Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. II. Complex spikes

1990 ◽  
Vol 63 (5) ◽  
pp. 1262-1275 ◽  
Author(s):  
L. S. Stone ◽  
S. G. Lisberger
Keyword(s):  
Eye Movements ◽  
Firing Rate ◽  
Target Motion ◽  
Image Motion ◽  
Retinal Slip ◽  
Complex Spike ◽  
Simple Spike ◽  
P Cells ◽  
Complex Spikes ◽  
Spike Firing

1. We report the complex-spike responses of two groups of Purkinje cells (P-cells). The cell were classified according to their simple-spike firing during smooth eye movements evoked by visual and vestibular stimuli with the use of established criteria (Lisberger and Fuchs 1978; Stone and Lisberger 1990). During pursuit with the head fixed, ipsi gaze-velocity P-cells (GVP-cells) showed increased simple-spike firing when gaze moved toward the side of the recording, whereas down GVP-cells showed increased simple-spike firing when gaze moved downward. 2. During pursuit of sinusoidal target motion, the complex-spike firing rate was modulated out-of-phase with the simple-spike firing rate. Ipsi GVP-cells showed increased complex-spike firing during pursuit away from the side of the recording, and down GVP-cells showed increased complex-spike firing during upward pursuit. The strength of the complex-spike response increased as a function of the frequency of sinusoidal target motion. 3. GVP-cells showed directionally selective complex-spike responses during the initiation of pursuit to ramp target motion. Ipsi GVP-cells had increased complex-spike firing 100 ms after the onset of contralaterally directed target motion and decreased complex-spike activity after the onset of ipsilaterally directed target motion. Down GVP-cells had increased complex-spike firing 100 ms after the onset of upward target motion and decreased firing after the onset of downward target motion. As during sinusoidal target motion, each cell's simple- and complex-spike responses had the opposite directional preferences. 4. When the monkeys fixated a stationary target during a transient vestibular stimulus, the retinal slip caused by the 14-ms latency of the vestibuloocular reflex (VOR) affected the complex-spike firing rate. For ipsi GVP-cells, ipsilateral head motion caused transient contralateral image motion and an increase in complex-spike firing. The same vestibular stimulus in darkness caused an almost identical eye movement but had no effect on complex-spike firing. We conclude that complex spikes in ipsi GVP-cells are driven by contralaterally directed image motion. 5. To determine the events surrounding complex-spike firing during pursuit, we triggered averages of eye and target velocity on the occurrence of complex spikes during pursuit of sine-wave target motion. The averages revealed a transient pulse of retinal image motion that peaked approximately 100 ms before the complex spike. We conclude that complex spikes during steady-state pursuit are driven by the retinal slip associated with imperfect pursuit.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Changes in the Responses of Purkinje Cells in the Floccular Complex of Monkeys After Motor Learning in Smooth Pursuit Eye Movements

2000 ◽  
Vol 84 (6) ◽  
pp. 2945-2960 ◽  
Author(s):  
Maninder Kahlon ◽  
Stephen G. Lisberger
Keyword(s):  
Eye Movements ◽  
Purkinje Cells ◽  
Image Motion ◽  
Population Response ◽  
Complex Spike ◽  
Pursuit Eye Movements ◽  
Simple Spike ◽  
Learning Speed ◽  
Complex Spikes ◽  
Spike Firing

We followed simple- and complex-spike firing of Purkinje cells (PCs) in the floccular complex of the cerebellum through learned modifications of the pursuit eye movements of two monkeys. Learning was induced by double steps of target speed in which initially stationary targets move at a “learning” speed for 100 ms and then change to either a higher or lower speed in the same direction. In randomly interleaved control trials, targets moved at the learning speed in the opposite direction. When the learning direction was theon direction for simple-spike responses, learning was associated with statistically significant changes in simple-spike firing for 10 of 32 PCs. Of the 10 PCs that showed significant expressions of learning, 8 showed changes in simple-spike output in the expected direction: increased or decreased firing when eye acceleration increased or decreased through learning. There were no statistically significant changes in simple-spike responses or eye acceleration during pursuit in the control direction. When the learning direction was in the off direction for simple-spike responses, none of 15 PCs showed significant correlates of learning. Although changes in simple-spike firing were recorded in only a subset of PCs, analysis of the population response showed that the same relationship between population firing and eye acceleration obtained before and after learning. Thus learning is associated with changes that render the modified population response appropriate to drive the changed behavior. To analyze complex-spike firing during learning we correlated complex-spike firing in the second, third, and fourth 100 ms after the onset of target motion with the retinal image motion in the previous 100 ms. Data were largely consistent with previous evidence that image motion drives complex spikes with a direction selectivity opposite that for simple spikes. Comparison of complex-spike responses at different times after the onset of control and learning target motions in the learning direction implied that complex spikes could guide learning during decreases but not increases in eye acceleration. Learning caused increases or decreases in the sensitivity of complex spikes to image motion in parallel with changes in eye acceleration. Complex-spike responses were similar in all PCs, including many in which learning did not modify simple-spike responses. Our data do not disprove current theories of cerebellar learning but suggest that these theories would have to be modified to account for simple- and complex-spike firing of floccular Purkinje cells reported here.

Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes

1990 ◽  
Vol 63 (5) ◽  
pp. 1241-1261 ◽  
Author(s):  
L. S. Stone ◽  
S. G. Lisberger
Keyword(s):  
Transient Response ◽  
Target Motion ◽  
Smooth Pursuit Eye Movements ◽  
Transient Change ◽  
Pursuit Eye Movements ◽  
Simple Spike ◽  
Sustained Change ◽  
Eye Velocity ◽  
P Cells ◽  
Spike Firing

1. We have identified a visually driven output from the flocculus of the monkey by studying the simple-spike responses of Purkinje cells (P-cells) during the initiation of smooth-pursuit eye movements. We report on two groups of P-cells that appear to be the horizontal and vertical gaze-velocity P-cells (GVP-cells) studied previously during periodic target and head motion. 2. During pursuit of periodic target motion, one group of P-cells prefers downward motion (down GVP-cells), and the other prefers motion toward the side of recording (ipsi GVP-cells). The two groups have mean directional preferences that are nearly orthogonal, but their responses during pursuit of sinusoidal target motion and sinusoidal vestibular stimulation are in other respects quantitatively similar. 3. During the initiation of pursuit to step-ramp target motion, GVP-cells show a large transient change in simple-spike firing rate followed by a sustained change in firing that persists during steady-state pursuit. 4. The transient response is directionally selective, so that GVP-cells show a pulse of simple spikes for pursuit in the ON-direction and a dip in simple-spike firing for pursuit in the OFF-direction. The amplitude of the transient response is too large to be explained by the sensitivity of GVP-cells to eye velocity measured during pursuit of sinusoidal target motion. 5. To test whether the transient change in simple-spike firing was related to a visual input or to an eye-acceleration input to the flocculus, we recorded the firing of ipsi GVP-cells during a rapid eye acceleration caused by a transient vestibular stimulus in darkness. Most GVP-cells showed little or no transient response under these conditions, even though eye acceleration was greater than during the initiation of pursuit. We conclude that the transient response at the initiation of pursuit is probably caused by visual mossy-fiber inputs to the flocculus. 6. The sustained change in simple-spike firing is also directionally selective, with large increases in simple-spike firing for pursuit in the ON-direction and smaller decreases for pursuit in the OFF-direction. For pursuit in the ON-direction, the amplitude of the sustained response is well predicted by the sensitivity of GVP-cells to eye velocity measured during pursuit of sinusoidal target motion. 7. To determine whether the sustained response was driven by visual inputs, we recorded simple-spike firing when image motion was prevented by electronically stabilizing the target image on the fovea during steady-state pursuit.(ABSTRACT TRUNCATED AT 400 WORDS)

Simple spike responses of gaze velocity Purkinje cells in the floccular lobe of the monkey during the onset and offset of pursuit eye movements

1994 ◽  
Vol 72 (4) ◽  
pp. 2045-2050 ◽  
Author(s):  
R. J. Krauzlis ◽  
S. G. Lisberger
Keyword(s):  
Eye Movements ◽  
Firing Rate ◽  
Purkinje Cells ◽  
Target Motion ◽  
Transient Increase ◽  
Pursuit Eye Movements ◽  
Simple Spike ◽  
Preferred Direction ◽  
Population Average ◽  
Ventral Paraflocculus

1. We recorded the simple spike firing rate of gaze velocity Purkinje cells (GVP-cells) in the flocculus/ventral paraflocculus of two monkeys during the smooth pursuit eye movements evoked by a target that was initially at rest, started suddenly, moved at a constant velocity, and then stopped. 2. For target motion in the preferred direction, GVP-cells showed a large transient increase in firing rate at the onset of pursuit, a smaller but sustained increase during the maintenance of pursuit, and a smooth return to baseline firing with little undershoot at the offset of pursuit. For target motion in the nonpreferred direction, GVP-cells showed a small decrease in firing rate at the onset of pursuit, a similar sustained decrease during the maintenance of pursuit, but a large transient increase in firing rate at the offset of pursuit before returning to baseline firing. 3. We pooled the data in our sample of horizontal GVP-cells by subtracting the population average of firing rate recorded during pursuit in the nonpreferred direction from the population average recorded during pursuit in the preferred direction. We transformed this net population average by passing it through a model of the brain stem final common pathway and the oculomotor plant. This yielded a signal that closely matched the observed trajectory of eye velocity during pursuit. We conclude that the transient overshoots exhibited in the firing rate of GVP-cells can provide appropriate compensation for the lagging dynamics of the oculomotor plant.

Effect of simple spike firing mode on complex spike firing rate and waveform in cerebellar Purkinje cells in non-anesthetized mice

2004 ◽  
Vol 367 (2) ◽  
pp. 171-176 ◽  
Author(s):  
Laurent Servais ◽  
Bertrand Bearzatto ◽  
Raphaël Hourez ◽  
Bernard Dan ◽  
Serge N. Schiffmann ◽  
...  
Keyword(s):  
Firing Rate ◽  
Purkinje Cells ◽  
Complex Spike ◽  
Simple Spike ◽  
Firing Mode ◽  
Cerebellar Purkinje Cells ◽  
Spike Firing

scholarly journals Interaction of plasticity and circuit organization during the acquisition of cerebellum-dependent motor learning

eLife ◽  
2013 ◽  
Vol 2 ◽  
Author(s):  
Yan Yang ◽  
Stephen G Lisberger
Keyword(s):  
Motor Learning ◽  
Firing Rate ◽  
Mossy Fiber ◽  
Brain Slices ◽  
Short Term ◽  
Spike Response ◽  
Complex Spike ◽  
Simple Spike ◽  
Cerebellar Purkinje Cells ◽  
Spike Firing

Motor learning occurs through interactions between the cerebellar circuit and cellular plasticity at different sites. Previous work has established plasticity in brain slices and suggested plausible sites of behavioral learning. We now reveal what actually happens in the cerebellum during short-term learning. We monitor the expression of plasticity in the simple-spike firing of cerebellar Purkinje cells during trial-over-trial learning in smooth pursuit eye movements of monkeys. Our findings imply that: 1) a single complex-spike response driven by one instruction for learning causes short-term plasticity in a Purkinje cell’s mossy fiber/parallel-fiber input pathways; 2) complex-spike responses and simple-spike firing rate are correlated across the Purkinje cell population; and 3) simple-spike firing rate at the time of an instruction for learning modulates the probability of a complex-spike response, possibly through a disynaptic feedback pathway to the inferior olive. These mechanisms may participate in long-term motor learning.

scholarly journals The vestibular-related frontal cortex and its role in smooth-pursuit eye movements and vestibular-pursuit interactions

2006 ◽  
Vol 16 (1-2) ◽  
pp. 1-22 ◽  
Author(s):  
Junko Fukushima ◽  
Teppei Akao ◽  
Sergei Kurkin ◽  
Chris R.S. Kaneko ◽  
Kikuro Fukushima
Keyword(s):  
Eye Movements ◽  
Frontal Cortex ◽  
Smooth Pursuit ◽  
Vestibular Stimulation ◽  
Target Motion ◽  
Head Movements ◽  
Image Motion ◽  
Target Velocity ◽  
Eye Velocity ◽  
Pursuit Neurons

In order to see clearly when a target is moving slowly, primates with high acuity foveae use smooth-pursuit and vergence eye movements. The former rotates both eyes in the same direction to track target motion in frontal planes, while the latter rotates left and right eyes in opposite directions to track target motion in depth. Together, these two systems pursue targets precisely and maintain their images on the foveae of both eyes. During head movements, both systems must interact with the vestibular system to minimize slip of the retinal images. The primate frontal cortex contains two pursuit-related areas; the caudal part of the frontal eye fields (FEF) and supplementary eye fields (SEF). Evoked potential studies have demonstrated vestibular projections to both areas and pursuit neurons in both areas respond to vestibular stimulation. The majority of FEF pursuit neurons code parameters of pursuit such as pursuit and vergence eye velocity, gaze velocity, and retinal image motion for target velocity in frontal and depth planes. Moreover, vestibular inputs contribute to the predictive pursuit responses of FEF neurons. In contrast, the majority of SEF pursuit neurons do not code pursuit metrics and many SEF neurons are reported to be active in more complex tasks. These results suggest that FEF- and SEF-pursuit neurons are involved in different aspects of vestibular-pursuit interactions and that eye velocity coding of SEF pursuit neurons is specialized for the task condition.

Discharges of neurons in the dorsal paraflocculus of monkeys during eye movements and visual stimulation

1986 ◽  
Vol 56 (4) ◽  
pp. 1129-1146 ◽  
Author(s):  
H. Noda ◽  
A. Mikami
Keyword(s):  
Eye Movements ◽  
Slip Velocity ◽  
Visual Stimulation ◽  
The Other ◽  
Eye Position ◽  
Tonic Activity ◽  
Stimulus Movement ◽  
Retinal Slip ◽  
Position Sensitivity ◽  
P Cells

Extracellular recordings were obtained from 319 input units and 304 Purkinje cells (P-cells) in the dorsal paraflocculus of alert monkeys trained to fixate a visual target. They changed discharge rates with either eye movement, eye position, or visual stimulus movement. Of the 319 input units, recorded in the granular layer or white matter, most were mossy fibers (MFs), but 90 (28%) showed characteristic cellular spikes. The latter units were probably granular cells (p-GC). Of the 319 input units, 163 (51%) showed bursts with saccades (burst units) and 62 (19%) showed a prelude on the average 124 ms prior to the onset of saccade (long-lead burst units). Sixty-five (20%) had tonic activity related to eye position and also showed bursts with saccades (burst-tonic units), and the remaining 29 (9%) showed only tonic activity (tonic units). MFs and p-GCs showed no significant differences in the proportion of each type of unit or in their response properties. The majority of burst units (63%) were pan directional, whereas all long-lead burst units had directional selectivity. The preferred directions of long-lead burst, burst tonic, and directionally selective burst units were found in all four quadrants. Position-related activity was found in 48% of the burst-tonic and tonic units to be linearly related to eye position and to show position threshold. The other units also had position thresholds but their activity was not monotonically related to fixation position. Six climbing fibers (CFs), 32 input units (including 13 p-GC), and 8 P-cells showed cyclic responses during sinusoidal movements of a visual pattern. One class of MF units (57%) responded only to the direction, whereas the others responded to both the direction and retinal-slip velocity. Both CF and P-cell units responded to sinusoidal retinal-slip velocity. Of 67 input units, 23 showed cyclic modulation in firing during sinusoidal eye movements in the horizontal plane. Nineteen were burst-tonic and four were tonic units. They also showed position sensitivity. The phase of the cyclic responses tended to lag behind the eye velocity during low-frequency trackings. Of 237 P-cells, 163 (68.8%) discharged with saccades (burst P-cells), 42 (17.7%) paused with saccades (pause P-cells), and 32 (13.5%) discharged with saccades in one direction and paused in the other (burst-pause P-cells). Position sensitivity was found in 38 P-cells; 12 were burst, 5 were pause, and 10 were burst-pause P-cells. Eleven did not respond with saccades.(ABSTRACT TRUNCATED AT 400 WORDS)

Effects of Nucleus Prepositus Hypoglossi Lesions on Visual Climbing Fiber Activity in the Rabbit Flocculus

2000 ◽  
Vol 84 (5) ◽  
pp. 2552-2563 ◽  
Author(s):  
M. P. Arts ◽  
C. I. De Zeeuw ◽  
J. Lips ◽  
E. Rosbak ◽  
J. I. Simpson
Keyword(s):  
Constant Velocity ◽  
Inferior Olive ◽  
Vertical Axis ◽  
Firing Frequency ◽  
Optokinetic Stimulation ◽  
Spontaneous Firing ◽  
Complex Spike ◽  
Prepositus Hypoglossi ◽  
Complex Spikes ◽  
Spike Firing

The caudal dorsal cap (dc) of the inferior olive is involved in the control of horizontal compensatory eye movements. It provides those climbing fibers to the vestibulocerebellum that modulate optimally to optokinetic stimulation about the vertical axis. This modulation is mediated at least in part via an excitatory input to the caudal dc from the pretectal nucleus of the optic tract and the dorsal terminal nucleus of the accessory optic system. In addition, the caudal dc receives a substantial GABAergic input from the nucleus prepositus hypoglossi (NPH). To investigate the possible contribution of this bilateral inhibitory projection to the visual responsiveness of caudal dc neurons, we recorded the climbing fiber activity (i.e., complex spikes) of vertical axis Purkinje cells in the flocculus of anesthetized rabbits before and after ablative lesions of the NPH. When the NPH ipsilateral to the recorded flocculus was lesioned, the spontaneous complex spike firing frequency did not change significantly; but when both NPHs were lesioned, the spontaneous complex spike firing frequency increased significantly. When only the contralateral NPH was lesioned, the spontaneous complex spike firing frequency decreased significantly. Neither unilateral nor bilateral lesions had a significant influence on the depth of complex spike modulation during constant velocity optokinetic stimulation or on the transient continuation of complex spike modulation that occurred when the constant velocity optokinetic stimulation stopped. The effects of the lesions on the spontaneous complex spike firing frequency could not be explained when only the projections from the NPH to the inferior olive were considered. Therefore we investigated at the electron microscopic level the nature of the commissural connection between the two NPHs. The terminals of this projection were found to be predominantly GABAergic and to terminate in part on GABAergic neurons. When this inhibitory commissural connection is taken into consideration, then the effects of NPH lesions on the spontaneous firing frequency of floccular complex spikes are qualitatively explicable in terms of relative weighting of the commissural and caudal dc projections of the NPH. In summary, we conclude that in the anesthetized rabbit the inhibitory projection of the NPH to the caudal dc influences the spontaneous firing frequency of floccular complex spikes but not their modulation by optokinetic stimulation.

scholarly journals Neurons of the inferior olive respond to broad classes of sensory input while subject to homeostatic control

2018 ◽  
Author(s):  
Chiheng Ju ◽  
Laurens W.J. Bosman ◽  
Tycho M. Hoogland ◽  
Arthiha Velauthapillai ◽  
Pavithra Murugesan ◽  
...  
Keyword(s):  
Purkinje Cells ◽  
Inferior Olive ◽  
Recent History ◽  
Climbing Fibre ◽  
Homeostatic Control ◽  
Complex Spike ◽  
History Of ◽  
Sensory Evoked ◽  
Complex Spikes ◽  
Spike Firing

AbstractCerebellar Purkinje cells integrate sensory information with motor efference copies to adapt movements to behavioural and environmental requirements. They produce complex spikes that are triggered by the activity of climbing fibres originating in neurons of the inferior olive. These complex spikes can shape the onset, amplitude and direction of movements as well as the adaptation of such movements to sensory feedback. Clusters of nearby inferior olive neurons project to parasagittally aligned stripes of Purkinje cells, referred to as “microzones”. It is currently unclear to what extent individual Purkinje cells within a single microzone integrate climbing fibre inputs from multiple sources of different sensory origins, and to what extent sensory-evoked climbing fibre responses depend on the strength and recent history of activation. Here we imaged complex spike responses in cerebellar lobule crus 1 to various types of sensory stimulation in awake mice. We find that different sensory modalities and receptive fields have a mild, but consistent, tendency to converge on individual Purkinje cells. Purkinje cells encoding the same stimulus show increased events with coherent complex spike firing and tend to lie close together. Moreover, whereas complex spike firing is only mildly affected by variations in stimulus strength, it strongly depends on the recent history of climbing fibre activity. Our data point towards a mechanism in the olivo-cerebellar system that regulates complex spike firing during mono- or multisensory stimulation around a relatively low set-point, highlighting an integrative coding scheme of complex spike firing under homeostatic control.

Transitions between pursuit eye movements and fixation in the monkey: dependence on context

1996 ◽  
Vol 76 (3) ◽  
pp. 1622-1638 ◽  
Author(s):  
R. J. Krauzlis ◽  
F. A. Miles
Keyword(s):  
Eye Movements ◽  
Constant Velocity ◽  
Target Position ◽  
Velocity Profiles ◽  
Target Motion ◽  
Gradual Transition ◽  
Retinal Slip ◽  
Visuomotor Processing ◽  
Backward Perturbations ◽  
Eye Velocity

1. We compared the visuomotor processing underlying the onset and offset of pursuit by recording the eye movements of three monkeys as they smoothly tracked a target that was initially at rest, started to move suddenly at a constant velocity along the horizontal meridian, and then stopped. We presented this sequence of target motions in two different contexts. In the first context the target sometimes stopped after 500 ms, but on other interleaved trials the target either continued moving at a constant velocity, slowed down, speeded up, or reversed direction. In the second context the target always stopped, but the duration of the preceding constant velocity was randomized from 500 to 700 ms. 2. The dynamics of the eye velocity during the offset of pursuit were markedly different in the two experiments. When the target stopped only sometimes, the decrease in eye velocity at the offset of pursuit often overshot zero, producing a brief, small reversal in the direction of pursuit before eye speed settled to zero. When the target always stopped, the decrease in eye velocity at the offset of pursuit followed a more gradual transition toward zero with no overshoot. Thus the eye velocity profiles obtained in the first experiment contradict, whereas those obtained in the second experiment confirm, previous characterizations of the offset of pursuit as an exponential decay toward zero eye speed. 3. To investigate the basis of the different eye velocity profiles obtained in the two experiments, we probed the state of transmission along the visuomotor pathways for pursuit with the use of small perturbations in the motion of the target. We used perturbations consisting of 1 degree step changes in target position superimposed on the constant velocity motion of the target, on the basis of previous findings that such perturbations elicit saccades during fixation but smooth changes in eye speed during maintained pursuit. Single perturbations were imposed at regularly spaced intervals on separate interleaved trials during the onset, maintenance, and offset of pursuit. 4. Perturbations imposed during the onset and maintenance of pursuit had similar effects regardless of whether the target stopped only sometimes or always. In both experiments, perturbations that stepped the target in the direction opposite to the constant velocity of the target produced decreases in eye speed; perturbations in the same direction produced negligible or inconsistent changes in eye speed. The changes in eye speed caused by perturbations were largest for those perturbations introduced within the first 100 ms after the start of target motion, before the onset of the smooth eye movement, and became progressively smaller as target motion continued. The largest changes in eye speed were therefore caused by those perturbations imposed during periods of large retinal slip and by those perturbations whose direction opposed that slip. 5. Perturbations imposed during the offset of pursuit had different effects depending on whether the target stopped only sometimes or always. When the target stopped only sometimes, forward perturbations produced large increases in eye speed, whereas backward perturbations produced negligible or inconsistent changes in eye speed. Thus the visuomotor processing underlying the offset of pursuit in this experiment strongly resembled that underlying the onset of pursuit: in both cases, those perturbations in the direction opposing large retinal slip produced the largest effects. In contrast, when the target always stopped, neither forward nor backward perturbations imposed during the offset of pursuit produced large changes in eye speed. This indicates that the visuomotor processing underlying the offset of pursuit in this experiment was different from the processing underlying the onset of pursuit. 6. Perturbations also produced changes in the frequency of saccades, although these effects were less consistent than the changes in pursuit eye speed

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