Cerebellar Complex Spike Firing Is Suitable to Induce as Well as to Stabilize Motor Learning

Catz, Nicolas; Dicke, Peter W.; Thier, Peter

doi:10.1016/j.cub.2005.11.037

Cited by 105 publications

(118 citation statements)

References 25 publications

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“…Such well directed changes in effectiveness could be a consequence of the modulation of the climbing fibers responses. In fact, we have recently shown (20) that STSA leads to a redistribution of CSs with more CSs right around saccade end in the case of inward adaptation and a CS pause around the time of saccade end in the case of outward adaptation. Assuming that CSs induce long-term depression of parallel fiber synapses (21), more CSs around the saccade end should suppress SS activity in this period, thereby shortening the PB as observed.…”

Section: Discussionmentioning

confidence: 95%

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Cerebellar-dependent motor learning is based on pruning a Purkinje cell population response

Catz

Dicke

Thier

2008

Proc. Natl. Acad. Sci. U.S.A.

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124

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The improvement of motor behavior, based on experience, is a form of learning that is critically dependent on the cerebellum. A well studied example of cerebellar motor learning is short-term saccadic adaptation (STSA). In STSA, information on saccadic errors is used to improve future saccades. The information optimizing saccade metrics is conveyed by Purkinje cells simple spikes (PC-SS) because they are the critical input to the premotor circuits for saccades. We recorded PC-SS of monkeys undergoing STSA to reveal the code used for improving behavior. We found that the discharge of individual PC-SS was unable to account for the behavioral changes. The PC-SS population burst (PB), however, exhibited changes that closely paralleled the qualitatively different changes of saccade kinematics associated with gain-increase and gain-decrease STSA, respectively. Gain-increase STSA, characterized by an increase in saccade duration, replicates the relationship between saccade duration and the end of the PB valid for unadapted saccades. In contrast, gain-decrease STSA, which sports normal saccade duration but reduced saccadic velocity, is characterized by a PB that ends well before the adapted saccade. This suggests that the duration of normal as well as gain-increased saccades is determined by appropriately setting the end of PB end. However, the duration of gain-decreased saccades is apparently not modified by the cerebellum because the PB signals ends too early to determine saccade end. In summary, STSA, and most probably cerebellar-dependent learning in general, is based on optimizing the shape of a PC-SS population response.

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Section: Discussionmentioning

confidence: 95%

“…The arrow indicates the course of adaptation. The CS responses were taken from a recent study on the influence of STSA on CS discharge patterns (20).…”

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confidence: 99%

Cerebellar-dependent motor learning is based on pruning a Purkinje cell population response

Catz

Dicke

Thier

2008

Proc. Natl. Acad. Sci. U.S.A.

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124

100

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“…We surmised that P-cells that already had SS activity related to saccades would be more likely to exhibit changes in CS activity during saccade errors than those that did not. Note that Catz et al (2005) tested all P-cells in folia with oculomotor activity whether or not the P-cells exhibited a saccade-related change in SS activity. To test for saccade-related SS activity, we asked the monkey to make 15°saccades to target jumps that started straight ahead and landed along one of eight directions spaced at 45°intervals from 0 to 315°and chosen pseudo-randomly (Spike2 random number generator function).…”

Section: General Proceduresmentioning

confidence: 99%

“…During backward adaptation, Catz et al (2005) reported an increase in both the rate and duration of the average population CS response as adaptation evolved. The change began during the saccade and ended early in the intersaccadic error interval (their Fig.…”

Section: Comparison With Other Studiesmentioning

confidence: 99%

Complex Spike Activity in the Oculomotor Vermis of the Cerebellum: A Vectorial Error Signal for Saccade Motor Learning?

Soetedjo¹,

Kojima²,

Fuchs³

2008

Journal of Neurophysiology

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Soetedjo R, Kojima Y, Fuchs AF. Complex spike activity in the oculomotor vermis of the cerebellum: a vectorial error signal for saccade motor learning ? J Neurophysiol 100: 1949-1966, 2008. First published July 23, 2008 doi:10.1152/jn.90526.2008. Brain stem signals that generate saccadic eye movements originate in the superior colliculus. They reach the pontine burst generator for horizontal saccades via short-latency pathways and a longer pathway through the oculomotor vermis (OMV) of the cerebellum. Lesion studies implicate the OMV in the adaptation of saccade amplitude that occurs when saccades become inaccurate because of extraocular muscle weakness or behavioral manipulations. We studied the nature of the possible error signal that might drive adaptation by examining the complex spike (CS) activity of vermis Purkinje (P-) cells in monkeys. We produced a saccade error by displacing the target as a saccade was made toward it; a corrective saccade ϳ200 ms later eliminated the resulting error. In most P-cells, the probability of CS firing changed, but only in the error interval between the primary and corrective saccade. For most P-cells, CSs occurred in a tight cluster ϳ100 ms after error onset. The probability of CS occurrence depended on both error direction and size. Across our sample, all error directions were represented; most had a horizontal component. In more than one half of our P-cells, the probability of CS occurrence was greatest for error sizes Ͻ5°a nd less for larger errors. In the remaining cells, there was a uniform increased probability of CS occurrence for all errors Յ7-9°. CS responses disappeared when the target was extinguished during a saccade. We discuss the properties of this putative CS error signal in the context of the characteristics of saccade adaptation produced by the target displacement paradigm.

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“…The deeper layers of the SC are connected to the medioposterior cerebellum (caudal fastigial nucleus and oculomotor vermis; Ohtsuka and Noda 1990) via nucleus reticularis tegmenti pontis (NRTP; May et al 1990;Ohtsuka and Noda 1990) and dorsal lateral pontine nucleus (Thier and Mock 2005). Lesions to the medioposterior cerebellum impair rapid saccade amplitude adaptation during the McLaughlin task (Barash et al 1999;Robinson et al 2002;Takagi et al 2000) and the burst metrics of neurons in NRTP (Takeichi et al 2005), caudal fastigial nucleus (Inaba et al 2003;Scudder and McGee 2003), and oculomotor vermis (Catz et al 2005(Catz et al , 2008Soetedjo and Fuchs 2006) are altered along with saccade amplitude during head-restrained saccadic adaptation. Future studies are required to classify the types of motor command signals (gaze, eye, or head) represented at each level of this circuit prior to describing modifications to these signals during gaze adaptation using the McLaughlin task.…”

Section: Physiological Implicationsmentioning

confidence: 99%

Head-Unrestrained Gaze Adaptation in the Rhesus Macaque

Cecala

Freedman²

2009

Journal of Neurophysiology

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. The ability to adjust the amplitude of gaze shifts in response to persistent visual errors ("gaze adaptation") has been investigated primarily by introducing visual errors at the end of saccades produced by head-restrained primates. Very little is known about the behavior and neural mechanisms underlying gaze adaptation when the head is free to move. We tested alternative hypotheses about the signals that are altered during gaze adaptation by increasing (25°3 50°; "forward adaptation") or decreasing (50°3 25°; "backward adaptation") the size of large, head-unrestrained gaze shifts. In our three rhesus monkey subjects, changes to primary gaze shift amplitude occurred regardless of the particular combinations of eye and head movements that made up the amplitude-altered gaze shifts. The relative changes to eye and head movements that occurred during adaptation could be predicted based on the magnitude of gaze adaptation and the positions of the eyes in the orbits at gaze onset. These results are consistent with the hypothesis that gaze adaptation occurs at the level of a gaze shift command and inconsistent with hypotheses based on the assumption that gaze adaptation results from alterations to eye-and/or head-specific signals.

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Cerebellar Complex Spike Firing Is Suitable to Induce as Well as to Stabilize Motor Learning

Abstract: We suggest that CS firing may underlie the stabilization of a learned motor behavior, rather than serving as an electrophysiological correlate of an error.

Cited by 105 publications

References 25 publications

Cerebellar-dependent motor learning is based on pruning a Purkinje cell population response

Cerebellar-dependent motor learning is based on pruning a Purkinje cell population response

Complex Spike Activity in the Oculomotor Vermis of the Cerebellum: A Vectorial Error Signal for Saccade Motor Learning?

Head-Unrestrained Gaze Adaptation in the Rhesus Macaque

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