Neurodevelopmental changes in social reinforcement processing: A functional magnetic resonance imaging study

Soonjo Hwang, Harma Meffert, Michelle R. VanTieghem, Stuart F White, Stephen Sinclair, Susan Y. Bookheimer, Robert James Blair

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Objective: In the current study we investigated neurodevelopmental changes in response to social and non-social reinforcement. Methods: Fifty-three healthy participants including 16 early adolescents (age, 10-15 years), 16 late adolescents (age, 15-18 years), and 21 young adults (age, 21-25 years) completed a social/non-social reward learning task while undergoing functional magnetic resonance imaging. Participants responded to fractal image stimuli and received social or non-social reward/non-rewards according to their accuracy. ANOVAs were conducted on both the blood oxygen level dependent response data and the product of a context-dependent psychophysiological interaction (gPPI) analysis involving ventromedial prefrontal cortex (vmPFC) and bilateral insula cortices as seed regions. Results: Early adolescents showed significantly increased activation in the amygdala and anterior insula cortex in response to non-social monetary rewards relative to both social reward/non-reward and monetary non-rewards compared to late adolescents and young adults. In addition, early adolescents showed significantly more positive connectivity between the vmPFC/bilateral insula cortices seeds and other regions implicated in reinforcement processing (the amygdala, posterior cingulate cortex, insula cortex, and lentiform nucleus) in response to non-reward and especially social non-reward, compared to late adolescents and young adults. Conclusion: It appears that early adolescence may be marked by: (i) a selective increase in responsiveness to non-social, relative to social, rewards; and (ii) enhanced, integrated functioning of reinforcement circuitry for non-reward, and in particular, with respect to posterior cingulate and insula cortices, for social non-reward.

Original languageEnglish (US)
Pages (from-to)369-381
Number of pages13
JournalClinical Psychopharmacology and Neuroscience
Volume15
Issue number4
DOIs
StatePublished - Jan 1 2017

Fingerprint

Social Reinforcement
Magnetic Resonance Imaging
Reward
Young Adult
Gyrus Cinguli
Amygdala
Prefrontal Cortex
Seeds
Corpus Striatum
Fractals
Analysis of Variance
Healthy Volunteers
Learning
Oxygen

Keywords

  • Amygdala
  • Anterior insula
  • Context-dependent psychophysiological interaction
  • Functional magnetic resonance imaging
  • Social reward
  • Ventro-medial prefrontal cortex

ASJC Scopus subject areas

  • Psychiatry and Mental health
  • Behavioral Neuroscience
  • Pharmacology (medical)

Cite this

Neurodevelopmental changes in social reinforcement processing : A functional magnetic resonance imaging study. / Hwang, Soonjo; Meffert, Harma; VanTieghem, Michelle R.; White, Stuart F; Sinclair, Stephen; Bookheimer, Susan Y.; Blair, Robert James.

In: Clinical Psychopharmacology and Neuroscience, Vol. 15, No. 4, 01.01.2017, p. 369-381.

Research output: Contribution to journalArticle

@article{906896cb311e49b8829260daa24eab4f,
title = "Neurodevelopmental changes in social reinforcement processing: A functional magnetic resonance imaging study",
abstract = "Objective: In the current study we investigated neurodevelopmental changes in response to social and non-social reinforcement. Methods: Fifty-three healthy participants including 16 early adolescents (age, 10-15 years), 16 late adolescents (age, 15-18 years), and 21 young adults (age, 21-25 years) completed a social/non-social reward learning task while undergoing functional magnetic resonance imaging. Participants responded to fractal image stimuli and received social or non-social reward/non-rewards according to their accuracy. ANOVAs were conducted on both the blood oxygen level dependent response data and the product of a context-dependent psychophysiological interaction (gPPI) analysis involving ventromedial prefrontal cortex (vmPFC) and bilateral insula cortices as seed regions. Results: Early adolescents showed significantly increased activation in the amygdala and anterior insula cortex in response to non-social monetary rewards relative to both social reward/non-reward and monetary non-rewards compared to late adolescents and young adults. In addition, early adolescents showed significantly more positive connectivity between the vmPFC/bilateral insula cortices seeds and other regions implicated in reinforcement processing (the amygdala, posterior cingulate cortex, insula cortex, and lentiform nucleus) in response to non-reward and especially social non-reward, compared to late adolescents and young adults. Conclusion: It appears that early adolescence may be marked by: (i) a selective increase in responsiveness to non-social, relative to social, rewards; and (ii) enhanced, integrated functioning of reinforcement circuitry for non-reward, and in particular, with respect to posterior cingulate and insula cortices, for social non-reward.",
keywords = "Amygdala, Anterior insula, Context-dependent psychophysiological interaction, Functional magnetic resonance imaging, Social reward, Ventro-medial prefrontal cortex",
author = "Soonjo Hwang and Harma Meffert and VanTieghem, {Michelle R.} and White, {Stuart F} and Stephen Sinclair and Bookheimer, {Susan Y.} and Blair, {Robert James}",
year = "2017",
month = "1",
day = "1",
doi = "10.9758/cpn.2017.15.4.369",
language = "English (US)",
volume = "15",
pages = "369--381",
journal = "Clinical Psychopharmacology and Neuroscience",
issn = "1738-1088",
publisher = "Korean College of Neuropsychopharmacology",
number = "4",

}

TY - JOUR

T1 - Neurodevelopmental changes in social reinforcement processing

T2 - A functional magnetic resonance imaging study

AU - Hwang, Soonjo

AU - Meffert, Harma

AU - VanTieghem, Michelle R.

AU - White, Stuart F

AU - Sinclair, Stephen

AU - Bookheimer, Susan Y.

AU - Blair, Robert James

PY - 2017/1/1

Y1 - 2017/1/1

N2 - Objective: In the current study we investigated neurodevelopmental changes in response to social and non-social reinforcement. Methods: Fifty-three healthy participants including 16 early adolescents (age, 10-15 years), 16 late adolescents (age, 15-18 years), and 21 young adults (age, 21-25 years) completed a social/non-social reward learning task while undergoing functional magnetic resonance imaging. Participants responded to fractal image stimuli and received social or non-social reward/non-rewards according to their accuracy. ANOVAs were conducted on both the blood oxygen level dependent response data and the product of a context-dependent psychophysiological interaction (gPPI) analysis involving ventromedial prefrontal cortex (vmPFC) and bilateral insula cortices as seed regions. Results: Early adolescents showed significantly increased activation in the amygdala and anterior insula cortex in response to non-social monetary rewards relative to both social reward/non-reward and monetary non-rewards compared to late adolescents and young adults. In addition, early adolescents showed significantly more positive connectivity between the vmPFC/bilateral insula cortices seeds and other regions implicated in reinforcement processing (the amygdala, posterior cingulate cortex, insula cortex, and lentiform nucleus) in response to non-reward and especially social non-reward, compared to late adolescents and young adults. Conclusion: It appears that early adolescence may be marked by: (i) a selective increase in responsiveness to non-social, relative to social, rewards; and (ii) enhanced, integrated functioning of reinforcement circuitry for non-reward, and in particular, with respect to posterior cingulate and insula cortices, for social non-reward.

AB - Objective: In the current study we investigated neurodevelopmental changes in response to social and non-social reinforcement. Methods: Fifty-three healthy participants including 16 early adolescents (age, 10-15 years), 16 late adolescents (age, 15-18 years), and 21 young adults (age, 21-25 years) completed a social/non-social reward learning task while undergoing functional magnetic resonance imaging. Participants responded to fractal image stimuli and received social or non-social reward/non-rewards according to their accuracy. ANOVAs were conducted on both the blood oxygen level dependent response data and the product of a context-dependent psychophysiological interaction (gPPI) analysis involving ventromedial prefrontal cortex (vmPFC) and bilateral insula cortices as seed regions. Results: Early adolescents showed significantly increased activation in the amygdala and anterior insula cortex in response to non-social monetary rewards relative to both social reward/non-reward and monetary non-rewards compared to late adolescents and young adults. In addition, early adolescents showed significantly more positive connectivity between the vmPFC/bilateral insula cortices seeds and other regions implicated in reinforcement processing (the amygdala, posterior cingulate cortex, insula cortex, and lentiform nucleus) in response to non-reward and especially social non-reward, compared to late adolescents and young adults. Conclusion: It appears that early adolescence may be marked by: (i) a selective increase in responsiveness to non-social, relative to social, rewards; and (ii) enhanced, integrated functioning of reinforcement circuitry for non-reward, and in particular, with respect to posterior cingulate and insula cortices, for social non-reward.

KW - Amygdala

KW - Anterior insula

KW - Context-dependent psychophysiological interaction

KW - Functional magnetic resonance imaging

KW - Social reward

KW - Ventro-medial prefrontal cortex

UR - http://www.scopus.com/inward/record.url?scp=85032722348&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85032722348&partnerID=8YFLogxK

U2 - 10.9758/cpn.2017.15.4.369

DO - 10.9758/cpn.2017.15.4.369

M3 - Article

C2 - 29073749

AN - SCOPUS:85032722348

VL - 15

SP - 369

EP - 381

JO - Clinical Psychopharmacology and Neuroscience

JF - Clinical Psychopharmacology and Neuroscience

SN - 1738-1088

IS - 4

ER -