Dysfunctional social reinforcement processing in disruptive behavior disorders: An functional magnetic resonance imaging study

Soonjo Hwang, Harma Meffert, Michelle R. Van Tieghem, Stephen Sinclair, Susan Y. Bookheimer, Brigette Vaughan, Robert James Blair

Research output: Contribution to journalArticle

Abstract

Objective: Prior functional magnetic resonance imaging (fMRI) work has revealed that children/adolescents with disruptive behavior disorders (DBDs) show dysfunctional reward/non-reward processing of non-social reinforcements in the context of instrumental learning tasks. Neural responsiveness to social reinforcements during instrumental learning, despite the importance of this for socialization, has not yet been previously investigated. Methods: Twenty-nine healthy children/adolescents and 19 children/adolescents with DBDs performed the fMRI social/ non-social reinforcement learning task. Participants responded to random fractal image stimuli and received social and non-social rewards/non-rewards according to their accuracy. Results: Children/adolescents with DBDs showed significantly reduced responses within the caudate and posterior cingulate cortex (PCC) to non-social (financial) rewards and social non-rewards (the distress of others). Connectivity analyses revealed that children/adolescents with DBDs have decreased positive functional connectivity between the ventral striatum (VST) and the ventromedial prefrontal cortex (vmPFC) seeds and the lateral frontal cortex in response to reward relative to non-reward, irrespective of its sociality. In addition, they showed decreased positive connectivity between the vmPFC seed and the amygdala in response to non-reward relative to reward. Conclusion: These data indicate compromised reinforcement processing of both non-social rewards and social non-rewards in children/adolescents with DBDs within core regions for instrumental learning and reinforcement-based decision-making (caudate and PCC). In addition, children/adolescents with DBDs show dysfunctional interactions between the VST, vmPFC, and lateral frontal cortex in response to rewarded instrumental actions potentially reflecting disruptions in attention to rewarded stimuli.

Original languageEnglish (US)
Pages (from-to)449-460
Number of pages12
JournalClinical Psychopharmacology and Neuroscience
Volume16
Issue number4
DOIs
StatePublished - Nov 2018

Fingerprint

Social Reinforcement
Attention Deficit and Disruptive Behavior Disorders
Reward
Magnetic Resonance Imaging
Operant Conditioning
Prefrontal Cortex
Gyrus Cinguli
Frontal Lobe
Seeds
Fractals
Socialization
Amygdala
Decision Making
Learning
Reinforcement (Psychology)

Keywords

  • Caudate
  • Disruptive behavior disorder
  • Posterior cingulate cortex
  • Social reward
  • Ventral striatum
  • Ventro-medial prefrontal cortex.

ASJC Scopus subject areas

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

Cite this

Dysfunctional social reinforcement processing in disruptive behavior disorders : An functional magnetic resonance imaging study. / Hwang, Soonjo; Meffert, Harma; Van Tieghem, Michelle R.; Sinclair, Stephen; Bookheimer, Susan Y.; Vaughan, Brigette; Blair, Robert James.

In: Clinical Psychopharmacology and Neuroscience, Vol. 16, No. 4, 11.2018, p. 449-460.

Research output: Contribution to journalArticle

@article{dcb0f7d0e66c44b7b38cb11bad72a4b6,
title = "Dysfunctional social reinforcement processing in disruptive behavior disorders: An functional magnetic resonance imaging study",
abstract = "Objective: Prior functional magnetic resonance imaging (fMRI) work has revealed that children/adolescents with disruptive behavior disorders (DBDs) show dysfunctional reward/non-reward processing of non-social reinforcements in the context of instrumental learning tasks. Neural responsiveness to social reinforcements during instrumental learning, despite the importance of this for socialization, has not yet been previously investigated. Methods: Twenty-nine healthy children/adolescents and 19 children/adolescents with DBDs performed the fMRI social/ non-social reinforcement learning task. Participants responded to random fractal image stimuli and received social and non-social rewards/non-rewards according to their accuracy. Results: Children/adolescents with DBDs showed significantly reduced responses within the caudate and posterior cingulate cortex (PCC) to non-social (financial) rewards and social non-rewards (the distress of others). Connectivity analyses revealed that children/adolescents with DBDs have decreased positive functional connectivity between the ventral striatum (VST) and the ventromedial prefrontal cortex (vmPFC) seeds and the lateral frontal cortex in response to reward relative to non-reward, irrespective of its sociality. In addition, they showed decreased positive connectivity between the vmPFC seed and the amygdala in response to non-reward relative to reward. Conclusion: These data indicate compromised reinforcement processing of both non-social rewards and social non-rewards in children/adolescents with DBDs within core regions for instrumental learning and reinforcement-based decision-making (caudate and PCC). In addition, children/adolescents with DBDs show dysfunctional interactions between the VST, vmPFC, and lateral frontal cortex in response to rewarded instrumental actions potentially reflecting disruptions in attention to rewarded stimuli.",
keywords = "Caudate, Disruptive behavior disorder, Posterior cingulate cortex, Social reward, Ventral striatum, Ventro-medial prefrontal cortex.",
author = "Soonjo Hwang and Harma Meffert and {Van Tieghem}, {Michelle R.} and Stephen Sinclair and Bookheimer, {Susan Y.} and Brigette Vaughan and Blair, {Robert James}",
year = "2018",
month = "11",
doi = "10.9758/cpn.2018.16.1.449",
language = "English (US)",
volume = "16",
pages = "449--460",
journal = "Clinical Psychopharmacology and Neuroscience",
issn = "1738-1088",
publisher = "Korean College of Neuropsychopharmacology",
number = "4",

}

TY - JOUR

T1 - Dysfunctional social reinforcement processing in disruptive behavior disorders

T2 - An functional magnetic resonance imaging study

AU - Hwang, Soonjo

AU - Meffert, Harma

AU - Van Tieghem, Michelle R.

AU - Sinclair, Stephen

AU - Bookheimer, Susan Y.

AU - Vaughan, Brigette

AU - Blair, Robert James

PY - 2018/11

Y1 - 2018/11

N2 - Objective: Prior functional magnetic resonance imaging (fMRI) work has revealed that children/adolescents with disruptive behavior disorders (DBDs) show dysfunctional reward/non-reward processing of non-social reinforcements in the context of instrumental learning tasks. Neural responsiveness to social reinforcements during instrumental learning, despite the importance of this for socialization, has not yet been previously investigated. Methods: Twenty-nine healthy children/adolescents and 19 children/adolescents with DBDs performed the fMRI social/ non-social reinforcement learning task. Participants responded to random fractal image stimuli and received social and non-social rewards/non-rewards according to their accuracy. Results: Children/adolescents with DBDs showed significantly reduced responses within the caudate and posterior cingulate cortex (PCC) to non-social (financial) rewards and social non-rewards (the distress of others). Connectivity analyses revealed that children/adolescents with DBDs have decreased positive functional connectivity between the ventral striatum (VST) and the ventromedial prefrontal cortex (vmPFC) seeds and the lateral frontal cortex in response to reward relative to non-reward, irrespective of its sociality. In addition, they showed decreased positive connectivity between the vmPFC seed and the amygdala in response to non-reward relative to reward. Conclusion: These data indicate compromised reinforcement processing of both non-social rewards and social non-rewards in children/adolescents with DBDs within core regions for instrumental learning and reinforcement-based decision-making (caudate and PCC). In addition, children/adolescents with DBDs show dysfunctional interactions between the VST, vmPFC, and lateral frontal cortex in response to rewarded instrumental actions potentially reflecting disruptions in attention to rewarded stimuli.

AB - Objective: Prior functional magnetic resonance imaging (fMRI) work has revealed that children/adolescents with disruptive behavior disorders (DBDs) show dysfunctional reward/non-reward processing of non-social reinforcements in the context of instrumental learning tasks. Neural responsiveness to social reinforcements during instrumental learning, despite the importance of this for socialization, has not yet been previously investigated. Methods: Twenty-nine healthy children/adolescents and 19 children/adolescents with DBDs performed the fMRI social/ non-social reinforcement learning task. Participants responded to random fractal image stimuli and received social and non-social rewards/non-rewards according to their accuracy. Results: Children/adolescents with DBDs showed significantly reduced responses within the caudate and posterior cingulate cortex (PCC) to non-social (financial) rewards and social non-rewards (the distress of others). Connectivity analyses revealed that children/adolescents with DBDs have decreased positive functional connectivity between the ventral striatum (VST) and the ventromedial prefrontal cortex (vmPFC) seeds and the lateral frontal cortex in response to reward relative to non-reward, irrespective of its sociality. In addition, they showed decreased positive connectivity between the vmPFC seed and the amygdala in response to non-reward relative to reward. Conclusion: These data indicate compromised reinforcement processing of both non-social rewards and social non-rewards in children/adolescents with DBDs within core regions for instrumental learning and reinforcement-based decision-making (caudate and PCC). In addition, children/adolescents with DBDs show dysfunctional interactions between the VST, vmPFC, and lateral frontal cortex in response to rewarded instrumental actions potentially reflecting disruptions in attention to rewarded stimuli.

KW - Caudate

KW - Disruptive behavior disorder

KW - Posterior cingulate cortex

KW - Social reward

KW - Ventral striatum

KW - Ventro-medial prefrontal cortex.

UR - http://www.scopus.com/inward/record.url?scp=85055857189&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85055857189&partnerID=8YFLogxK

U2 - 10.9758/cpn.2018.16.1.449

DO - 10.9758/cpn.2018.16.1.449

M3 - Article

AN - SCOPUS:85055857189

VL - 16

SP - 449

EP - 460

JO - Clinical Psychopharmacology and Neuroscience

JF - Clinical Psychopharmacology and Neuroscience

SN - 1738-1088

IS - 4

ER -