Pattern of dopamine signaling during aversive events predicts active avoidance learning

Learning to avoid aversive outcomes is an adaptive strategy to limit one’s future exposure to stressful events. However, there is considerable variance in active avoidance learning across a population. The mesolimbic dopamine system contributes to behaviors elicited by aversive stimuli, although it...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 116; no. 27; pp. 13641 - 13650
Main Authors Stelly, Claire E., Haug, Graham C., Fonzi, Kaitlyn M., Garcia, Miriam A., Tritley, Sean C., Magnon, Alexa P., Ramos, Maria Alicia P., Wanat, Matthew J.
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 02.07.2019
SeriesPNAS Plus
Subjects
Animals
Avoidance Learning - physiology
Biological Sciences
Corpus Striatum - physiology
Cues
Dopamine - physiology
Electroshock
Male
PNAS Plus
Rats
Rats, Sprague-Dawley
Signal Transduction - physiology
active avoidance
dopamine
learning
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Summary:Learning to avoid aversive outcomes is an adaptive strategy to limit one’s future exposure to stressful events. However, there is considerable variance in active avoidance learning across a population. The mesolimbic dopamine system contributes to behaviors elicited by aversive stimuli, although it is unclear if the heterogeneity in active avoidance learning is explained by differences in dopamine transmission. Furthermore, it is not known how dopamine signals evolve throughout active avoidance learning. To address these questions, we performed voltammetry recordings of dopamine release in the ventral medial striatum throughout training on inescapable footshock and signaled active avoidance tasks. This approach revealed differences in the pattern of dopamine signaling during the aversive cue and the safety period that corresponded to subsequent task performance. Dopamine transmission throughout the footshock bout did not predict performance but rather was modulated by the prior stress exposure. Additionally, we demonstrate that dopamine encodes a safety prediction error signal, which illustrates that ventral medial striatal dopamine release conveys a learning signal during both appetitive and aversive conditions.
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Author contributions: C.E.S. and M.J.W. designed research; C.E.S., G.C.H., and K.M.F. performed research; C.E.S., G.C.H., K.M.F., M.A.G., S.C.T., A.P.M., M.A.P.R., and M.J.W. analyzed data; and C.E.S. and M.J.W. wrote the paper.
Edited by Susan G. Amara, NIH, Bethesda, MD, and approved May 28, 2019 (received for review March 12, 2019)
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.1904249116