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Nucleus accumbens, thalamus and insula connectivity during incentive anticipation in typical adults and adolescents

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Cho, Youngsun T., Fromm, Stephen, Guyer, Amanda E., Detloff, Allison, Pine, Daniel S., Fudge, Julie L., Ernst, Monique·2013·NeuroImage

DOI 10.1016/j.neuroimage.2012.10.013PMC PMC3949208

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Abstract

Reward neurocircuitry links motivation with complex behavioral responses. Studies of incentive processing have repeatedly demonstrated activation of nucleus accumbens (NAc), thalamus, and anterior insula, three key components of reward neurocircuitry. The contribution of the thalamus to this circuitry in humans has been relatively ignored, a gap that needs to be filled, given the central role of this structure in processing and filtering information. This study aimed to understand how these three regions function as a network during gain or loss anticipation in adults and youth. Towards this goal, functional magnetic resonance imaging (fMRI) and dynamic causal modeling (DCM) were used to examine effective connectivity among these three nodes in healthy adults and adolescents who performed the monetary incentive delay (MID) task. Seven connectivity models, based on anatomic connections, were tested. They were estimated for incentive anticipation and underwent Bayesian Model Selection (BMS) to determine the best-fit model for each adult and adolescent group. Connection strengths were extracted from the best-fit model and examined for significance in each group. These variables were then entered into a linear mixed model to test between-group effects on effective connectivity in reward neurocircuitry. The best-fit model for both groups included all possible anatomic connections. Three main findings emerged: (1) Across the task, thalamus and insula significantly influenced NAc; (2) A broader set of significant connections was found for the loss-cue condition than the gain-cue condition in both groups; (3) Finally, between-group comparisons of connectivity strength failed to detect statistical differences, suggesting that adults and adolescents use this incentive-processing network in a similar manner. This study demonstrates the way in which the thalamus and insula influence the NAc during incentive processing in humans. Specifically, this is the first study to demonstrate in humans the key role of thalamus projections onto the NAc in support of reward processing. Our results suggest that anticipation of gain/loss involves an 'alerting' signal (thalamus) that converges with interoceptive information (insula) to shape action selection programs in the ventral striatum.

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Authors: Cho, Y. T., Fromm, S., Guyer, A. E., Detloff, A., Pine, D. S., Fudge, J. L., & Ernst, M.
Affiliations: University of Rochester Medicine (US)
United States Department of Health and Human Services (US)
University of California, Davis (US)
ORCID: Cho, Youngsun T.
Guyer, Amanda E.
Pine, Daniel S.
Fudge, Julie L.
Venue: NeuroImage
Publisher: Elsevier BV
Published: 2013-02
Volume: 66
Pages: 508-521
ISSN: 1053-8119 (ISSN-L)
DOI: 10.1016/j.neuroimage.2012.10.013
PMC: PMC3949208
OpenAlex: W2002598673
Semantic Scholar: a82dc97e82fae7172c54dbb31e757f42201d9085
Cited by: 173
References: 99
Citations by year: 2026: 6 · 2025: 7 · 2024: 7 · 2023: 12 · 2022: 16 · 2021: 13 · 2020: 8 · 2019: 13 · 2018: 23 · 2017: 12 · 2016: 14 · 2015: 17 · 2014: 16 · 2013: 8
FWCI: 6.70
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: NeuroImage (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (5f30mh091926-02)
National Institute of Mental Health (F30 MH091926-02, F30 MH091926)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: nucleus accumbens, thalamus, anterior insula, reward processing, effective connectivity, monetary incentive delay task, adolescents, adults, loss anticipation, interoception, action selection, ventral striatum
MeSH terms: Adolescent, Adult, Brain Mapping, Cerebral Cortex, Cues, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Middle Aged, Neural Pathways, Nucleus Accumbens, Reward, Thalamus, Young Adult, Anticipation, Psychological

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Nucleus accumbens, thalamus and insula connectivity during incentive anticipation in typical adults and adolescents

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