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Striatal and septo-hypothalamic responses to anticipation and outcome of affiliative rewards

Research output: Contribution to journalArticlepeer-review

Tiago Bortolini, Bruno Melo, Rodrigo Basilio, Ronald Fischer, Roland Zahn, Ricardo de Oliveira-Souza, Brian Knutson, Jorge Moll

Original languageEnglish
Article number118474
Pages (from-to)118474
JournalNeuroImage
Volume243
Early online date15 Aug 2021
DOIs
E-pub ahead of print15 Aug 2021
PublishedNov 2021

Bibliographical note

Funding Information: This work was supported by grants from FAPERJ [E-26/ 202.962/2015; E-26/201.941/2020], the National Council of Technological and Scientific Development (465346/2014-6; 434517/2018-6; 313141/2018-5), and intramural grants from the D'Or Institute for Research and Education (IDOR). The funding sources were not involved in the study design, the collection, analysis, and interpretation of data, in the writing of the report, and in the decision to submit the article for publication. We thank Kelly MacNiven for her generous help sharing scripts and advice with analysis. Publisher Copyright: © 2021 Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

King's Authors

Abstract

Humans are intrinsically motivated to bond with others. The ability to experience affiliative emotions (such as affection/tenderness, sexual attraction, and admiration/awe) may incentivize and promote these affiliative bonds. Here, we interrogate the role of the critical reward circuitry, especially the Nucleus Accumbens (NAcc) and the septo-hypothalamic region, in the anticipation of and response to affiliative rewards using a novel incentive delay task. During Functional Magnetic Resonance Imaging (FMRI), participants (n=23 healthy humans; 14 female) anticipated and watched videos involving affiliative (tenderness, erotic desire, and awe) and nonaffiliative (i.e., food) rewards, as well as neutral scenes. On the one hand, anticipation of both affiliative and nonaffiliative rewards increased activity in the NAcc, anterior insula, and supplementary motor cortex, but activity in the amygdala and the ventromedial prefrontal cortex (vmPFC) increased in response to reward outcomes. On the other hand, affiliative rewards more specifically increased activity in the septo-hypothalamic area. Moreover, NAcc activity during anticipation correlated with positive arousal for all rewards, whereas septo-hypothalamic activity during the outcome correlated with positive arousal and motivation for subsequent re-exposure only for affiliative rewards. Together, these findings implicate a general appetitive response in the NAcc to different types of rewards but suggests a more specific response in the septo-hypothalamic region in response to affiliative rewards outcomes. This work also presents a new task for distinguishing between neural responses to affiliative and non-affiliative rewards.

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