Cerebellar Neurodynamics Predict Decision Timing and Outcome on the Single-Trial Level

Cell. 2020 Feb 6;180(3):536-551.e17. doi: 10.1016/j.cell.2019.12.018. Epub 2020 Jan 16.

Abstract

Goal-directed behavior requires the interaction of multiple brain regions. How these regions and their interactions with brain-wide activity drive action selection is less understood. We have investigated this question by combining whole-brain volumetric calcium imaging using light-field microscopy and an operant-conditioning task in larval zebrafish. We find global, recurring dynamics of brain states to exhibit pre-motor bifurcations toward mutually exclusive decision outcomes. These dynamics arise from a distributed network displaying trial-by-trial functional connectivity changes, especially between cerebellum and habenula, which correlate with decision outcome. Within this network the cerebellum shows particularly strong and predictive pre-motor activity (>10 s before movement initiation), mainly within the granule cells. Turn directions are determined by the difference neuroactivity between the ipsilateral and contralateral hemispheres, while the rate of bi-hemispheric population ramping quantitatively predicts decision time on the trial-by-trial level. Our results highlight a cognitive role of the cerebellum and its importance in motor planning.

Keywords: Cerebellum; Light field microscopy; action selection; decision making; demixed principal component analysis; motor planning; operant learning; population ramping activity; whole-brain calcium imaging; zebrafish.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Behavior, Animal / physiology
  • Brain Mapping / methods
  • Cerebellum / physiology*
  • Cerebrum / physiology
  • Cognition / physiology
  • Conditioning, Operant / physiology
  • Decision Making / physiology*
  • Goals
  • Habenula / physiology
  • Hot Temperature
  • Larva / physiology
  • Motor Activity / physiology
  • Movement
  • Neurons / physiology
  • Psychomotor Performance / physiology
  • Reaction Time / physiology*
  • Rhombencephalon / physiology
  • Zebrafish / physiology*