Purkinje cells translate subjective salience into readiness to act and choice performance

Lorenzo Bina; Vincenzo Romano; Tycho M. Hoogland; Laurens W.J. Bosman; Chris I. De Zeeuw

doi:10.1016/j.celrep.2021.110116

Purkinje cells translate subjective salience into readiness to act and choice performance

Lorenzo Bina, Vincenzo Romano, Tycho M. Hoogland, Laurens W.J. Bosman^*, Chris I. De Zeeuw^*

^*Corresponding author for this work

Neurosciences

Research output: Contribution to journal › Article › Academic › peer-review

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Abstract

The brain selectively allocates attention from a continuous stream of sensory input. This process is typically attributed to computations in distinct regions of the forebrain and midbrain. Here, we explore whether cerebellar Purkinje cells encode information about the selection of sensory inputs and could thereby contribute to non-motor forms of learning. We show that complex spikes of individual Purkinje cells change the sensory modality they encode to reflect changes in the perceived salience of sensory input. Comparisons with mouse models deficient in cerebellar plasticity suggest that changes in complex spike activity instruct potentiation of Purkinje cells simple spike firing, which is required for efficient learning. Our findings suggest that during learning, climbing fibers do not directly guide motor output, but rather contribute to a general readiness to act via changes in simple spike activity, thereby bridging the sequence from non-motor to motor functions.

Original language	English
Article number	110116
Journal	Cell Reports
Volume	37
Issue number	11
DOIs	https://doi.org/10.1016/j.celrep.2021.110116
Publication status	Published - 14 Dec 2021

Bibliographical note

Funding Information:
The authors wish to thank Sander van Gurp, Sander Lindeman, and Mario Negrello for their contributions to the pilot phase of this project; Hugo Hoedemaker, Maryam El Hamdioui, Danique Broere, Morgann Dettingmeijer, and Celia Mak for their aid with surgeries and data collection; Marcel van der Heijden for recording and analyzing the sound of the stimulator; Sanne Smid for help with video analysis; and Gerard Borst and Steven Kushner for discussions on the interpretation and presentation of the results. Financial support was provided by the Netherlands Organization for Scientific Research (NWO-ALW; C.I.D.Z.), the Dutch Organization for Medical Sciences (ZonMW; C.I.D.Z.), BIG (C.I.D.Z.), Medical Neuro-Delta (C.I.D.Z.), INTENSE LSH-NWO (C.I.D.Z.), ERC-adv and ERC-POC (C.I.D.Z.), Van Raamsdonk-fonds (C.I.D.Z.), 3V-Fonds KNAW (T.M.H. and C.I.D.Z.), Albinism Fonds NIN (C.I.D.Z.), and Health Holland (TKI-LSH LSHM18001 [T.M.H.] and TKI-LSH EMCLSH21017 [L.W.J.B.]).

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© 2021 The Authors

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title = "Purkinje cells translate subjective salience into readiness to act and choice performance",

abstract = "The brain selectively allocates attention from a continuous stream of sensory input. This process is typically attributed to computations in distinct regions of the forebrain and midbrain. Here, we explore whether cerebellar Purkinje cells encode information about the selection of sensory inputs and could thereby contribute to non-motor forms of learning. We show that complex spikes of individual Purkinje cells change the sensory modality they encode to reflect changes in the perceived salience of sensory input. Comparisons with mouse models deficient in cerebellar plasticity suggest that changes in complex spike activity instruct potentiation of Purkinje cells simple spike firing, which is required for efficient learning. Our findings suggest that during learning, climbing fibers do not directly guide motor output, but rather contribute to a general readiness to act via changes in simple spike activity, thereby bridging the sequence from non-motor to motor functions.",

author = "Lorenzo Bina and Vincenzo Romano and Hoogland, {Tycho M.} and Bosman, {Laurens W.J.} and {De Zeeuw}, {Chris I.}",

note = "Funding Information: The authors wish to thank Sander van Gurp, Sander Lindeman, and Mario Negrello for their contributions to the pilot phase of this project; Hugo Hoedemaker, Maryam El Hamdioui, Danique Broere, Morgann Dettingmeijer, and Celia Mak for their aid with surgeries and data collection; Marcel van der Heijden for recording and analyzing the sound of the stimulator; Sanne Smid for help with video analysis; and Gerard Borst and Steven Kushner for discussions on the interpretation and presentation of the results. Financial support was provided by the Netherlands Organization for Scientific Research (NWO-ALW; C.I.D.Z.), the Dutch Organization for Medical Sciences (ZonMW; C.I.D.Z.), BIG (C.I.D.Z.), Medical Neuro-Delta (C.I.D.Z.), INTENSE LSH-NWO (C.I.D.Z.), ERC-adv and ERC-POC (C.I.D.Z.), Van Raamsdonk-fonds (C.I.D.Z.), 3V-Fonds KNAW (T.M.H. and C.I.D.Z.), Albinism Fonds NIN (C.I.D.Z.), and Health Holland (TKI-LSH LSHM18001 [T.M.H.] and TKI-LSH EMCLSH21017 [L.W.J.B.]). Publisher Copyright: {\textcopyright} 2021 The Authors",

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AU - De Zeeuw, Chris I.

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N2 - The brain selectively allocates attention from a continuous stream of sensory input. This process is typically attributed to computations in distinct regions of the forebrain and midbrain. Here, we explore whether cerebellar Purkinje cells encode information about the selection of sensory inputs and could thereby contribute to non-motor forms of learning. We show that complex spikes of individual Purkinje cells change the sensory modality they encode to reflect changes in the perceived salience of sensory input. Comparisons with mouse models deficient in cerebellar plasticity suggest that changes in complex spike activity instruct potentiation of Purkinje cells simple spike firing, which is required for efficient learning. Our findings suggest that during learning, climbing fibers do not directly guide motor output, but rather contribute to a general readiness to act via changes in simple spike activity, thereby bridging the sequence from non-motor to motor functions.

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Purkinje cells translate subjective salience into readiness to act and choice performance

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