A dopaminergic reward prediction error signal shapes maternal behavior in mice

Xie, Yunyao, Huang, Longwen, Corona, Alberto, Pagliaro, Alexa H, Shea, Stephen D (December 2022) A dopaminergic reward prediction error signal shapes maternal behavior in mice. Neuron. S0896-6273(22)01073. ISSN 0896-6273

URL: https://www.ncbi.nlm.nih.gov/pubmed/36543170

DOI: 10.1016/j.neuron.2022.11.019

Abstract

How social contact is perceived as rewarding and subsequently modifies interactions is unclear. Dopamine (DA) from the ventral tegmental area (VTA) regulates sociality, but the ongoing, unstructured nature of free behavior makes it difficult to ascertain how. Here, we tracked the emergence of a repetitive stereotyped parental retrieval behavior and conclude that VTA DA neurons incrementally refine it by reinforcement learning (RL). Trial-by-trial performance was correlated with the history of DA neuron activity, but DA signals were inconsistent with VTA directly influencing the current trial. We manipulated the subject's expectation of imminent pup contact and show that DA signals convey reward prediction error, a fundamental component of RL. Finally, closed-loop optogenetic inactivation of DA neurons at the onset of pup contact dramatically slowed emergence of parental care. We conclude that this component of maternal behavior is shaped by an RL mechanism in which social contact itself is the primary reward.

Item Type:	Paper
Subjects:	bioinformatics bioinformatics > genomics and proteomics > genetics & nucleic acid processing bioinformatics > genomics and proteomics bioinformatics > genomics and proteomics > genetics & nucleic acid processing > protein structure, function, modification organism description > animal organism description > animal behavior bioinformatics > genomics and proteomics > genetics & nucleic acid processing > protein structure, function, modification > protein types > dopamine organism description > animal > gender > female organism description > animal > gender organism description > animal behavior > learning organism description > animal > mammal organism description > animal behavior > maternal organism description > animal > mammal > rodent > mouse organs, tissues, organelles, cell types and functions > cell types and functions > cell types > neurons organs, tissues, organelles, cell types and functions > cell types and functions > cell types > neurons organs, tissues, organelles, cell types and functions > cell types and functions > cell types > neurons bioinformatics > genomics and proteomics > genetics & nucleic acid processing > protein structure, function, modification > protein types organism description > animal > mammal > rodent organs, tissues, organelles, cell types and functions > tissues types and functions > ventral tegmental area
CSHL Authors:	Huang, Longwen Corona, Alberto Pagliaro, Alexa Shea, Stephen D. Xie, Yunyao
Communities:	CSHL Cancer Center Program CSHL Cancer Center Shared Resources > Animal Services CSHL labs > Shea lab CSHL labs > Zador lab School of Biological Sciences > Publications
SWORD Depositor:	CSHL Elements
Depositing User:	CSHL Elements
Date:	13 December 2022
Date Deposited:	06 Jan 2023 16:59
Last Modified:	29 Feb 2024 18:49
PMCID:	PMC9957971
URI:	https://repository.cshl.edu/id/eprint/40782

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