Shifted balance of dorsal versus ventral striatal communication with frontal reward and regulatory regions in cannabis‐dependent males
The transition from voluntary to addictive behavior is characterized by a loss of regulatory control in favor of reward driven behavior. Animal models indicate that this process is neurally underpinned by a shift in ventral–dorsal striatal control of behavior; however, this shift has not been direct...
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| Published in | Human brain mapping Vol. 39; no. 12; pp. 5062 - 5073 |
|---|---|
| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
John Wiley & Sons, Inc
01.12.2018
|
| Subjects | |
| Online Access | Get full text |
| ISSN | 1065-9471 1097-0193 1097-0193 |
| DOI | 10.1002/hbm.24345 |
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| Abstract | The transition from voluntary to addictive behavior is characterized by a loss of regulatory control in favor of reward driven behavior. Animal models indicate that this process is neurally underpinned by a shift in ventral–dorsal striatal control of behavior; however, this shift has not been directly examined in humans. The present resting state functional magnetic resonance imaging (fMRI) study employed a two‐step approach to: (a) precisely map striatal alterations using a novel, data‐driven network classification strategy combining intrinsic connectivity contrast with multivoxel pattern analysis and, (b) to determine whether a ventral to dorsal striatal shift in connectivity with reward and regulatory control regions can be observed in abstinent (28 days) male cannabis‐dependent individuals (
n
= 24) relative to matched controls (
n
= 28). Network classification revealed that the groups can be reliably discriminated by global connectivity profiles of two striatal regions that mapped onto the ventral (nucleus accumbens) and dorsal striatum (caudate). Subsequent functional connectivity analysis demonstrated a relative shift between ventral and dorsal striatal communication with fronto‐limbic regions that have been consistently involved in reward processing (rostral anterior cingulate cortex [ACC]) and executive/regulatory functions (dorsomedial prefrontal cortex [PFC]). Specifically, in the cannabis‐dependent subjects, connectivity between the ventral striatum with the rostral ACC increased, whereas both striatal regions were uncoupled from the regulatory dorsomedial PFC. Together, these findings suggest a shift in the balance between dorsal and ventral striatal control in cannabis dependence. Similar changes have been observed in animal models and may promote the loss of control central to addictive behavior. |
|---|---|
| AbstractList | The transition from voluntary to addictive behavior is characterized by a loss of regulatory control in favor of reward driven behavior. Animal models indicate that this process is neurally underpinned by a shift in ventral–dorsal striatal control of behavior; however, this shift has not been directly examined in humans. The present resting state functional magnetic resonance imaging (fMRI) study employed a two‐step approach to: (a) precisely map striatal alterations using a novel, data‐driven network classification strategy combining intrinsic connectivity contrast with multivoxel pattern analysis and, (b) to determine whether a ventral to dorsal striatal shift in connectivity with reward and regulatory control regions can be observed in abstinent (28 days) male cannabis‐dependent individuals (n = 24) relative to matched controls (n = 28). Network classification revealed that the groups can be reliably discriminated by global connectivity profiles of two striatal regions that mapped onto the ventral (nucleus accumbens) and dorsal striatum (caudate). Subsequent functional connectivity analysis demonstrated a relative shift between ventral and dorsal striatal communication with fronto‐limbic regions that have been consistently involved in reward processing (rostral anterior cingulate cortex [ACC]) and executive/regulatory functions (dorsomedial prefrontal cortex [PFC]). Specifically, in the cannabis‐dependent subjects, connectivity between the ventral striatum with the rostral ACC increased, whereas both striatal regions were uncoupled from the regulatory dorsomedial PFC. Together, these findings suggest a shift in the balance between dorsal and ventral striatal control in cannabis dependence. Similar changes have been observed in animal models and may promote the loss of control central to addictive behavior. The transition from voluntary to addictive behavior is characterized by a loss of regulatory control in favor of reward driven behavior. Animal models indicate that this process is neurally underpinned by a shift in ventral–dorsal striatal control of behavior; however, this shift has not been directly examined in humans. The present resting state functional magnetic resonance imaging (fMRI) study employed a two‐step approach to: (a) precisely map striatal alterations using a novel, data‐driven network classification strategy combining intrinsic connectivity contrast with multivoxel pattern analysis and, (b) to determine whether a ventral to dorsal striatal shift in connectivity with reward and regulatory control regions can be observed in abstinent (28 days) male cannabis‐dependent individuals ( n = 24) relative to matched controls ( n = 28). Network classification revealed that the groups can be reliably discriminated by global connectivity profiles of two striatal regions that mapped onto the ventral (nucleus accumbens) and dorsal striatum (caudate). Subsequent functional connectivity analysis demonstrated a relative shift between ventral and dorsal striatal communication with fronto‐limbic regions that have been consistently involved in reward processing (rostral anterior cingulate cortex [ACC]) and executive/regulatory functions (dorsomedial prefrontal cortex [PFC]). Specifically, in the cannabis‐dependent subjects, connectivity between the ventral striatum with the rostral ACC increased, whereas both striatal regions were uncoupled from the regulatory dorsomedial PFC. Together, these findings suggest a shift in the balance between dorsal and ventral striatal control in cannabis dependence. Similar changes have been observed in animal models and may promote the loss of control central to addictive behavior. The transition from voluntary to addictive behavior is characterized by a loss of regulatory control in favor of reward driven behavior. Animal models indicate that this process is neurally underpinned by a shift in ventral-dorsal striatal control of behavior; however, this shift has not been directly examined in humans. The present resting state functional magnetic resonance imaging (fMRI) study employed a two-step approach to: (a) precisely map striatal alterations using a novel, data-driven network classification strategy combining intrinsic connectivity contrast with multivoxel pattern analysis and, (b) to determine whether a ventral to dorsal striatal shift in connectivity with reward and regulatory control regions can be observed in abstinent (28 days) male cannabis-dependent individuals (n = 24) relative to matched controls (n = 28). Network classification revealed that the groups can be reliably discriminated by global connectivity profiles of two striatal regions that mapped onto the ventral (nucleus accumbens) and dorsal striatum (caudate). Subsequent functional connectivity analysis demonstrated a relative shift between ventral and dorsal striatal communication with fronto-limbic regions that have been consistently involved in reward processing (rostral anterior cingulate cortex [ACC]) and executive/regulatory functions (dorsomedial prefrontal cortex [PFC]). Specifically, in the cannabis-dependent subjects, connectivity between the ventral striatum with the rostral ACC increased, whereas both striatal regions were uncoupled from the regulatory dorsomedial PFC. Together, these findings suggest a shift in the balance between dorsal and ventral striatal control in cannabis dependence. Similar changes have been observed in animal models and may promote the loss of control central to addictive behavior.The transition from voluntary to addictive behavior is characterized by a loss of regulatory control in favor of reward driven behavior. Animal models indicate that this process is neurally underpinned by a shift in ventral-dorsal striatal control of behavior; however, this shift has not been directly examined in humans. The present resting state functional magnetic resonance imaging (fMRI) study employed a two-step approach to: (a) precisely map striatal alterations using a novel, data-driven network classification strategy combining intrinsic connectivity contrast with multivoxel pattern analysis and, (b) to determine whether a ventral to dorsal striatal shift in connectivity with reward and regulatory control regions can be observed in abstinent (28 days) male cannabis-dependent individuals (n = 24) relative to matched controls (n = 28). Network classification revealed that the groups can be reliably discriminated by global connectivity profiles of two striatal regions that mapped onto the ventral (nucleus accumbens) and dorsal striatum (caudate). Subsequent functional connectivity analysis demonstrated a relative shift between ventral and dorsal striatal communication with fronto-limbic regions that have been consistently involved in reward processing (rostral anterior cingulate cortex [ACC]) and executive/regulatory functions (dorsomedial prefrontal cortex [PFC]). Specifically, in the cannabis-dependent subjects, connectivity between the ventral striatum with the rostral ACC increased, whereas both striatal regions were uncoupled from the regulatory dorsomedial PFC. Together, these findings suggest a shift in the balance between dorsal and ventral striatal control in cannabis dependence. Similar changes have been observed in animal models and may promote the loss of control central to addictive behavior. |
| Author | Dau, Wolfgang Zhou, Feng Zimmermann, Kaeli Becker, Benjamin Banger, Markus Kendrick, Keith M. Weber, Bernd Hurlemann, René Scheele, Dirk Xin, Fei |
| AuthorAffiliation | 1 The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Laboratory for Neuroinformation University of Electronic Science and Technology of China Chengdu China 4 Center for Economics and Neuroscience, Department of Epileptology University of Bonn Bonn Germany 2 Department of Psychiatry and Division of Medical Psychology University of Bonn Bonn Germany 3 Department of Addiction and Psychotherapy LVR‐Clinic Bonn Bonn Germany 5 Department of Neurocognition Life & Brain Center Bonn Germany |
| AuthorAffiliation_xml | – name: 4 Center for Economics and Neuroscience, Department of Epileptology University of Bonn Bonn Germany – name: 5 Department of Neurocognition Life & Brain Center Bonn Germany – name: 2 Department of Psychiatry and Division of Medical Psychology University of Bonn Bonn Germany – name: 1 The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Laboratory for Neuroinformation University of Electronic Science and Technology of China Chengdu China – name: 3 Department of Addiction and Psychotherapy LVR‐Clinic Bonn Bonn Germany |
| Author_xml | – sequence: 1 givenname: Feng surname: Zhou fullname: Zhou, Feng organization: The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Laboratory for Neuroinformation University of Electronic Science and Technology of China Chengdu China – sequence: 2 givenname: Kaeli surname: Zimmermann fullname: Zimmermann, Kaeli organization: Department of Psychiatry and Division of Medical Psychology University of Bonn Bonn Germany – sequence: 3 givenname: Fei surname: Xin fullname: Xin, Fei organization: The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Laboratory for Neuroinformation University of Electronic Science and Technology of China Chengdu China – sequence: 4 givenname: Dirk orcidid: 0000-0002-7613-0376 surname: Scheele fullname: Scheele, Dirk organization: Department of Psychiatry and Division of Medical Psychology University of Bonn Bonn Germany – sequence: 5 givenname: Wolfgang surname: Dau fullname: Dau, Wolfgang organization: Department of Addiction and Psychotherapy LVR‐Clinic Bonn Bonn Germany – sequence: 6 givenname: Markus surname: Banger fullname: Banger, Markus organization: Department of Addiction and Psychotherapy LVR‐Clinic Bonn Bonn Germany – sequence: 7 givenname: Bernd orcidid: 0000-0002-7811-9605 surname: Weber fullname: Weber, Bernd organization: Center for Economics and Neuroscience, Department of Epileptology University of Bonn Bonn Germany, Department of Neurocognition Life & Brain Center Bonn Germany – sequence: 8 givenname: René surname: Hurlemann fullname: Hurlemann, René organization: Department of Psychiatry and Division of Medical Psychology University of Bonn Bonn Germany – sequence: 9 givenname: Keith M. orcidid: 0000-0002-0371-5904 surname: Kendrick fullname: Kendrick, Keith M. organization: The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Laboratory for Neuroinformation University of Electronic Science and Technology of China Chengdu China – sequence: 10 givenname: Benjamin orcidid: 0000-0002-9014-9671 surname: Becker fullname: Becker, Benjamin organization: The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Laboratory for Neuroinformation University of Electronic Science and Technology of China Chengdu China |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30277629$$D View this record in MEDLINE/PubMed |
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| Keywords | reward cognitive control functional connectivity striatum anterior cingulate data-driven prefrontal cortex addiction intrinsic connectivity contrast cannabis |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Feng Zhou and Kaeli Zimmermann contributed equally to this work. Funding information National Natural Science Foundation of China, Grant/Award Number: 91632117, 31530032; Deutsche Forschungsgemeinschaft, Grant/Award Number: BE5465/2‐1, HU1302/4‐1; Fundamental Research Funds for Central Universities , Grant/Award Number: ZYGX2015Z002; Science, Innovation and Technology Department of the Sichuan Province, Grant/Award Number: 2018JY0001 |
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| SubjectTerms | Addictive behaviors Adolescent Adult Amphetamines Animal behavior Animal models Cannabis Caudate-putamen Classification Connectivity analysis Connectome - methods Cortex (cingulate) Dependence Executive Function - physiology Functional magnetic resonance imaging Gyrus Cinguli - diagnostic imaging Gyrus Cinguli - physiopathology Humans Magnetic Resonance Imaging Male Males Marijuana Marijuana Abuse - diagnostic imaging Marijuana Abuse - physiopathology Neostriatum Nerve Net - diagnostic imaging Nerve Net - physiopathology Neuroimaging Nucleus accumbens Pattern analysis Prefrontal cortex Prefrontal Cortex - diagnostic imaging Prefrontal Cortex - physiopathology Regulatory sequences Reinforcement Reward Ventral Striatum - diagnostic imaging Ventral Striatum - physiopathology Young Adult |
| Title | Shifted balance of dorsal versus ventral striatal communication with frontal reward and regulatory regions in cannabis‐dependent males |
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