrodes were chronically implanted either in contact with the bony labyrinth in the control group or close to the stump of the vestibular nerve after labyrinthectomy. Complete labyrinthectomy was performed under halothane anesthesia. 3. The criterion used to select vestibular neurons for analysis was their recruitment by an electric shock on the vestibular nerve. Of the 589 recorded neurons, 424, defined as second-order vestibular neurons, were recruited at monosynaptic latencies (0.85-1.15 ms) and 165 were recruited at polysynaptic latencies. One hundred three second-order vestibular neurons were recorded in the control group, 173 in the just-postoperative group, and 148 in the 1-wk-postoperative group. 4. The activity of the electrically recruited neurons was recorded during sinusoidal horizontal head rotation in the dark (0.3 Hz, 40 degrees/s peak velocity). The behavior of the neurons was analyzed by plotting their firing rate against head velocity. The Y-intercept of the regression line was used to express spontaneous firing rate (resting discharge), and its slope was used to express the sensitivity of the neuron-to-head velocity. 5. In the absence of statistically significant difference between the characteristics of the neuronal discharge of the second-order vestibular neurons recorded in the SVN, LVN, and rostral MVN, the data were pooled. The Resting discharge of these cells amounted to 41.0 +/- 24.7 (SD) spikes/s in the control state, fell to 7.2 +/- 13.9 spikes/s just after labyrinthectomy, and completely returned to normal values 1 wk after surgery (42.5 +/- 21.6 spikes/s). Among the monosynaptically recruited neurons, the percentage of silent units was 0% in the control group, 69% in the just-postoperative group, and 0% in the 1-wk-postoperative group. 6. By contrast, the sensitivity to head velocity of the second-order vestibular neurons, which was 0.69 +/- 0.48 (SD) spikes.s-1/deg.s-1 in the control state and which fell to 0.03 +/- 0.11 spikes.s-1/deg.s-1 just after labyrinthectomy, remained low 1 wk after injury (0.21 +/- 0.26 spikes.s-1/deg.s-1). Moreover, the slight recovery of sensitivity to head rotation was due only to units behaving as type II neurons. 7. The mean resting discharge of the polysynaptically recruited neurons (pooled from the 3 explored nuclei) was 31.6 +/- 19.3 spikes/s in the control group. It decreased to 11.6 +/- 12.1 spikes/s in the just-postoperative group and recovered to 39.8 +/- 20.2 spikes/s in the 1-wk-postoperative group. No neuron was silent at rest either in the control group or in the 1-wk-postoperative group. Just after labyrinthectomy, 35% of the neurons had a null resting activity. The mean sensitivity to head velocity of these neurons was 0.55 +/- 0.42 spikes.s-1/deg.s-1 in the control group. It decreased to 0.05 +/- 0.12 spikes.s-1/deg.s-1 in the just-postoperative group and recovered to 0.22 +/- 0.17 spikes.s-1/deg.s-1 in the 1-wk-postoperative group. 8. We conclude that, at least in the guinea pig, the restoration of the spontaneous activity of the deafferented neurons is complete 1 wk after a unilateral labyrinthectomy and thus probably plays an important role in vestibular compensation...

Pursuit—Vestibular Interactions in Brain Stem Neurons During Rotation and Translation

2005 ◽  
Vol 93 (6) ◽  
pp. 3418-3433 ◽  
Author(s):  
Hui Meng ◽  
Andrea M. Green ◽  
J. David Dickman ◽  
Dora E. Angelaki
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
Smooth Pursuit ◽  
Viewing Distance ◽  
Vestibuloocular Reflex ◽  
Type Ii ◽  
Smooth Pursuit Eye Movements ◽  
Firing Rates ◽  
Pursuit Eye Movements ◽  
Neural Activities

Under natural conditions, the vestibular and pursuit systems work synergistically to stabilize the visual scene during movement. How translational vestibular signals [translational vestibuloocular reflex (TVOR)] are processed in the premotor pathways for slow eye movements continues to remain a challenging question. To further our understanding of how premotor neurons contribute to this processing, we recorded neural activities from the prepositus and rostral medial vestibular nuclei in macaque monkeys. Vestibular neurons were tested during 0.5-Hz rotation and lateral translation (both with gaze stable and during VOR cancellation tasks), as well as during smooth pursuit eye movements. Data were collected at two different viewing distances, 80 and 20 cm. Based on their responses to rotation and pursuit, eye-movement–sensitive neurons were classified into position–vestibular–pause (PVP) neurons, eye–head (EH) neurons, and burst–tonic (BT) cells. We found that approximately half of the type II PVP and EH neurons with ipsilateral eye movement preference were modulated during TVOR cancellation. In contrast, few of the EH and none of the type I PVP cells with contralateral eye movement preference modulated during translation in the absence of eye movements; nor did any of the BT neurons change their firing rates during TVOR cancellation. Of the type II PVP and EH neurons that modulated during TVOR cancellation, cell firing rates increased for either ipsilateral or contralateral displacement, a property that could not be predicted on the basis of their rotational or pursuit responses. In contrast, under stable gaze conditions, all neuron types, including EH cells, were modulated during translation according to their ipsilateral/contralateral preference for pursuit eye movements. Differences in translational response sensitivities for far versus near targets were seen only in type II PVP and EH cells. There was no effect of viewing distance on response phase for any cell type. When expressed relative to motor output, neural sensitivities during translation (although not during rotation) and pursuit were equivalent, particularly for the 20-cm viewing distance. These results suggest that neural activities during the TVOR were more motorlike compared with cell responses during the rotational vestibuloocular reflex (RVOR). We also found that neural responses under stable gaze conditions could not always be predicted by a linear vectorial addition of the cell activities during pursuit and VOR cancellation. The departure from linearity was more pronounced for the TVOR under near-viewing conditions. These results extend previous observations for the neural processing of otolith signals within the premotor circuitry that generates the RVOR and smooth pursuit eye movements.

Expression of motor learning in the response of the primate vestibuloocular reflex pathway to electrical stimulation

1992 ◽  
Vol 67 (6) ◽  
pp. 1493-1508 ◽  
Author(s):  
D. M. Broussard ◽  
H. M. Bronte-Stewart ◽  
S. G. Lisberger
Keyword(s):  
Electrical Stimulation ◽  
Eye Movements ◽  
Motor Learning ◽  
Eye Movement ◽  
Image Motion ◽  
Vestibuloocular Reflex ◽  
Horizontal Canal ◽  
Vestibular Afferents ◽  
Eye Velocity ◽  
Stimulation Of

1. The vestibuloocular reflex (VOR) undergoes long-term adaptive changes in the presence of persistent retinal image motion during head turns. Previous experiments using natural stimuli have provided evidence that the VOR is subserved by parallel pathways, including some that are modified during learning and some that are not. We have used electrical stimulation of the vestibular labyrinth to investigate the temporal properties of the signals that are transmitted through the modified pathways. 2. Electrodes were implanted chronically in the superior semi-circular canal, the horizontal canal, or the vestibule for electrical activation of the vestibular afferents. Learning was induced by fitting the monkeys with spectacles that magnified or miniaturized vision. Before, during, and after motor learning, we measured the eye movements evoked by electrical stimulation of the labyrinth as well as the gain of the VOR, defined as eye speed divided by head speed during natural vestibular stimulation in the dark. 3. Trains of pulses applied to the labyrinth caused the eyes to move away from the side of stimulation with an initial rapid change in eye velocity followed by a steady-state plateau. Changes in the gain of the VOR caused large changes in the trajectory and magnitude of eye velocity during the plateau, showing that our stimulating electrodes had access to the modified pathways. 4. A single, brief current pulse applied to the labyrinth evoked an eye movement that had a latency of 5 ms and consisted of a pulse of eye velocity away from the side of the stimulation followed by a rebound toward the side of stimulation. To quantify the effect of motor learning on these eye movements, we pooled the data across different VOR gains and computed the slope of the relationship between eye velocity and VOR gain at each millisecond after the stimulus. We refer to the slope as the "modification index." 5. In comparison with the evoked eye velocity, the modification index took longer to return to baseline and showed a large peak at the time of the rebound in eye velocity. Increases in stimulus current increased both the amplitude and the duration of the modification index and revealed several later peaks. These observations suggest that the full expression of motor learning requires activation of multisynaptic pathways and recruitment of primary vestibular afferents with higher thresholds for electrical stimulation. 6. The modification index was almost always positive during the initial deflection in eye velocity, and the latency of the first change in the modification index was usually the same as the latency of the evoked eye movement.(ABSTRACT TRUNCATED AT 400 WORDS)

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.

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)

Dorsal Y group in the squirrel monkey. I. Neuronal responses during rapid and long-term modifications of the vertical VOR

1995 ◽  
Vol 73 (2) ◽  
pp. 615-631 ◽  
Author(s):  
A. M. Partsalis ◽  
Y. Zhang ◽  
S. M. Highstein
Keyword(s):  
Eye Movement ◽  
Neuronal Response ◽  
Head Rotation ◽  
High Gain ◽  
Optokinetic Stimulation ◽  
Linear Interaction ◽  
Full Field ◽  
Head Velocity ◽  
Visual Vestibular Interaction ◽  
Y Cells

1. The activity of 113 Y group neurons was recorded extracellularly in 5 alert squirrel monkeys. Sixty-two cells were recorded in naive animals, and 51 cells were recorded after adaptation of the vestibuloocular reflex (VOR) with the use of telescopic lenses. The animals were lying on their right side, so that head rotation was in the vertical (pitch) plane and optokinetic stimulation elicited vertical eye movement. The responses of most cells, as well as the concurrent eye movement, were studied during 1) the VOR, elicited in darkness or in light by sinusoidal head rotation, 2) visual following, elicited by sinusoidal rotation of a full-field optokinetic drum around the stationary animal, and 3) paradigms of visual-vestibular interaction, elicited by combined sinusoidal vestibular and optokinetic stimulation. Stimulation parameters for both head and drum velocity were usually 0.5 Hz, 35 degrees/s peak velocity. 2. Y group cells respond vigorously during visual following and during suppression of the VOR (produced by in-phase rotation of the head and the optokinetic drum); the response is approximately in-phase with eye velocity during visual following, and approximately in-phase with head velocity during suppression of the VOR. During the VOR in darkness, Y cells usually exhibit only slight modulation. The results suggest a linear interaction of visual following and vestibular signals on Y cells during vertical visual-vestibular interaction. Taking into account the excitatory projection of Y cells to superior rectus and inferior oblique motoneurons, a causal role of the Y group in rapid modification of VOR gain during visual-vestibular interaction is suggested. 3. Nine Y neurons from two animals were recorded continuously, for periods ranging from 30 min to 5 h, while the VOR was being adapted to higher or lower gain. Progressive changes of the gain of the VOR in darkness were evident after approximately 30 min from the initiation of head rotation under visual-vestibular mismatch. Consistent changes of the gain and/or phase of the neuronal response during the VOR in darkness were noted in all cases. The phase of the neuronal response gradually approximated head velocity phase during adaptation of the VOR to low gain, increases in the neuronal gain thereafter ensued; the opposite changes were observed during adaptation of the VOR to high gain. 4. Sixteen Y cells were recorded from 1 animal chronically adapted to high VOR gain with the use of magnifying lenses, and 35 cells were recorded from 2 animals chronically adapted to low VOR gain with the use of miniaturizing lenses.(ABSTRACT TRUNCATED AT 400 WORDS)

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