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.

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.

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 Ethanol effects on the olivocerebellar system

1982 ◽  
Vol 60 (5) ◽  
pp. 610-614 ◽  
Author(s):  
J. G. Sinclair ◽  
G. F. Lo ◽  
D. P. Harris
Keyword(s):  
Purkinje Cell ◽  
Purkinje Cells ◽  
Inferior Olive ◽  
Climbing Fibre ◽  
Complex Spike ◽  
Anaesthetized Rats ◽  
Cerebellar Purkinje Cells ◽  
Cell Synapse

Ethanol (1.5 g/kg i.v.) was found to decrease spontaneous complex spike (CS) activity in cerebellar Purkinje cells in urethane anaesthetized rats while not changing the threshold required to evoke a CS by juxtafastigial stimulation. Thus ethanol does not decrease CS activity by an action at the climbing fibre – Purkinje cell synapse. Tremor induced by harmaline (5 mg/kg i.v.) in unanaesthetized animals was markedly antagonized by ethanol (0.5–2.0 g/kg i.v.) in all animals tested. However, in nine urethane-anaesthetized animals, ethanol markedly reversed the effects of harmaline on Purkinje cells in only two cases and partially reversed the effects in another four cells. Thus, the depressant effects of ethanol on the inferior olive is not totally responsible for the blockade of the harmaline tremor but would account for the decrease in spontaneous CS activity.

Nonclock behavior of inferior olive neurons: interspike interval of Purkinje cell complex spike discharge in the awake behaving monkey is random

1995 ◽  
Vol 73 (4) ◽  
pp. 1329-1340 ◽  
Author(s):  
J. G. Keating ◽  
W. T. Thach
Keyword(s):  
Fourier Transform ◽  
Purkinje Cells ◽  
Spike Activity ◽  
Interspike Interval ◽  
Inferior Olive ◽  
Fourier Transforms ◽  
Wrist Movement ◽  
General Role ◽  
Complex Spike ◽  
Bodily Movement

1. Complex spikes of cerebellar Purkinje cells recorded from awake, behaving monkeys were studied to determine the extent to which their discharge could be quantified as periodic. Three Rhesus monkeys were trained to perform up to five different tasks involving rotation of the wrist in relation to a visual cue. Complex spike activity was recorded during task performance and intertrial time. Interspike intervals were determined from the discharge of each of 89 Purkinje cells located throughout lobules IV, V, and VI. Autocorrelation and Fourier transform of the autocorrelation function were performed on the data. In addition, the activity from one cell was transformed so that the discharge occurred on the beat of a 10-Hz clock, and in a further transformation, on the beat of a noisy 10-Hz clock. These transformed data were then analyzed as described above. 2. Fourier transform of the autocorrelogram function of the data that had been transformed to a 10-Hz clock, and that of the noisy 10-Hz clock, both showed a prominent peak at 10 Hz. However, the autocorrelograms and the Fourier transforms of the autocorrelogram functions failed to reveal a prominent periodicity for the actual discharge of any of cells, at any frequency up to 100 Hz: the discharge appeared random with respect to the interspike interval. The discharge was not random with respect to behavior. Complex spike activity was commonly time locked to the start of wrist movement. We examined this discharge to see whether oscillatory discharge could be seen after alignment of the data on the start of wrist movement, or after alignment of the data on the complex spike occurring peri-start of wrist movement. No oscillation was seen for either alignment. 3. The inferior olive, which sends its climbing fibers to the cerebellum, has been implicated in such different activities as 1) pathological tremor of the soft palate, 2) physiological tremor, 3) the normal initiation of all bodily movement, and 4) motor learning. Previous work in pharmacologically or surgically treated animals has shown that, under some conditions, the discharge of these neurons is periodic and synchronous. This firing pattern has been interpreted to support a role in the first two activities. But measurements reported here in the awake monkey show just the opposite: the discharge is aperiodic to the extent of being random. As such, the inferior olive cannot be a "motor clock" in the general role that has been proposed.(ABSTRACT TRUNCATED AT 400 WORDS)

Developmental Changes in Evoked Purkinje Cell Complex Spike Responses

2003 ◽  
Vol 90 (4) ◽  
pp. 2349-2357 ◽  
Author(s):  
Daniel A. Nicholson ◽  
John H. Freeman
Keyword(s):  
Motor Learning ◽  
Purkinje Cell ◽  
Inferior Olive ◽  
Cell Complex ◽  
Climbing Fibers ◽  
Somatosensory Stimulation ◽  
Complex Spike ◽  
Long Latency ◽  
Inhibitory Feedback ◽  
Complex Spikes

The development of synaptic interconnections between the cerebellum and inferior olive, the sole source of climbing fibers, could contribute to the ontogeny of certain forms of motor learning (e.g., eyeblink conditioning). Purkinje cell complex spikes are produced exclusively by climbing fibers and exhibit short- and long-latency activity in response to somatosensory stimulation. Previous studies have demonstrated that evoked short- and long-latency complex spikes generally occur on separate trials and that this response segregation is regulated by inhibitory feedback to the inferior olive. The present experiment tested the hypothesis that complex spikes evoked by periorbital stimulation are regulated by inhibitory feedback from the cerebellum and that this feedback develops between postnatal days (PND) 17 and 24. Recordings from individual Purkinje cell complex spikes in urethan-anesthetized rats indicated that the segregation of short- and long-latency evoked complex spike activity emerges between PND17 and PND24. In addition, infusion of picrotoxin, a GABAA-receptor antagonist, into the inferior olive abolished the response pattern segregation in PND24 rats, producing evoked complex spike response patterns similar to those characteristic of younger rats. These data support the view that cerebellar feedback to the inferior olive, which is exclusively inhibitory, undergoes substantial changes in the same developmental time window in which certain forms of motor learning emerge.

Reproduction of complex spike firing patterns with modulated effective coupling conductance in inferior olive neurons

2010 ◽  
Vol 68 ◽  
pp. e435 ◽  
Author(s):  
Miho Onizuka ◽  
Nicolas Schweighofer ◽  
Yuichi Katori ◽  
Kazuyuki Aihara ◽  
Keisuke Toyama ◽  
...  
Keyword(s):  
Inferior Olive ◽  
Effective Coupling ◽  
Firing Patterns ◽  
Complex Spike ◽  
Inferior Olive Neurons ◽  
Coupling Conductance ◽  
Spike Firing

Simple and Complex Spike Firing Patterns in Purkinje Cells During Classical Conditioning

2008 ◽  
Vol 7 (4) ◽  
pp. 563-566 ◽  
Author(s):  
Anders Rasmussen ◽  
Dan-Anders Jirenhed ◽  
Germund Hesslow
Keyword(s):  
Classical Conditioning ◽  
Purkinje Cells ◽  
Firing Patterns ◽  
Complex Spike ◽  
Spike Firing

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)

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