scholarly journals Firing behaviour of squirrel monkey eye movement‐related vestibular nucleus neurons during gaze saccades

2003 ◽  
Vol 546 (1) ◽  
pp. 207-224 ◽  
Author(s):  
Robert A. McCrea ◽  
Greg T. Gdowski
1993 ◽  
Vol 69 (2) ◽  
pp. 642-645 ◽  
Author(s):  
Y. Zhang ◽  
A. M. Partsalis ◽  
S. M. Highstein

1. Properties of superior vestibular nucleus (SVN) neurons and their projection to the cerebellar flocculus were studied in alert squirrel monkeys by using chronic unit and eye movement recording and microstimulation techniques. Twenty-three cells were antidromically activated from the ipsilateral flocculus, and seventeen of these were also orthodromically activated from the ipsilateral VIIth nerve at monosynaptic latencies. Only 1 of these 23 units was also inhibited by flocculus stimulation. According to their response properties, 9 of the cells were pure vestibular, 2 were vestibular-pause, and 12 were position-vestibular cells. The mean eye position sensitivity of these position-vestibular cells was significantly lower than that of cells projecting to the oculomotor nucleus (OMN). No eye movement-only neurons were antidromically activated from the flocculus. No cells could be antidromically activated from both the oculomotor nucleus and the flocculus.


1989 ◽  
Vol 1 (2) ◽  
pp. 230-241 ◽  
Author(s):  
Thomas J. Anastasio ◽  
David A. Robinson

The mechanisms of eye-movement control are among the best understood in motor neurophysiology. Detailed anatomical and physiological data have paved the way for theoretical models that have unified existing knowledge and suggested further experiments. These models have generally taken the form of black-box diagrams (for example, Robinson 1981) representing the flow of hypothetical signals between idealized signal-processing blocks. They approximate overall oculomotor behavior but indicate little about how real eye-movement signals would be carried and processed by real neural networks. Neurons that combine and transmit oculomotor signals, such as those in the vestibular nucleus (VN), actually do so in a diverse, seemingly random way that would be impossible to predict from a block diagram. The purpose of this study is to use a neural-network learning scheme (Rumelhart et al. 1986) to construct parallel, distributed models of the vestibulo-oculomotor system that simulate the diversity of responses recorded experimentally from VN neurons.


1992 ◽  
Vol 68 (1) ◽  
pp. 319-332 ◽  
Author(s):  
J. L. McFarland ◽  
A. F. Fuchs

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)


2018 ◽  
Vol 119 (1) ◽  
pp. 73-83 ◽  
Author(s):  
Shawn D. Newlands ◽  
Ben Abbatematteo ◽  
Min Wei ◽  
Laurel H. Carney ◽  
Hongge Luan

Roughly half of all vestibular nucleus neurons without eye movement sensitivity respond to both angular rotation and linear acceleration. Linear acceleration signals arise from otolith organs, and rotation signals arise from semicircular canals. In the vestibular nerve, these signals are carried by different afferents. Vestibular nucleus neurons represent the first point of convergence for these distinct sensory signals. This study systematically evaluated how rotational and translational signals interact in single neurons in the vestibular nuclei: multisensory integration at the first opportunity for convergence between these two independent vestibular sensory signals. Single-unit recordings were made from the vestibular nuclei of awake macaques during yaw rotation, translation in the horizontal plane, and combinations of rotation and translation at different frequencies. The overall response magnitude of the combined translation and rotation was generally less than the sum of the magnitudes in responses to the stimuli applied independently. However, we found that under conditions in which the peaks of the rotational and translational responses were coincident these signals were approximately additive. With presentation of rotation and translation at different frequencies, rotation was attenuated more than translation, regardless of which was at a higher frequency. These data suggest a nonlinear interaction between these two sensory modalities in the vestibular nuclei, in which coincident peak responses are proportionally stronger than other, off-peak interactions. These results are similar to those reported for other forms of multisensory integration, such as audio-visual integration in the superior colliculus. NEW & NOTEWORTHY This is the first study to systematically explore the interaction of rotational and translational signals in the vestibular nuclei through independent manipulation. The results of this study demonstrate nonlinear integration leading to maximum response amplitude when the timing and direction of peak rotational and translational responses are coincident.


1994 ◽  
Vol 72 (2) ◽  
pp. 974-998 ◽  
Author(s):  
S. G. Lisberger

1. We have used a combination of eye movement recordings and computer modeling to study long-term adaptive modification (motor learning) in the vestibuloocular reflex (VOR). The eye movement recordings place constraints on possible sites for motor learning. The computer model abides by these constraints, as well as constraints provided by data in previous papers, to formalize a new hypothesis about the sites of motor learning. The model was designed to reproduce as much of the existing neural and behavioral data as possible. 2. Motor learning was induced in monkeys by fitting them with spectacles that caused the gain of the VOR (eye speed divided by head speed) to increase to values > 1.6 or to decrease to values < 0.4. We elicited pursuit by providing ramp motion of a small target at 30 degrees/s along the horizontal axis. Changes in the gain of the VOR caused only small and inconsistent changes in the eye acceleration in the first 100 ms after the onset of pursuit and had no effect on the eye velocity during tracking of steady target motion. Electrical stimulation in the flocculus and ventral paraflocculus with single pulses or trains of pulses caused smooth eye movement toward the side of stimulation after latencies of 9–11 ms. Neither the latency, the peak eye velocity, nor the initial eye acceleration varied as a consistent function of the gain of the VOR. 3. The computer model contained nodes that represented position-vestibular-pause cells (PVP-cells) and flocculus target neurons (FTNs) in the vestibular nucleus, and horizontal gaze-velocity Purkinje cells (HGVP-cells) in the cerebellar flocculus and ventral paraflocculus. Node FTN represented only the “E-c FTNs,” which show increased firing for eye motion away from the side of recording. The transfer functions in the model included dynamic elements (filters) as well as static elements (summing junctions, gain elements, and time delays). Except for the transfer functions that converted visual motion inputs into commands for smooth eye movement, the model was linear. 4. The performance of the model was determined both by computer simulation and, for the VOR in the dark, by analytic solution of linear equations. For simulation, we adjusted the parameters by hand to match the output of the model to the eye velocity of monkeys and to match the activity of the relevant nodes in the model to the firing of HGVP-cells, FTNs, and PVP-cells when the gain of the VOR was 0.4, 1.0, and 1.6.(ABSTRACT TRUNCATED AT 400 WORDS)


1999 ◽  
Vol 82 (1) ◽  
pp. 416-428 ◽  
Author(s):  
Robert A. McCrea ◽  
Greg T. Gdowski ◽  
Richard Boyle ◽  
Timothy Belton

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.


1995 ◽  
Vol 73 (6) ◽  
pp. 2279-2292 ◽  
Author(s):  
Y. Zhang ◽  
A. M. Partsalis ◽  
S. M. Highstein

1. Seven upward eye velocity flocculus target neurons (FTNs) and two flocculus projecting neurons (FPNs) were studied before and after ipsilateral flocculus inactivation by injection of muscimol in the alert squirrel monkey. An additional seven FTNs and seven FPNs recorded from the corresponding FTN and FPN areas were recorded after injection. Response properties of FTNs and FPNs were characterized by visual-vestibular interaction paradigms and were compared before and after flocculus inactivation. 2. In FTNs the mean firing rate increased within 2-5 min after muscimol injection in the flocculus and reached a plateau level in approximately 10-20 min. The average mean firing rate for seven FTNs increased from 117 to 174 spikes/s, a net increase of 57 spikes/s (49%). Accompanying the large increase of the mean firing rate, a spontaneous nystagmus in the darkness developed with the slow phase directed upward and contralateral. 3. The firing rate modulation during visual following of a sinusoidal optokinetic drum (0.5 Hz) decreased within 2-5 min after muscimol injection in the flocculus and reached a level of 0 in approximately 10-20 min for all FTNs. After that, some cells remained unmodulated for the period of recording; other cells gradually reversed their phase and developed a modulation out of phase with drum velocity. The depletion of the visual following eye velocity signal on superior vestibular nucleus (SVN) FTNs accompanied a small but consistent decrease of visual following eye velocity amplitude. The average maximum decrease of eye velocity was 26 +/- 9% (mean +/- SD). 4. After flocculus inactivation, even though the modulation response at 0.5 Hz during visual following was abolished, a slow-component eye velocity signal with the same on direction was revealed by a constant-velocity optokinetic stimulus. It is concluded that there are at least two kinds of eye velocity signals during the optokinetic response. These signals are combined at the FTNs and are subsequently relayed to the oculomotor neurons. The source of the fast component is the flocculus, and the source of the slow component is another, as yet unidentified brain structure. 5. The effect of flocculus inactivation on the modulation amplitude during the vestibuloocular reflex (VOR) in darkness was variable: two cells did not change, two cells decreased, and three cells increased their amplitude. The response phase tended to move toward a phase lead, but the change was small. The effect on VOR suppression was more prominent.(ABSTRACT TRUNCATED AT 400 WORDS)


1999 ◽  
Vol 81 (3) ◽  
pp. 1199-1211 ◽  
Author(s):  
Sohei Chimoto ◽  
Yoshiki Iwamoto ◽  
Kaoru Yoshida

Projections and firing properties of down eye-movement neurons in the interstitial nucleus of Cajal in the cat. To clarify the role of the interstitial nucleus of Cajal (INC) in the control of vertical eye movements, projections of burst-tonic and tonic neurons in and around the INC were studied. This paper describes neurons with downwardon directions. We examined, by antidromic activation, whether these down INC (d-INC) neurons contribute to two pathways: a commissural pathway to the contralateral (c-) INC and a descending pathway to the ipsilateral vestibular nucleus (i-VN). Stimulation of the two pathways showed that as many as 74% of neurons were activated antidromically from one of the pathways. Of 113 d-INC neurons tested, 44 were activated from the commissural pathway and 40 from the descending pathway. No neurons were activated from both pathways. We concluded that commissural and descending pathways from the INC originate from two separate groups of neurons. Tracking of antidromic microstimulation in the two nuclei revealed multiple low-threshold sites and varied latencies; this was interpreted as a sign of existence of axonal arborization. Neurons with commissural projections tended to be located more dorsally than those with descending projections. Neurons with descending projections had significantly greater eye-position sensitivity and smaller saccadic sensitivity than neurons with commissural projections. The two groups of INC neurons increased their firing rate in nose-up head rotations and responded best to the rotation in the plane of contralateral posterior/ipsilateral anterior canal pair. Neurons with commissural projections showed a larger phase lag of response to sinusoidal rotation (54.6 ± 7.6°) than neurons with descending projections (45.0 ± 5.5°). Most neurons with descending projections received disynaptic excitation from the contralateral vestibular nerve. Neurons with commissural projections rarely received such disynaptic input. We suggest that downward-position-vestibular (DPV) neurons in the VN and VN-projecting d-INC neurons form a loop, together with possible commissural loops linking the bilateral VNs and the bilateral INCs. By comparing the quantitative measures of d-INC neurons with those of DPV neurons, we further suggest that integration of head velocity signals proceeds from DPV neurons to d-INC neurons with descending projections and then to d-INC neurons with commissural projections, whereas saccadic velocity signals are processed in the reverse order.


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