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Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys.

Medina JF, Lisberger SG - Nat. Neurosci. (2008)

Bottom Line: The hypothesis of cerebellar learning proposes that complex spikes in Purkinje cells engage mechanisms of plasticity in the cerebellar cortex; in turn, changes in the cerebellum depress the simple-spike response of Purkinje cells to a given stimulus and cause the adaptive modification of a motor behavior.Many elements of this hypothesis have been supported by prior experiments, and correlations have been found [corrected] between complex spikes, simple-spike plasticity and behavior [corrected] during the learning process.We carried out a trial-by-trial analysis of Purkinje cell responses in awake-behaving monkeys and found evidence for a causal role for complex spikes in the induction of cerebellar plasticity during a simple motor learning task.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Pennsylvania, 3720 Walnut Street, Philadelphia, Pennsylvania 19104, USA.

ABSTRACT
The hypothesis of cerebellar learning proposes that complex spikes in Purkinje cells engage mechanisms of plasticity in the cerebellar cortex; in turn, changes in the cerebellum depress the simple-spike response of Purkinje cells to a given stimulus and cause the adaptive modification of a motor behavior. Many elements of this hypothesis have been supported by prior experiments, and correlations have been found [corrected] between complex spikes, simple-spike plasticity and behavior [corrected] during the learning process. We carried out a trial-by-trial analysis of Purkinje cell responses in awake-behaving monkeys and found evidence for a causal role for complex spikes in the induction of cerebellar plasticity during a simple motor learning task. We found that the presence of a complex spike on one learning trial was linked to a substantial depression of simple-spike responses on the subsequent trial, at a time when behavioral learning was expressed.

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Neural and behavioral learning after single complex spikes emitted at the offset of target motion in on-direction learning trials. a,c: Black and red traces show average eye velocity and simple spike firing in the first 10 learning trials and after 100 learning trials. In a, the black dashed trace shows target velocity. The arrow indicates the time when off-direction image motion was present because the eyes were moving in the on-direction and the target was stationary. b: Probability of a complex spike in the learning trials. Traces in a-c are averages across 13 Purkinje cells. Legend below a also applies to c. d,e; average trial-over-trial change in simple spike firing (d) and eye velocity (e), for the “0-0” sequences (blue) and the “1-0” sequences (red). The target ceased moving at t=0, and the two vertical dashed lines bound the interval when learning was analyzed. The black traces show the average change obtained by performing the trial-over-trial subtraction on 200 randomly chosen sequences of 2 consecutive learning trials, and the gray envelope indicates ±2 SD. f: Red and black traces show learned changes in simple spike firing rate and eye velocity. Vertical dashed line indicates the time of the offset of target motion. Horizontal dashed line indicates zero. g: Quantitative relationship between complex spike probability and learned changes in simple spike activity. Blue symbols show data from the offset of target motion in on-direction learning experiments; gray symbols are replotted from Figure 4 showing data from the change in target direction in off-direction learning experiments.
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Figure 7: Neural and behavioral learning after single complex spikes emitted at the offset of target motion in on-direction learning trials. a,c: Black and red traces show average eye velocity and simple spike firing in the first 10 learning trials and after 100 learning trials. In a, the black dashed trace shows target velocity. The arrow indicates the time when off-direction image motion was present because the eyes were moving in the on-direction and the target was stationary. b: Probability of a complex spike in the learning trials. Traces in a-c are averages across 13 Purkinje cells. Legend below a also applies to c. d,e; average trial-over-trial change in simple spike firing (d) and eye velocity (e), for the “0-0” sequences (blue) and the “1-0” sequences (red). The target ceased moving at t=0, and the two vertical dashed lines bound the interval when learning was analyzed. The black traces show the average change obtained by performing the trial-over-trial subtraction on 200 randomly chosen sequences of 2 consecutive learning trials, and the gray envelope indicates ±2 SD. f: Red and black traces show learned changes in simple spike firing rate and eye velocity. Vertical dashed line indicates the time of the offset of target motion. Horizontal dashed line indicates zero. g: Quantitative relationship between complex spike probability and learned changes in simple spike activity. Blue symbols show data from the offset of target motion in on-direction learning experiments; gray symbols are replotted from Figure 4 showing data from the change in target direction in off-direction learning experiments.

Mentions: An independent confirmation of the trial-over-trial effect of a single complex spike comes from analysis of an unanticipated sharp increase in the probability of complex spike responses just after the offset of target motion for on-direction learning trials (Fig. 7b). At this time, smooth eye velocity is in the on-direction of the Purkinje cell (for simple spike responses), and off-direction image motion (the main stimulus for complex spike responses20,21) occurs because the target is suddenly stationary while the eyes keep moving (arrow in Fig. 7a).


Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys.

Medina JF, Lisberger SG - Nat. Neurosci. (2008)

Neural and behavioral learning after single complex spikes emitted at the offset of target motion in on-direction learning trials. a,c: Black and red traces show average eye velocity and simple spike firing in the first 10 learning trials and after 100 learning trials. In a, the black dashed trace shows target velocity. The arrow indicates the time when off-direction image motion was present because the eyes were moving in the on-direction and the target was stationary. b: Probability of a complex spike in the learning trials. Traces in a-c are averages across 13 Purkinje cells. Legend below a also applies to c. d,e; average trial-over-trial change in simple spike firing (d) and eye velocity (e), for the “0-0” sequences (blue) and the “1-0” sequences (red). The target ceased moving at t=0, and the two vertical dashed lines bound the interval when learning was analyzed. The black traces show the average change obtained by performing the trial-over-trial subtraction on 200 randomly chosen sequences of 2 consecutive learning trials, and the gray envelope indicates ±2 SD. f: Red and black traces show learned changes in simple spike firing rate and eye velocity. Vertical dashed line indicates the time of the offset of target motion. Horizontal dashed line indicates zero. g: Quantitative relationship between complex spike probability and learned changes in simple spike activity. Blue symbols show data from the offset of target motion in on-direction learning experiments; gray symbols are replotted from Figure 4 showing data from the change in target direction in off-direction learning experiments.
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Figure 7: Neural and behavioral learning after single complex spikes emitted at the offset of target motion in on-direction learning trials. a,c: Black and red traces show average eye velocity and simple spike firing in the first 10 learning trials and after 100 learning trials. In a, the black dashed trace shows target velocity. The arrow indicates the time when off-direction image motion was present because the eyes were moving in the on-direction and the target was stationary. b: Probability of a complex spike in the learning trials. Traces in a-c are averages across 13 Purkinje cells. Legend below a also applies to c. d,e; average trial-over-trial change in simple spike firing (d) and eye velocity (e), for the “0-0” sequences (blue) and the “1-0” sequences (red). The target ceased moving at t=0, and the two vertical dashed lines bound the interval when learning was analyzed. The black traces show the average change obtained by performing the trial-over-trial subtraction on 200 randomly chosen sequences of 2 consecutive learning trials, and the gray envelope indicates ±2 SD. f: Red and black traces show learned changes in simple spike firing rate and eye velocity. Vertical dashed line indicates the time of the offset of target motion. Horizontal dashed line indicates zero. g: Quantitative relationship between complex spike probability and learned changes in simple spike activity. Blue symbols show data from the offset of target motion in on-direction learning experiments; gray symbols are replotted from Figure 4 showing data from the change in target direction in off-direction learning experiments.
Mentions: An independent confirmation of the trial-over-trial effect of a single complex spike comes from analysis of an unanticipated sharp increase in the probability of complex spike responses just after the offset of target motion for on-direction learning trials (Fig. 7b). At this time, smooth eye velocity is in the on-direction of the Purkinje cell (for simple spike responses), and off-direction image motion (the main stimulus for complex spike responses20,21) occurs because the target is suddenly stationary while the eyes keep moving (arrow in Fig. 7a).

Bottom Line: The hypothesis of cerebellar learning proposes that complex spikes in Purkinje cells engage mechanisms of plasticity in the cerebellar cortex; in turn, changes in the cerebellum depress the simple-spike response of Purkinje cells to a given stimulus and cause the adaptive modification of a motor behavior.Many elements of this hypothesis have been supported by prior experiments, and correlations have been found [corrected] between complex spikes, simple-spike plasticity and behavior [corrected] during the learning process.We carried out a trial-by-trial analysis of Purkinje cell responses in awake-behaving monkeys and found evidence for a causal role for complex spikes in the induction of cerebellar plasticity during a simple motor learning task.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Pennsylvania, 3720 Walnut Street, Philadelphia, Pennsylvania 19104, USA.

ABSTRACT
The hypothesis of cerebellar learning proposes that complex spikes in Purkinje cells engage mechanisms of plasticity in the cerebellar cortex; in turn, changes in the cerebellum depress the simple-spike response of Purkinje cells to a given stimulus and cause the adaptive modification of a motor behavior. Many elements of this hypothesis have been supported by prior experiments, and correlations have been found [corrected] between complex spikes, simple-spike plasticity and behavior [corrected] during the learning process. We carried out a trial-by-trial analysis of Purkinje cell responses in awake-behaving monkeys and found evidence for a causal role for complex spikes in the induction of cerebellar plasticity during a simple motor learning task. We found that the presence of a complex spike on one learning trial was linked to a substantial depression of simple-spike responses on the subsequent trial, at a time when behavioral learning was expressed.

Show MeSH
Related in: MedlinePlus