Dataset Information

Cerebellar climbing fibers encode expected reward size.

ABSTRACT: Climbing fiber inputs to the cerebellum encode error signals that instruct learning. Recently, evidence has accumulated to suggest that the cerebellum is also involved in the processing of reward. To study how rewarding events are encoded, we recorded the activity of climbing fibers when monkeys were engaged in an eye movement task. At the beginning of each trial, the monkeys were cued to the size of the reward that would be delivered upon successful completion of the trial. Climbing fiber activity increased when the monkeys were presented with a cue indicating a large reward, but not a small reward. Reward size did not modulate activity at reward delivery or during eye movements. Comparison between climbing fiber and simple spike activity indicated different interactions for coding of movement and reward. These results indicate that climbing fibers encode the expected reward size and suggest a general role of the cerebellum in associative learning beyond error correction.

SUBMITTER: Larry N

PROVIDER: S-EPMC6844644 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Publications

Cerebellar climbing fibers encode expected reward size.

Larry Noga N Yarkoni Merav M Lixenberg Adi A Joshua Mati M

eLife 20191029

Climbing fiber inputs to the cerebellum encode error signals that instruct learning. Recently, evidence has accumulated to suggest that the cerebellum is also involved in the processing of reward. To study how rewarding events are encoded, we recorded the activity of climbing fibers when monkeys were engaged in an eye movement task. At the beginning of each trial, the monkeys were cued to the size of the reward that would be delivered upon successful completion of the trial. Climbing fiber activ ...[more]

PMID: 31661073

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Project description:A crucial issue in understanding cerebellar function is the interaction between simple spike (SS) and complex spike (CS) discharge, the two fundamentally different activity modalities of Purkinje cells. Although several hypotheses have provided insights into the interaction, none fully explains or is completely consistent with the spectrum of experimental observations. Here, we show that during a pseudo-random manual tracking task in the monkey (Macaca mulatta), climbing fiber discharge dynamically controls the information present in the SS firing, triggering robust and rapid changes in the SS encoding of motor signals in 67% of Purkinje cells. The changes in encoding, tightly coupled to CS occurrences, consist of either increases or decreases in the SS sensitivity to kinematics or position errors and are not due to differences in SS firing rates or variability. Nor are the changes in sensitivity due to CS rhythmicity. In addition, the CS-coupled changes in encoding are not evoked by changes in kinematics or position errors. Instead, CS discharge most often leads alterations in behavior. Increases in SS encoding of a kinematic parameter are associated with larger changes in that parameter than are decreases in SS encoding. Increases in SS encoding of position error are followed by and scale with decreases in error. The results suggest a novel function of CSs, in which climbing fiber input dynamically controls the state of Purkinje cell SS encoding in advance of changes in behavior.SIGNIFICANCE STATEMENT Purkinje cells, the sole output of the cerebellar cortex, manifest two fundamentally different activity modalities, complex spike (CS) discharge and simple spike (SS) firing. Elucidating cerebellar function will require an understanding of the interactions, both short- and long-term, between CS and SS firing. This study shows that CSs dynamically control the information encoded in a Purkinje cell's SS activity by rapidly increasing or decreasing the SS sensitivity to kinematics and/or performance errors independent of firing rate. In many cases, the CS-coupled shift in SS encoding leads a change in behavior. These novel findings on the interaction between CS and SS firing provide for a new hypothesis in which climbing fiber input adjusts the encoding of SS information in advance of a change in behavior.

Dataset Information

Cerebellar climbing fibers encode expected reward size.

Publications

Cerebellar climbing fibers encode expected reward size.

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