Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents

Monique Ernst, Eric E. Nelson, Sandra Jazbec, Erin B. McClure, Christopher S. Monk, Ellen Leibenluft, Robert James Blair, Daniel S. Pine

Research output: Contribution to journalArticle

422 Citations (Scopus)

Abstract

Adolescents' propensity for risk-taking and reward-seeking behaviors suggests a heightened sensitivity for reward, reflected by greater feedback-related activity changes in reward circuitry (e.g., nucleus accumbens), and/or a lower sensitivity to potential harm reflected by weaker feedback-related activity changes in avoidance circuitry (e.g., amygdala) relative to adults. Responses of nucleus accumbens and amygdala to valenced outcomes (reward receipt and reward omission) were assayed using an event-related functional magnetic resonance imaging procedure paired with a monetary reward task in 14 adults and 16 adolescents. Bilateral amygdala and nucleus accumbens showed significantly greater activation when winning than when failing to win in both groups. Group comparisons revealed stronger activation of left nucleus accumbens by adolescents, and of left amygdala by adults. When examining responses to reward receipts and to reward omissions separately, the most robust group difference was within the amygdala during reward omission. The reduction of the fMRI BOLD signal in the amygdala in response to reward omission was larger for adults than for adolescents. Correlations showed a close link between negative emotion and amygdala decreased BOLD signal in adults, and between positive emotion and nucleus accumbens activation in adolescents. Overall, these findings support the notion that the signal differences between positive and negative outcomes involve the nucleus accumbens more in adolescents than in adults, and the amygdala more in adults than in adolescents. These developmental differences, if replicated, may have important implications for the development of early-onset disorders of emotion and motivation.

Original languageEnglish (US)
Pages (from-to)1279-1291
Number of pages13
JournalNeuroImage
Volume25
Issue number4
DOIs
StatePublished - May 1 2005

Fingerprint

Nucleus Accumbens
Amygdala
Reward
Emotions
Magnetic Resonance Imaging
Risk-Taking
Motivation

Keywords

  • Development
  • Limbic
  • Maturation
  • Neuroimaging
  • Pediatric
  • Reward
  • Ventral striatum
  • fMRI

ASJC Scopus subject areas

  • Neurology
  • Cognitive Neuroscience

Cite this

Ernst, M., Nelson, E. E., Jazbec, S., McClure, E. B., Monk, C. S., Leibenluft, E., ... Pine, D. S. (2005). Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents. NeuroImage, 25(4), 1279-1291. https://doi.org/10.1016/j.neuroimage.2004.12.038

Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents. / Ernst, Monique; Nelson, Eric E.; Jazbec, Sandra; McClure, Erin B.; Monk, Christopher S.; Leibenluft, Ellen; Blair, Robert James; Pine, Daniel S.

In: NeuroImage, Vol. 25, No. 4, 01.05.2005, p. 1279-1291.

Research output: Contribution to journalArticle

Ernst, M, Nelson, EE, Jazbec, S, McClure, EB, Monk, CS, Leibenluft, E, Blair, RJ & Pine, DS 2005, 'Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents', NeuroImage, vol. 25, no. 4, pp. 1279-1291. https://doi.org/10.1016/j.neuroimage.2004.12.038
Ernst, Monique ; Nelson, Eric E. ; Jazbec, Sandra ; McClure, Erin B. ; Monk, Christopher S. ; Leibenluft, Ellen ; Blair, Robert James ; Pine, Daniel S. / Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents. In: NeuroImage. 2005 ; Vol. 25, No. 4. pp. 1279-1291.
@article{8dbce44926b8492f9c75b73a05e54047,
title = "Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents",
abstract = "Adolescents' propensity for risk-taking and reward-seeking behaviors suggests a heightened sensitivity for reward, reflected by greater feedback-related activity changes in reward circuitry (e.g., nucleus accumbens), and/or a lower sensitivity to potential harm reflected by weaker feedback-related activity changes in avoidance circuitry (e.g., amygdala) relative to adults. Responses of nucleus accumbens and amygdala to valenced outcomes (reward receipt and reward omission) were assayed using an event-related functional magnetic resonance imaging procedure paired with a monetary reward task in 14 adults and 16 adolescents. Bilateral amygdala and nucleus accumbens showed significantly greater activation when winning than when failing to win in both groups. Group comparisons revealed stronger activation of left nucleus accumbens by adolescents, and of left amygdala by adults. When examining responses to reward receipts and to reward omissions separately, the most robust group difference was within the amygdala during reward omission. The reduction of the fMRI BOLD signal in the amygdala in response to reward omission was larger for adults than for adolescents. Correlations showed a close link between negative emotion and amygdala decreased BOLD signal in adults, and between positive emotion and nucleus accumbens activation in adolescents. Overall, these findings support the notion that the signal differences between positive and negative outcomes involve the nucleus accumbens more in adolescents than in adults, and the amygdala more in adults than in adolescents. These developmental differences, if replicated, may have important implications for the development of early-onset disorders of emotion and motivation.",
keywords = "Development, Limbic, Maturation, Neuroimaging, Pediatric, Reward, Ventral striatum, fMRI",
author = "Monique Ernst and Nelson, {Eric E.} and Sandra Jazbec and McClure, {Erin B.} and Monk, {Christopher S.} and Ellen Leibenluft and Blair, {Robert James} and Pine, {Daniel S.}",
year = "2005",
month = "5",
day = "1",
doi = "10.1016/j.neuroimage.2004.12.038",
language = "English (US)",
volume = "25",
pages = "1279--1291",
journal = "NeuroImage",
issn = "1053-8119",
publisher = "Academic Press Inc.",
number = "4",

}

TY - JOUR

T1 - Amygdala and nucleus accumbens in responses to receipt and omission of gains in adults and adolescents

AU - Ernst, Monique

AU - Nelson, Eric E.

AU - Jazbec, Sandra

AU - McClure, Erin B.

AU - Monk, Christopher S.

AU - Leibenluft, Ellen

AU - Blair, Robert James

AU - Pine, Daniel S.

PY - 2005/5/1

Y1 - 2005/5/1

N2 - Adolescents' propensity for risk-taking and reward-seeking behaviors suggests a heightened sensitivity for reward, reflected by greater feedback-related activity changes in reward circuitry (e.g., nucleus accumbens), and/or a lower sensitivity to potential harm reflected by weaker feedback-related activity changes in avoidance circuitry (e.g., amygdala) relative to adults. Responses of nucleus accumbens and amygdala to valenced outcomes (reward receipt and reward omission) were assayed using an event-related functional magnetic resonance imaging procedure paired with a monetary reward task in 14 adults and 16 adolescents. Bilateral amygdala and nucleus accumbens showed significantly greater activation when winning than when failing to win in both groups. Group comparisons revealed stronger activation of left nucleus accumbens by adolescents, and of left amygdala by adults. When examining responses to reward receipts and to reward omissions separately, the most robust group difference was within the amygdala during reward omission. The reduction of the fMRI BOLD signal in the amygdala in response to reward omission was larger for adults than for adolescents. Correlations showed a close link between negative emotion and amygdala decreased BOLD signal in adults, and between positive emotion and nucleus accumbens activation in adolescents. Overall, these findings support the notion that the signal differences between positive and negative outcomes involve the nucleus accumbens more in adolescents than in adults, and the amygdala more in adults than in adolescents. These developmental differences, if replicated, may have important implications for the development of early-onset disorders of emotion and motivation.

AB - Adolescents' propensity for risk-taking and reward-seeking behaviors suggests a heightened sensitivity for reward, reflected by greater feedback-related activity changes in reward circuitry (e.g., nucleus accumbens), and/or a lower sensitivity to potential harm reflected by weaker feedback-related activity changes in avoidance circuitry (e.g., amygdala) relative to adults. Responses of nucleus accumbens and amygdala to valenced outcomes (reward receipt and reward omission) were assayed using an event-related functional magnetic resonance imaging procedure paired with a monetary reward task in 14 adults and 16 adolescents. Bilateral amygdala and nucleus accumbens showed significantly greater activation when winning than when failing to win in both groups. Group comparisons revealed stronger activation of left nucleus accumbens by adolescents, and of left amygdala by adults. When examining responses to reward receipts and to reward omissions separately, the most robust group difference was within the amygdala during reward omission. The reduction of the fMRI BOLD signal in the amygdala in response to reward omission was larger for adults than for adolescents. Correlations showed a close link between negative emotion and amygdala decreased BOLD signal in adults, and between positive emotion and nucleus accumbens activation in adolescents. Overall, these findings support the notion that the signal differences between positive and negative outcomes involve the nucleus accumbens more in adolescents than in adults, and the amygdala more in adults than in adolescents. These developmental differences, if replicated, may have important implications for the development of early-onset disorders of emotion and motivation.

KW - Development

KW - Limbic

KW - Maturation

KW - Neuroimaging

KW - Pediatric

KW - Reward

KW - Ventral striatum

KW - fMRI

UR - http://www.scopus.com/inward/record.url?scp=17844403263&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=17844403263&partnerID=8YFLogxK

U2 - 10.1016/j.neuroimage.2004.12.038

DO - 10.1016/j.neuroimage.2004.12.038

M3 - Article

VL - 25

SP - 1279

EP - 1291

JO - NeuroImage

JF - NeuroImage

SN - 1053-8119

IS - 4

ER -