Spontaneous behaviour is structured by reinforcement without explicit reward

Jeffrey E. Markowitz, Winthrop F. Gillis, Maya Jay, Jeffrey Wood, Ryley W. Harris, Robert Cieszkowski, Rebecca Scott, David Brann, Dorothy Koveal, Tomasz Kula, Caleb Weinreb, Mohammed Abdal Monium Osman, Sandra Romero Pinto, Naoshige Uchida, Scott W. Linderman, Bernardo L. Sabatini and Sandeep Robert Datta ()
Additional contact information
Jeffrey E. Markowitz: Harvard Medical School
Winthrop F. Gillis: Harvard Medical School
Maya Jay: Harvard Medical School
Jeffrey Wood: Harvard Medical School
Ryley W. Harris: Harvard Medical School
Robert Cieszkowski: Harvard Medical School
Rebecca Scott: Harvard Medical School
David Brann: Harvard Medical School
Dorothy Koveal: Harvard Medical School
Tomasz Kula: Harvard Medical School
Caleb Weinreb: Harvard Medical School
Mohammed Abdal Monium Osman: Harvard Medical School
Sandra Romero Pinto: Harvard University
Naoshige Uchida: Harvard University
Scott W. Linderman: Stanford University
Bernardo L. Sabatini: Harvard Medical School
Sandeep Robert Datta: Harvard Medical School

Nature, 2023, vol. 614, issue 7946, 108-117

Abstract: Abstract Spontaneous animal behaviour is built from action modules that are concatenated by the brain into sequences1,2. However, the neural mechanisms that guide the composition of naturalistic, self-motivated behaviour remain unknown. Here we show that dopamine systematically fluctuates in the dorsolateral striatum (DLS) as mice spontaneously express sub-second behavioural modules, despite the absence of task structure, sensory cues or exogenous reward. Photometric recordings and calibrated closed-loop optogenetic manipulations during open field behaviour demonstrate that DLS dopamine fluctuations increase sequence variation over seconds, reinforce the use of associated behavioural modules over minutes, and modulate the vigour with which modules are expressed, without directly influencing movement initiation or moment-to-moment kinematics. Although the reinforcing effects of optogenetic DLS dopamine manipulations vary across behavioural modules and individual mice, these differences are well predicted by observed variation in the relationships between endogenous dopamine and module use. Consistent with the possibility that DLS dopamine fluctuations act as a teaching signal, mice build sequences during exploration as if to maximize dopamine. Together, these findings suggest a model in which the same circuits and computations that govern action choices in structured tasks have a key role in sculpting the content of unconstrained, high-dimensional, spontaneous behaviour.

Date: 2023
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DOI: 10.1038/s41586-022-05611-2

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