Nature of functional links in valuation networks differentiates impulsive behaviors between abstinent heroin-dependent subjects and nondrug-using subjects
Advanced neuroimaging studies have identified brain correlates of pathological impulsivity in a variety of neuropsychiatric disorders. However, whether and how these spatially separate and functionally integrated neural correlates collectively contribute to aberrant impulsive behaviors remains uncle...
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| Published in | NeuroImage (Orlando, Fla.) Vol. 115; pp. 76 - 84 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
15.07.2015
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| Subjects | |
| Online Access | Get full text |
| ISSN | 1053-8119 1095-9572 1095-9572 |
| DOI | 10.1016/j.neuroimage.2015.04.060 |
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| Abstract | Advanced neuroimaging studies have identified brain correlates of pathological impulsivity in a variety of neuropsychiatric disorders. However, whether and how these spatially separate and functionally integrated neural correlates collectively contribute to aberrant impulsive behaviors remains unclear. Building on recent progress in neuroeconomics toward determining a biological account of human behaviors, we employed resting-state functional MRI to characterize the nature of the links between these neural correlates and to investigate their impact on impulsivity. We demonstrated that through functional connectivity with the ventral medial prefrontal cortex, the δ-network (regions of the executive control system, such as the dorsolateral prefrontal cortex) and the β-network (regions of the reward system involved in the mesocorticolimbic pathway), jointly influence impulsivity measured by the Barratt impulsiveness scale scores. In control nondrug-using subjects, the functional link between the β- and δ-networks is balanced, and the δ-network competitively controls impulsivity. However, in abstinent heroin-dependent subjects, the link is imbalanced, with stronger β-network connectivity and weaker δ-network connectivity. The imbalanced link is associated with impulsivity, indicating that the β- and δ-networks may mutually reinforce each other in abstinent heroin-dependent subjects. These findings of an aberrant link between the β- and δ-networks in abstinent heroin-dependent subjects may shed light on the mechanism of aberrant behaviors of drug addiction and may serve as an endophenotype to mark individual subjects' self-control capacity.
•We characterized the nature of functional links between valuation networks.•With the functional links to vmPFC, δ and β networks were found jointly influence the impulsivity.•The δ and β networks were balanced and competitively control impulsivity in CN group.•The δ and β networks were imbalanced and mutually reinforce impulsivity in HD group.•This altered δ–β relationship could serve as an endophenotype of aberrant behaviors. |
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| AbstractList | Advanced neuroimaging studies have identified brain correlates of pathological impulsivity in a variety of neuropsychiatric disorders. However, whether and how these spatially separate and functionally integrated neural correlates collectively contribute to aberrant impulsive behaviors remains unclear. Building on recent progress in neuroeconomics toward determining a biological account of human behaviors, we employed resting-state functional MRI to characterize the nature of the links between these neural correlates and to investigate their impact on impulsivity. We demonstrated that through functional connectivity with the ventral medial prefrontal cortex, the delta -network (regions of the executive control system, such as the dorsolateral prefrontal cortex) and the beta -network (regions of the reward system involved in the mesocorticolimbic pathway), jointly influence impulsivity measured by the Barratt impulsiveness scale scores. In control nondrug-using subjects, the functional link between the beta - and delta -networks is balanced, and the delta -network competitively controls impulsivity. However, in abstinent heroin-dependent subjects, the link is imbalanced, with stronger beta -network connectivity and weaker delta -network connectivity. The imbalanced link is associated with impulsivity, indicating that the beta - and delta -networks may mutually reinforce each other in abstinent heroin-dependent subjects. These findings of an aberrant link between the beta - and delta -networks in abstinent heroin-dependent subjects may shed light on the mechanism of aberrant behaviors of drug addiction and may serve as an endophenotype to mark individual subjects' self-control capacity. Advanced neuroimaging studies have identified brain correlates of pathological impulsivity in a variety of neuropsychiatric disorders. However, whether and how these spatially separate and functionally integrated neural correlates collectively contribute to aberrant impulsive behaviors remains unclear. Building on recent progress in neuroeconomics toward determining a biological account of human behaviors, we employed resting-state functional MRI to characterize the nature of the links between these neural correlates and to investigate their impact on impulsivity. We demonstrated that through functional connectivity with the ventral medial prefrontal cortex, the δ-network (regions of the executive control system, such as the dorsolateral prefrontal cortex) and the β-network (regions of the reward system involved in the mesocorticolimbic pathway), jointly influence impulsivity measured by the Barratt impulsiveness scale scores. In control nondrug-using subjects, the functional link between the β- and δ-networks is balanced, and the δ-network competitively controls impulsivity. However, in abstinent heroin-dependent subjects, the link is imbalanced, with stronger β-network connectivity and weaker δ-network connectivity. The imbalanced link is associated with impulsivity, indicating that the β- and δ-networks may mutually reinforce each other in abstinent heroin-dependent subjects. These findings of an aberrant link between the β- and δ-networks in abstinent heroin-dependent subjects may shed light on the mechanism of aberrant behaviors of drug addiction and may serve as an endophenotype to mark individual subjects' self-control capacity. Advanced neuroimaging studies have identified brain correlates of pathological impulsivity in a variety of neuropsychiatric disorders. However, whether and how these spatially separate and functionally integrated neural correlates collectively contribute to aberrant impulsive behaviors remains unclear. Building on recent progress in neuroeconomics toward determining a biological account of human behaviors, we employed resting-state functional MRI to characterize the nature of the links between these neural correlates and to investigate their impact on impulsivity. We demonstrated that through functional connectivity with the ventral medial prefrontal cortex, the δ-network (regions of the executive control system, such as the dorsolateral prefrontal cortex) and the β-network (regions of the reward system involved in the mesocorticolimbic pathway), jointly influence impulsivity measured by the Barratt impulsiveness scale scores. In control nondrug-using subjects, the functional link between the β- and δ-networks is balanced, and the δ-network competitively controls impulsivity. However, in abstinent heroin-dependent subjects, the link is imbalanced, with stronger β-network connectivity and weaker δ-network connectivity. The imbalanced link is associated with impulsivity, indicating that the β- and δ-networks may mutually reinforce each other in abstinent heroin-dependent subjects. These findings of an aberrant link between the β- and δ-networks in abstinent heroin-dependent subjects may shed light on the mechanism of aberrant behaviors of drug addiction and may serve as an endophenotype to mark individual subjects' self-control capacity.Advanced neuroimaging studies have identified brain correlates of pathological impulsivity in a variety of neuropsychiatric disorders. However, whether and how these spatially separate and functionally integrated neural correlates collectively contribute to aberrant impulsive behaviors remains unclear. Building on recent progress in neuroeconomics toward determining a biological account of human behaviors, we employed resting-state functional MRI to characterize the nature of the links between these neural correlates and to investigate their impact on impulsivity. We demonstrated that through functional connectivity with the ventral medial prefrontal cortex, the δ-network (regions of the executive control system, such as the dorsolateral prefrontal cortex) and the β-network (regions of the reward system involved in the mesocorticolimbic pathway), jointly influence impulsivity measured by the Barratt impulsiveness scale scores. In control nondrug-using subjects, the functional link between the β- and δ-networks is balanced, and the δ-network competitively controls impulsivity. However, in abstinent heroin-dependent subjects, the link is imbalanced, with stronger β-network connectivity and weaker δ-network connectivity. The imbalanced link is associated with impulsivity, indicating that the β- and δ-networks may mutually reinforce each other in abstinent heroin-dependent subjects. These findings of an aberrant link between the β- and δ-networks in abstinent heroin-dependent subjects may shed light on the mechanism of aberrant behaviors of drug addiction and may serve as an endophenotype to mark individual subjects' self-control capacity. Advanced neuroimaging studies have identified brain correlates of pathological impulsivity in a variety of neuropsychiatric disorders. However, whether and how these spatially separate and functionally integrated neural correlates collectively contribute to aberrant impulsive behaviors remains unclear. Building on recent progress in neuroeconomics toward determining a biological account of human behaviors, we employed resting-state functional MRI to characterize the nature of the links between these neural correlates and to investigate their impact on impulsivity. We demonstrated that through functional connectivity with the ventral medial prefrontal cortex, the δ-network (regions of the executive control system, such as the dorsolateral prefrontal cortex) and the β-network (regions of the reward system involved in the mesocorticolimbic pathway), jointly influence impulsivity measured by the Barratt impulsiveness scale scores. In control nondrug-using subjects, the functional link between the β- and δ-networks is balanced, and the δ-network competitively controls impulsivity. However, in abstinent heroin-dependent subjects, the link is imbalanced, with stronger β-network connectivity and weaker δ-network connectivity. The imbalanced link is associated with impulsivity, indicating that the β- and δ-networks may mutually reinforce each other in abstinent heroin-dependent subjects. These findings of an aberrant link between the β- and δ-networks in abstinent heroin-dependent subjects may shed light on the mechanism of aberrant behaviors of drug addiction and may serve as an endophenotype to mark individual subjects' self-control capacity. •We characterized the nature of functional links between valuation networks.•With the functional links to vmPFC, δ and β networks were found jointly influence the impulsivity.•The δ and β networks were balanced and competitively control impulsivity in CN group.•The δ and β networks were imbalanced and mutually reinforce impulsivity in HD group.•This altered δ–β relationship could serve as an endophenotype of aberrant behaviors. Advanced neuroimaging studies have identified brain correlates of pathological impulsivity in a variety of neuropsychiatric disorders. However, whether and how these spatially separate and functionally integrated neural correlates collectively contribute to aberrant impulsive behaviors remains unclear. Building on recent progress in neuroeconomics towards determining a biological account of human behaviors, we employed resting-state functional MRI to characterize the nature of the links between these neural correlates and to investigate their impact on impulsivity. We demonstrated that through functional connectivity with the ventral medial prefrontal cortex, the δ-network (regions of the executive control system, such as the dorsolateral prefrontal cortex) and the β-network (regions of the reward system involved in the mesocorticolimbic pathway), jointly influence impulsivity measured by the Barratt Impulsiveness Scale scores. In control nondrug-using subjects, the functional link between the β- and δ-networks is balanced, and the δ-network competitively controls impulsivity. However, in abstinent heroin-dependent subjects, the link is imbalanced, with stronger β-network connectivity and weaker δ-network connectivity. The imbalanced link is associated with impulsivity, indicating that the β- and δ-networks may mutually reinforce each other in abstinent heroin-dependent subjects. These findings of an aberrant link between the β- and δ-networks in abstinent heroin-dependent subjects may shed light on the mechanism of aberrant behaviors of drug addiction and may serve as an endophenotype to mark individual subjects’ self-control capacity. |
| Author | Li, Wenjun Wang, Lubin Ma, Lin Zou, Feng Lei, Yu Jin, Xiao Zhai, Tianye Yang, Zheng Chen, Guangyu Chen, Gang Li, Shi-Jiang Ye, Enmao Shao, Yongcong |
| AuthorAffiliation | 2 Department of Biophysics, Medical College of Wisconsin, Milwaukee, Wisconsin, USA 4 Department of Radiology, The General Hospital of the People’s Liberation Army, Beijing, P.R. China 3 Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences, School of Basic Medicine, Peking Union Medical College, Beijing, P.R. China 1 Cognitive and Mental Health Research Center, Beijing Institute of Basic Medical Science, Beijing, P.R. China |
| AuthorAffiliation_xml | – name: 4 Department of Radiology, The General Hospital of the People’s Liberation Army, Beijing, P.R. China – name: 3 Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences, School of Basic Medicine, Peking Union Medical College, Beijing, P.R. China – name: 1 Cognitive and Mental Health Research Center, Beijing Institute of Basic Medical Science, Beijing, P.R. China – name: 2 Department of Biophysics, Medical College of Wisconsin, Milwaukee, Wisconsin, USA |
| Author_xml | – sequence: 1 givenname: Tianye surname: Zhai fullname: Zhai, Tianye organization: Cognitive and Mental Health Research Center, Beijing Institute of Basic Medical Science, Beijing, PR China – sequence: 2 givenname: Yongcong surname: Shao fullname: Shao, Yongcong organization: Cognitive and Mental Health Research Center, Beijing Institute of Basic Medical Science, Beijing, PR China – sequence: 3 givenname: Gang surname: Chen fullname: Chen, Gang organization: Department of Biophysics, Medical College of Wisconsin, Milwaukee, WI, USA – sequence: 4 givenname: Enmao surname: Ye fullname: Ye, Enmao organization: Cognitive and Mental Health Research Center, Beijing Institute of Basic Medical Science, Beijing, PR China – sequence: 5 givenname: Lin surname: Ma fullname: Ma, Lin organization: Department of Radiology, The General Hospital of the People's Liberation Army, Beijing, PR China – sequence: 6 givenname: Lubin surname: Wang fullname: Wang, Lubin organization: Cognitive and Mental Health Research Center, Beijing Institute of Basic Medical Science, Beijing, PR China – sequence: 7 givenname: Yu surname: Lei fullname: Lei, Yu organization: Cognitive and Mental Health Research Center, Beijing Institute of Basic Medical Science, Beijing, PR China – sequence: 8 givenname: Guangyu surname: Chen fullname: Chen, Guangyu organization: Department of Biophysics, Medical College of Wisconsin, Milwaukee, WI, USA – sequence: 9 givenname: Wenjun surname: Li fullname: Li, Wenjun organization: Department of Biophysics, Medical College of Wisconsin, Milwaukee, WI, USA – sequence: 10 givenname: Feng surname: Zou fullname: Zou, Feng organization: Cognitive and Mental Health Research Center, Beijing Institute of Basic Medical Science, Beijing, PR China – sequence: 11 givenname: Xiao surname: Jin fullname: Jin, Xiao organization: Cognitive and Mental Health Research Center, Beijing Institute of Basic Medical Science, Beijing, PR China – sequence: 12 givenname: Shi-Jiang surname: Li fullname: Li, Shi-Jiang email: sjli@mcw.edu organization: Department of Biophysics, Medical College of Wisconsin, Milwaukee, WI, USA – sequence: 13 givenname: Zheng surname: Yang fullname: Yang, Zheng email: Yangzhengchina@aliyun.com organization: Cognitive and Mental Health Research Center, Beijing Institute of Basic Medical Science, Beijing, PR China |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25944613$$D View this record in MEDLINE/PubMed |
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| Keywords | ADHD DSM-IV IPL DMPFC vmPFC iBOLD MNI IFG OFC SCID Heroin addiction SPM8 ANCOVA Neuroeconomics WM CC Valuation networks Self-control DLPFC Resting-state functional connectivity MRI GM CN 3D-SPGR FOV BIS LOO ROI PCC TE o-VBM FWHM NAcc HD FC AFNI TR EPI |
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| SubjectTerms | Adult Executive Function Female Heroin addiction Heroin Dependence - pathology Heroin Dependence - psychology Humans Image Processing, Computer-Assisted Impulsive Behavior Magnetic Resonance Imaging Male Nerve Net - pathology Neural Pathways - pathology Neuroeconomics Prefrontal Cortex - pathology Resting-state functional connectivity MRI Self-control Valuation networks |
| Title | Nature of functional links in valuation networks differentiates impulsive behaviors between abstinent heroin-dependent subjects and nondrug-using subjects |
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