Lasting associations between early-childhood temperament and late-adolescent reward-circuitry response to peer feedback
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Behavioral inhibition, a temperament identifiable in infancy, is associated with heightened withdrawal from social encounters. Prior studies raise particular interest in the striatum, which responds uniquely to monetary gains in behaviorally inhibited children followed into adolescence. Although behavioral manifestations of inhibition are expressed primarily in the social domain, it remains unclear whether observed striatal alterations to monetary incentives also extend to social contexts. In the current study, imaging data were acquired from 39 participants (17 males, 22 females; ages 16-18 years) characterized since infancy on measures of behavioral inhibition. A social evaluation task was used to assess neural response to anticipation and receipt of positive and negative feedback from novel peers, classified by participants as being of high or low interest. As with monetary rewards, striatal response patterns differed during both anticipation and receipt of social reward between behaviorally inhibited and noninhibited adolescents. The current results, when combined with prior findings, suggest that early-life temperament predicts altered striatal response in both social and nonsocial contexts and provide support for continuity between temperament measured in early childhood and neural response to social signals measured in late adolescence and early adulthood.
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Adolescents who are affected by SAD or at risk for SAD exhibit heightened neural activation in appetitive-motivational systems.
“A growing empirical base has shown that adolescents who are affected by SAD or at risk for SAD exhibit heightened neural activation in appetitive-motivational systems (Bar-Haim et al., 2009, Guyer et al., 2014, Guyer et al., 2012a, Guyer et al., 2006, Haber and Knutson, 2010, Hardin et al., 2006, Helfinstein et al., 2011, Helfinstein et al., 2012, Lahat et al., 2012, Perez-Edgar et al., 2013).”
From Gaining insight into adolescent vulnerability for social anxiety from developmental cognitive neuroscience (2014) · cites this paper as Guyer et al., 2014
Behaviorally inhibited and socially anxious adolescents have elevated neural activation in networks that coordinate motivated behavior and reward processing.
“Recent data from several studies show that behaviorally inhibited and socially anxious adolescents also have elevated neural activation in networks that coordinate motivated behavior and reward processing (Bar-Haim et al., 2009, Guyer et al., 2014, Guyer et al., 2012a, Guyer et al., 2006, Haber and Knutson, 2010, Hardin et al., 2006, Helfinstein et al., 2011, Helfinstein et al., 2012, Lahat et al.”
From Gaining insight into adolescent vulnerability for social anxiety from developmental cognitive neuroscience (2014) · cites this paper as Guyer et al., 2014
The caudate's role in behaviorally inhibited adolescents shifts away from reward responsiveness.
“further implicating a shift in the caudate's role away from reward responsiveness (Guyer et al., 2014).”
From Gaining insight into adolescent vulnerability for social anxiety from developmental cognitive neuroscience (2014) · cites this paper as Guyer et al., 2014
Adolescents with but not without BI showed putamen hyperactivation during the anticipation of feedback in a social evaluation task.
“In this task, adolescents with but not without BI showed putamen hyperactivation during the anticipation of feedback”
From Gaining insight into adolescent vulnerability for social anxiety from developmental cognitive neuroscience (2014) · cites this paper as Guyer et al., 2014
Caudate hypoactivation after the receipt of rewarding feedback (peer acceptance) was observed in behaviorally inhibited relative to non-inhibited adolescents.
“Here, caudate hypoactivation after the receipt of rewarding feedback (peer acceptance) was observed in behaviorally inhibited relative to non-inhibited adolescents”
From Gaining insight into adolescent vulnerability for social anxiety from developmental cognitive neuroscience (2014) · cites this paper as Guyer et al., 2014
Adolescents (age 18) categorized across infancy and childhood as behaviorally inhibited showed heightened levels of striatal activation when anticipating being evaluated by a peer of interest, even in the absence of manifesting psychopathology.
“adolescents (age 18) categorized across infancy and childhood as behaviorally inhibited, a temperamental trait that increases risk for developing clinical levels of social anxiety and that has been established as a susceptibility factor (Aron et al., 2012), showed heightened levels of striatal activation when anticipating being evaluated by a peer of interest, even in the absence of manifesting ps”
From Adolescent neurobiological susceptibility to social context (2016) · cites this paper as Guyer et al., 2014
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Self-citationSpielberg, J. M., Jarcho, J. M., Dahl, R. E., Pine, D. S., Ernst, M., & Nelson, E. E. (2015) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsu165 · Cited by 52 · see citing works
Self-citationJarcho, J. M., Tanofsky-Kraff, M., Nelson, E. E., Engel, S. G., Vannucci, A., Field, S. E., Romer, A. L., Hannallah, L., Brady, S. M., Demidowich, A. P., et al. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2014.12.054 · Cited by 43 · see citing works
Self-citationFour Mechanistic Models of Peer Influence on Adolescent Cannabis Use
Caouette, J. D., & Feldstein Ewing, S. W. (2017) · Current Addiction Reports · doi:10.1007/s40429-017-0144-0 · Cited by 42 · see citing works
The endocannabinoid system in social anxiety disorder: from pathophysiology to novel therapeutics
Ahmed, M., Boileau, I., Le Foll, B., Carvalho, A. F., & Kloiber, S. (2022) · Brazilian Journal of Psychiatry · doi:10.1590/1516-4446-2021-1926 · Cited by 11 · see citing works
- Authors
- Guyer, A. E., Benson, B., Choate, V. R., Bar-Haim, Y., Perez-Edgar, K., Jarcho, J. M., Pine, D. S., Ernst, M., Fox, N. A., & Nelson, E. E.
- Affiliations
- University of California, Davis (US)
- National Institute of Mental Health (US)
- University of Massachusetts Boston (US)
- University of Maryland, College Park (US)
- Corresponding author
- Guyer, Amanda E.
- Venue
- Development and Psychopathology
- Publisher
- Cambridge University Press (CUP)
- Published
- 2014-01-21
- Volume
- 26
- Issue
- 1
- Pages
- 229-243
- ISSN
- 0954-5794 (ISSN-L)
- 1469-2198
- PMC
- PMC4096565
- OpenAlex
- W2127515327
- Cited by
- 109
- References
- 88
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 3 · 2023: 4 · 2022: 8 · 2021: 9 · 2020: 5 · 2019: 30 · 2018: 7 · 2017: 8 · 2016: 9 · 2015: 7 · 2014: 9 · 2013: 3
- FWCI
- 6.13
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Development and Psychopathology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute of Mental Health (MH074454, MH080076, R00MH080076, U01MH074454, R01MH094633, R01MH074454)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Social Sciences › Psychology › Clinical Psychology › Child and Adolescent Psychosocial and Emotional Development
- Keywords
- behavioral inhibition, temperament, social reward, striatum, peer feedback, social evaluation, adolescent development, monetary rewards
- MeSH terms
- Adolescent, Brain, Child, Child, Preschool, Female, Humans, Image Processing, Computer-Assisted, Infant, Inhibition, Psychological, Interpersonal Relations, Magnetic Resonance Imaging, Male, Peer Group, Reward, Social Perception, Temperament, Functional Neuroimaging
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