Cerebellar granule cells acquire a widespread predictive feedback signal during motor learning

Andrea Giovannucci, Aleksandra Badura, Ben Deverett, Farzaneh Najafi, Talmo D. Pereira, Zhenyu Gao, Ilker Ozden, Alexander D. Kloth, Eftychios Pnevmatikakis, Liam Paninski, Chris I. De Zeeuw, Javier F. Medina, Samuel Sheng-Hung Wang

Research output: Contribution to journalArticle

45 Citations (Scopus)

Abstract

Cerebellar granule cells, which constitute half the brain's neurons, supply Purkinje cells with contextual information necessary for motor learning, but how they encode this information is unknown. Here we show, using two-photon microscopy to track neural activity over multiple days of cerebellum-dependent eyeblink conditioning in mice, that granule cell populations acquire a dense representation of the anticipatory eyelid movement. Initially, granule cells responded to neutral visual and somatosensory stimuli as well as periorbital airpuffs used for training. As learning progressed, two-thirds of monitored granule cells acquired a conditional response whose timing matched or preceded the learned eyelid movements. Granule cell activity covaried trial by trial to form a redundant code. Many granule cells were also active during movements of nearby body structures. Thus, a predictive signal about the upcoming movement is widely available at the input stage of the cerebellar cortex, as required by forward models of cerebellar control.

Original languageEnglish (US)
Pages (from-to)727-734
Number of pages8
JournalNature neuroscience
Volume20
Issue number5
DOIs
StatePublished - May 1 2017

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Learning
Eyelids
Cerebellar Cortex
Purkinje Cells
Photons
Cerebellum
Microscopy
Neurons
Brain
Population

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)

Cite this

Giovannucci, Andrea ; Badura, Aleksandra ; Deverett, Ben ; Najafi, Farzaneh ; Pereira, Talmo D. ; Gao, Zhenyu ; Ozden, Ilker ; Kloth, Alexander D. ; Pnevmatikakis, Eftychios ; Paninski, Liam ; De Zeeuw, Chris I. ; Medina, Javier F. ; Wang, Samuel Sheng-Hung. / Cerebellar granule cells acquire a widespread predictive feedback signal during motor learning. In: Nature neuroscience. 2017 ; Vol. 20, No. 5. pp. 727-734.
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Giovannucci, A, Badura, A, Deverett, B, Najafi, F, Pereira, TD, Gao, Z, Ozden, I, Kloth, AD, Pnevmatikakis, E, Paninski, L, De Zeeuw, CI, Medina, JF & Wang, SS-H 2017, 'Cerebellar granule cells acquire a widespread predictive feedback signal during motor learning', Nature neuroscience, vol. 20, no. 5, pp. 727-734. https://doi.org/10.1038/nn.4531

Cerebellar granule cells acquire a widespread predictive feedback signal during motor learning. / Giovannucci, Andrea; Badura, Aleksandra; Deverett, Ben; Najafi, Farzaneh; Pereira, Talmo D.; Gao, Zhenyu; Ozden, Ilker; Kloth, Alexander D.; Pnevmatikakis, Eftychios; Paninski, Liam; De Zeeuw, Chris I.; Medina, Javier F.; Wang, Samuel Sheng-Hung.

In: Nature neuroscience, Vol. 20, No. 5, 01.05.2017, p. 727-734.

Research output: Contribution to journalArticle

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Giovannucci A, Badura A, Deverett B, Najafi F, Pereira TD, Gao Z et al. Cerebellar granule cells acquire a widespread predictive feedback signal during motor learning. Nature neuroscience. 2017 May 1;20(5):727-734. https://doi.org/10.1038/nn.4531