A vermal Purkinje cell simple spike population response encodes the changes in eye movement kinematics due to smooth pursuit adaptation

Encoding of movement kinematics in Purkinje cell simple spike discharge has important implications for hypotheses of cerebellar cortical function. Several outstanding questions remain regarding representation of these kinematic signals. It is uncertain whether kinematic encoding occurs in unpredictable, feedback-dependent tasks or kinematic signals are conserved across tasks. Additionally, there is a need to understand the signals encoded in the instantaneous discharge of single cells without averaging across trials or time. To address these questions, this study recorded Purkinje cell firing in monkeys trained to perform a manual random tracking task in addition to circular tracking and center-out reach. Random tracking provides for extensive coverage of kinematic workspaces. Direction and speed errors are significantly greater during random than circular tracking. Cross-correlation analyses comparing hand and target velocity profiles show that hand velocity lags target velocity during random tracking. Correlations between simple spike firing from 120 Purkinje cells and hand position, velocity, and speed were evaluated with linear regression models including a time constant, τ, as a measure of the firing lead/lag relative to the kinematic parameters. Across the population, velocity accounts for the majority of simple spike firing variability (63 ± 30% of Radj2), followed by position (28 ± 24% of Radj2) and speed (11 ± 19% of Radj2). Simple spike firing often leads hand kinematics. Comparison of regression models based on averaged vs. nonaveraged firing and kinematics reveals lower Radj2 values for nonaveraged data; however, regression coefficients and τ values are highly similar. Finally, for most cells, model coefficients generated from random tracking accurately estimate simple spike firing in either circular tracking or center-out reach. These findings imply that the cerebellum controls movement kinematics, consistent with a forward internal model that predicts upcoming limb kinematics.

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Accuracy of Smooth Pursuit Eye Movement and Perception Rate of a False Contour While Pursuing a Rapidly Moving Image

IEICE Transactions on Fundamentals of Electronics Communications and Computer Sciences ◽

10.1587/transfun.e94.a.542 ◽

2011 ◽

Vol E94-A (2) ◽

pp. 542-547

Author(s):

Yusuke HORIE ◽

Yuta KAWAMURA ◽

Akiyuki SEITA ◽

Mitsuho YAMADA

Keyword(s):

Eye Movement ◽

Smooth Pursuit ◽

Moving Image ◽

Smooth Pursuit Eye Movement

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Role of Primate Cerebellar Hemisphere in Voluntary Eye Movement Control Revealed by Lesion Effects

Journal of Neurophysiology ◽

10.1152/jn.90440.2008 ◽

2009 ◽

Vol 101 (2) ◽

pp. 934-947 ◽

Cited By ~ 35

Author(s):

Masafumi Ohki ◽

Hiromasa Kitazawa ◽

Takahito Hiramatsu ◽

Kimitake Kaga ◽

Taiko Kitamura ◽

...

Keyword(s):

Eye Movements ◽

Eye Movement ◽

Smooth Pursuit ◽

Movement Control ◽

Cerebellar Hemisphere ◽

Target Velocity ◽

Eye Movement Control ◽

Pursuit Eye Movements ◽

Catch Up

The anatomical connection between the frontal eye field and the cerebellar hemispheric lobule VII (H-VII) suggests a potential role of the hemisphere in voluntary eye movement control. To reveal the involvement of the hemisphere in smooth pursuit and saccade control, we made a unilateral lesion around H-VII and examined its effects in three Macaca fuscata that were trained to pursue visually a small target. To the step (3°)-ramp (5–20°/s) target motion, the monkeys usually showed an initial pursuit eye movement at a latency of 80–140 ms and a small catch-up saccade at 140–220 ms that was followed by a postsaccadic pursuit eye movement that roughly matched the ramp target velocity. After unilateral cerebellar hemispheric lesioning, the initial pursuit eye movements were impaired, and the velocities of the postsaccadic pursuit eye movements decreased. The onsets of 5° visually guided saccades to the stationary target were delayed, and their amplitudes showed a tendency of increased trial-to-trial variability but never became hypo- or hypermetric. Similar tendencies were observed in the onsets and amplitudes of catch-up saccades. The adaptation of open-loop smooth pursuit velocity, tested by a step increase in target velocity for a brief period, was impaired. These lesion effects were recognized in all directions, particularly in the ipsiversive direction. A recovery was observed at 4 wk postlesion for some of these lesion effects. These results suggest that the cerebellar hemispheric region around lobule VII is involved in the control of smooth pursuit and saccadic eye movements.

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Express Saccades and Smooth Pursuit Eye Movement Function in Schizophrenic, Affective Disorder, and Normal Subjects

Journal of Cognitive Neuroscience ◽

10.1162/jocn.1993.5.3.303 ◽

1993 ◽

Vol 5 (3) ◽

pp. 303-316 ◽

Cited By ~ 25

Author(s):

Anne B. Sereno ◽

Philip S. Holzman

Keyword(s):

Response Time ◽

Eye Movement ◽

Smooth Pursuit ◽

Normal Subjects ◽

Control Group ◽

Saccadic Response ◽

Group A ◽

Schizophrenic Group ◽

Movement Function ◽

Normal Controls

Saccadic and smooth pursuit eye movements were recorded in three groups of subjects: a schizophrenic group, a non-schizophrenic psychotic patient comparison group, and a normal control group. Schizophrenic subjects demonstrated a greater decrease in saccadic response time than did normal controls in a gap task (when the fixation point was turned off 150 msec before the target appeared). The psychiatric comparison subjects did not differ from normal controls. Further, only schizophrenic subjects demonstrated a relation between smooth pursuit and saccadic eye movement performance, such that subjects with impaired smooth pursuit showed a larger decrease in saccadic response time in the gap task. The relation between performance on the gap task and quality of smooth pursuit and its relevance for a prefrontal deficit hypothesis of schizophrenia are discussed.

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A clinically oriented approach to smooth pursuit eye movement quantitative evaluation

Acta Neurologica Scandinavica ◽

10.1111/j.1600-0404.1993.tb04235.x ◽

2009 ◽

Vol 88 (4) ◽

pp. 273-278 ◽

Cited By ~ 4

Author(s):

M. Versino ◽

G. Beltrami ◽

D. Zambarbieri ◽

G. Castelnovo ◽

R. Bergamaschi ◽

...

Keyword(s):

Eye Movement ◽

Quantitative Evaluation ◽

Smooth Pursuit ◽

Smooth Pursuit Eye Movement ◽

Oriented Approach

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The Response of MSTd Neurons to Perturbations in Target Motion During Ongoing Smooth-Pursuit Eye Movements

Journal of Neurophysiology ◽

10.1152/jn.00563.2009 ◽

2010 ◽

Vol 103 (1) ◽

pp. 519-530 ◽

Cited By ~ 12

Author(s):

Seiji Ono ◽

Lukas Brostek ◽

Ulrich Nuding ◽

Stefan Glasauer ◽

Ulrich Büttner ◽

...

Keyword(s):

Eye Movement ◽

Smooth Pursuit ◽

Dynamic Properties ◽

Receptive Fields ◽

Gain Control ◽

Frontal Eye Field ◽

Cortical Areas ◽

Target Perturbation ◽

Behaving Monkeys ◽

Dynamic Gain

Several regions of the brain are involved in smooth-pursuit eye movement (SPEM) control, including the cortical areas MST (medial superior temporal) and FEF (frontal eye field). It has been shown that the eye-movement responses to a brief perturbation of the visual target during ongoing pursuit increases with higher pursuit velocities. To further investigate the underlying neuronal mechanism of this nonlinear dynamic gain control and the contributions of different cortical areas to it, we recorded from MSTd (dorsal division of the MST area) neurons in behaving monkeys ( Macaca mulatta) during step-ramp SPEM (5–20°/s) with and without superimposed target perturbation (one cycle, 5 Hz, ±10°/s). Smooth-pursuit–related MSTd neurons started to increase their activity on average 127 ms after eye-movement onset. Target perturbation consistently led to larger eye-movement responses and decreasing latencies with increasing ramp velocities, as predicted by dynamic gain control. For 36% of the smooth-pursuit–related MSTd neurons the eye-movement perturbation was accompanied by detectable changes in neuronal activity with a latency of 102 ms, with respect to the eye-movement response. The remaining smooth-pursuit–related MSTd neurons (64%) did not reflect the eye-movement perturbation. For the large majority of cases this finding could be predicted by the dynamic properties of the step-ramp responses. Almost all these MSTd neurons had large visual receptive fields responding to motion in preferred directions opposite to the optimal SPEM stimulus. Based on these findings it is unlikely that MSTd plays a major role for dynamic gain control and initiation of the perturbation response. However, neurons in MSTd could still participate in SPEM maintenance. Due to their visual field properties they could also play a role in other functions such as self-motion perception.

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

Journal of Neurophysiology ◽

10.1152/jn.1999.82.5.2612 ◽

1999 ◽

Vol 82 (5) ◽

pp. 2612-2632 ◽

Cited By ~ 115

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.

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QUANTITATIVE ANALYSIS OF SMOOTH PURSUIT EYE MOVEMENT

Nippon Jibiinkoka Gakkai Kaiho ◽

10.3950/jibiinkoka.98.681 ◽

1995 ◽

Vol 98 (4) ◽

pp. 681-696,759 ◽

Cited By ~ 1

Author(s):

MOTOYUKI HASHIBA ◽

KEIKO YASUI ◽

HIROTAKA WATABE ◽

TORU MATSUOKA ◽

SHUNKICHI BABA

Keyword(s):

Quantitative Analysis ◽

Eye Movement ◽

Smooth Pursuit ◽

Smooth Pursuit Eye Movement

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

Journal of Neurophysiology ◽

10.1152/jn.1992.68.1.319 ◽

1992 ◽

Vol 68 (1) ◽

pp. 319-332 ◽

Cited By ~ 211

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)

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