Models of heterogeneous dopamine signaling in an insect learning and memory center.


Journal

PLoS computational biology
ISSN: 1553-7358
Titre abrégé: PLoS Comput Biol
Pays: United States
ID NLM: 101238922

Informations de publication

Date de publication:
08 2021
Historique:
received: 09 06 2020
accepted: 22 06 2021
entrez: 10 8 2021
pubmed: 11 8 2021
medline: 23 11 2021
Statut: epublish

Résumé

The Drosophila mushroom body exhibits dopamine dependent synaptic plasticity that underlies the acquisition of associative memories. Recordings of dopamine neurons in this system have identified signals related to external reinforcement such as reward and punishment. However, other factors including locomotion, novelty, reward expectation, and internal state have also recently been shown to modulate dopamine neurons. This heterogeneity is at odds with typical modeling approaches in which these neurons are assumed to encode a global, scalar error signal. How is dopamine dependent plasticity coordinated in the presence of such heterogeneity? We develop a modeling approach that infers a pattern of dopamine activity sufficient to solve defined behavioral tasks, given architectural constraints informed by knowledge of mushroom body circuitry. Model dopamine neurons exhibit diverse tuning to task parameters while nonetheless producing coherent learned behaviors. Notably, reward prediction error emerges as a mode of population activity distributed across these neurons. Our results provide a mechanistic framework that accounts for the heterogeneity of dopamine activity during learning and behavior.

Identifiants

pubmed: 34375329
doi: 10.1371/journal.pcbi.1009205
pii: PCOMPBIOL-D-20-00986
pmc: PMC8354444
doi:

Substances chimiques

Dopamine VTD58H1Z2X

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1009205

Subventions

Organisme : NIBIB NIH HHS
ID : R01 EB029858
Pays : United States

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Linnie Jiang (L)

Mortimer B. Zuckerman Mind Brain Behavior Institute, Department of Neuroscience, Columbia University, New York, New York, United States of America.
Neurosciences Program, Stanford University, Stanford, California, United States of America.

Ashok Litwin-Kumar (A)

Mortimer B. Zuckerman Mind Brain Behavior Institute, Department of Neuroscience, Columbia University, New York, New York, United States of America.

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Classifications MeSH