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Cerebellar granule cells encode the expectation of reward
The human brain contains ~60 billion cerebellar granule cells(1), which outnumber all other neurons combined. Classical theories posit that a large, diverse population of granule cells allows for highly detailed representations of sensorimotor context, enabling downstream Purkinje cells to sense fin...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
2017
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5532014/ https://www.ncbi.nlm.nih.gov/pubmed/28321129 http://dx.doi.org/10.1038/nature21726 |
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author | Wagner, Mark J Kim, Tony Hyun Savall, Joan Schnitzer, Mark J Luo, Liqun |
author_facet | Wagner, Mark J Kim, Tony Hyun Savall, Joan Schnitzer, Mark J Luo, Liqun |
author_sort | Wagner, Mark J |
collection | PubMed |
description | The human brain contains ~60 billion cerebellar granule cells(1), which outnumber all other neurons combined. Classical theories posit that a large, diverse population of granule cells allows for highly detailed representations of sensorimotor context, enabling downstream Purkinje cells to sense fine contextual changes(2–6). Although evidence suggests a role for cerebellum in cognition(7–10), granule cells are known to encode only sensory(11–13) and motor(14) context. Using two-photon calcium imaging in behaving mice, here we show that granule cells convey information about the expectation of reward. Mice initiated voluntary forelimb movements for delayed water reward. Some granule cells responded preferentially to reward or reward omission, whereas others selectively encoded reward anticipation. Reward responses were not restricted to forelimb movement, as a Pavlovian task evoked similar responses. Compared to predictable rewards, unexpected rewards elicited markedly different granule cell activity despite identical stimuli and licking responses. In both tasks, reward signals were widespread throughout multiple cerebellar lobules. Tracking the same granule cells over several days of learning revealed that cells with reward-anticipating responses emerged from those that responded at the start of learning to reward delivery, whereas reward omission responses grew stronger as learning progressed. The discovery of predictive, non-sensorimotor encoding in granule cells is a major departure from current understanding of these neurons and dramatically enriches contextual information available to postsynaptic Purkinje cells, with important implications for cognitive processing in the cerebellum. |
format | Online Article Text |
id | pubmed-5532014 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2017 |
record_format | MEDLINE/PubMed |
spelling | pubmed-55320142017-09-20 Cerebellar granule cells encode the expectation of reward Wagner, Mark J Kim, Tony Hyun Savall, Joan Schnitzer, Mark J Luo, Liqun Nature Article The human brain contains ~60 billion cerebellar granule cells(1), which outnumber all other neurons combined. Classical theories posit that a large, diverse population of granule cells allows for highly detailed representations of sensorimotor context, enabling downstream Purkinje cells to sense fine contextual changes(2–6). Although evidence suggests a role for cerebellum in cognition(7–10), granule cells are known to encode only sensory(11–13) and motor(14) context. Using two-photon calcium imaging in behaving mice, here we show that granule cells convey information about the expectation of reward. Mice initiated voluntary forelimb movements for delayed water reward. Some granule cells responded preferentially to reward or reward omission, whereas others selectively encoded reward anticipation. Reward responses were not restricted to forelimb movement, as a Pavlovian task evoked similar responses. Compared to predictable rewards, unexpected rewards elicited markedly different granule cell activity despite identical stimuli and licking responses. In both tasks, reward signals were widespread throughout multiple cerebellar lobules. Tracking the same granule cells over several days of learning revealed that cells with reward-anticipating responses emerged from those that responded at the start of learning to reward delivery, whereas reward omission responses grew stronger as learning progressed. The discovery of predictive, non-sensorimotor encoding in granule cells is a major departure from current understanding of these neurons and dramatically enriches contextual information available to postsynaptic Purkinje cells, with important implications for cognitive processing in the cerebellum. 2017-03-20 2017-04-06 /pmc/articles/PMC5532014/ /pubmed/28321129 http://dx.doi.org/10.1038/nature21726 Text en Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms |
spellingShingle | Article Wagner, Mark J Kim, Tony Hyun Savall, Joan Schnitzer, Mark J Luo, Liqun Cerebellar granule cells encode the expectation of reward |
title | Cerebellar granule cells encode the expectation of reward |
title_full | Cerebellar granule cells encode the expectation of reward |
title_fullStr | Cerebellar granule cells encode the expectation of reward |
title_full_unstemmed | Cerebellar granule cells encode the expectation of reward |
title_short | Cerebellar granule cells encode the expectation of reward |
title_sort | cerebellar granule cells encode the expectation of reward |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5532014/ https://www.ncbi.nlm.nih.gov/pubmed/28321129 http://dx.doi.org/10.1038/nature21726 |
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