PUBLICATION

Glia Accumulate Evidence that Actions Are Futile and Suppress Unsuccessful Behavior

Authors
Mu, Y., Bennett, D.V., Rubinov, M., Narayan, S., Yang, C.T., Tanimoto, M., Mensh, B.D., Looger, L.L., Ahrens, M.B.
ID
ZDB-PUB-190625-1
Date
2019
Source
Cell   178(1): 27-43.e19 (Journal)
Registered Authors
Ahrens, Misha, Bennett, Davis, Mu, Yu, Narayan, Sujatha, Yang, Chao-Tsung
Keywords
astrocytes, behavioral states, evidence accumulation, glia, learned helplessness, neuromodulation, neuroscience, noradrenaline, norepinephrine, zebrafish
MeSH Terms
  • Adrenergic Neurons/metabolism
  • Animals
  • Animals, Genetically Modified/physiology
  • Astrocytes/cytology
  • Astrocytes/metabolism*
  • Behavior, Animal/physiology*
  • Brain/diagnostic imaging
  • Brain/physiology
  • Brain Mapping
  • Calcium/metabolism
  • Cell Communication/physiology
  • Feedback, Sensory/physiology
  • GABAergic Neurons/metabolism
  • Larva/physiology*
  • Membrane Potentials/physiology
  • Optogenetics
  • Swimming/physiology
  • Zebrafish/physiology*
PubMed
31230713 Full text @ Cell
Abstract
When a behavior repeatedly fails to achieve its goal, animals often give up and become passive, which can be strategic for preserving energy or regrouping between attempts. It is unknown how the brain identifies behavioral failures and mediates this behavioral-state switch. In larval zebrafish swimming in virtual reality, visual feedback can be withheld so that swim attempts fail to trigger expected visual flow. After tens of seconds of such motor futility, animals became passive for similar durations. Whole-brain calcium imaging revealed noradrenergic neurons that responded specifically to failed swim attempts and radial astrocytes whose calcium levels accumulated with increasing numbers of failed attempts. Using cell ablation and optogenetic or chemogenetic activation, we found that noradrenergic neurons progressively activated brainstem radial astrocytes, which then suppressed swimming. Thus, radial astrocytes perform a computation critical for behavior: they accumulate evidence that current actions are ineffective and consequently drive changes in behavioral states. VIDEO ABSTRACT.
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