Shifts in the functional topography of frontal cortex-striatum connectivity in alcohol use disorder.


Journal

Addiction biology
ISSN: 1369-1600
Titre abrégé: Addict Biol
Pays: United States
ID NLM: 9604935

Informations de publication

Date de publication:
11 2019
Historique:
received: 25 06 2018
revised: 09 10 2018
accepted: 09 10 2018
pubmed: 24 11 2018
medline: 29 10 2020
entrez: 24 11 2018
Statut: ppublish

Résumé

Frontostriatal circuits are centrally involved in the selection of behavioral programs and play a prominent role in alcohol use disorder (AUD) as well as other mental disorders. However, how frontal regions change their striatal connectivity to implement adaptive cognitive control is still not fully understood. Here, we developed an approach for functional magnetic resonance imaging (fMRI) connectivity analysis in which we change the focus from connectivity to individual voxels towards spatial information about the location of strongest functional connectivity. In resting state data of n = 66 participants with AUD and n = 40 healthy controls (HC) we used the approach to estimate frontostriatal connectivity gradients consistent with nonhuman primate tract-tracing studies, characterized for each frontal voxel the striatal peak connectivity location on this gradient (PeaCoG), and tested for group differences and associations with clinical variables. We identified a cluster in the right orbitofrontal cortex (rOFC) with a peak connectivity shift towards ventral striatal regions in AUD. Reduced variability of rOFC striatal peak connectivity in the AUD group suggests a "clamping" to the ventral striatum as the underlying effect. Within the AUD group striatal peak connectivity in the superior frontal gyrus was associated with self-efficacy to abstain from alcohol, in the medial frontal and dorsolateral prefrontal cortex with alcohol dependency, and in the right inferior frontal gyrus with the urge to consume alcohol. Our results demonstrate that the functional topography of frontostriatal circuits exhibits interindividual variability, which provides insight into frontostriatal network adaptations in AUD and potentially other mental disorders.

Identifiants

pubmed: 30468293
doi: 10.1111/adb.12692
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1245-1253

Subventions

Organisme : Bundesministerium für Bildung und Forschung
ID : 01GQ1003B
Pays : International
Organisme : Bundesministerium für Bildung und Forschung
ID : 01ZX1311A
Pays : International
Organisme : Horizon 2020 Framework Programme
ID : No 668863 (SyBil-AA)
Pays : International
Organisme : Deutsche Forschungsgemeinschaft
ID : SFB 636/D6
Pays : International

Informations de copyright

© 2018 Society for the Study of Addiction.

Références

Haber SN. The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat. 2003;26(4):317-330.
Haber SN. Corticostriatal circuitry. Dialogues Clin Neurosci. 2016;18(1):7-21.
Shipp S. The functional logic of corticostriatal connections. Brain Struct Funct. 2017;222(2):669-706.
Forbes EE, Rodriguez EE, Musselman S, Narendran R. Prefrontal response and Frontostriatal functional connectivity to monetary reward in abstinent alcohol-dependent young adults. PLoS One. 2014;9(5):e94640.
Goldstein RZ, Volkow ND. Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci. 2011;12(11):652-669.
Akine Y, Kato M, Muramatsu T, et al. Altered brain activation by a false recognition task in young abstinent patients with alcohol dependence. Alcohol Clin Exp Res. 2007;31(9):1589-1597.
Goldstein RZ, Leskovjan AC, Hoff AL, et al. Severity of neuropsychological impairment in cocaine and alcohol addiction: association with metabolism in the prefrontal cortex. Neuropsychologia. 2004;42(11):1447-1458.
Goldstein RZ, Volkow ND. Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. Am J Psychiatry. 2002;159(10):1642-1652.
Li CR, Luo X, Yan P, Bergquist K, Sinha R. Altered impulse control in alcohol dependence: neural measures of stop signal performance. Alcohol Clin Exp Res. 2009;33(4):740-750.
Camchong J, Stenger VA, Fein G. Resting state synchrony in short-term versus long-term abstinent alcoholics. Alcohol Clin Exp Res. 2013b;37(5):794-803.
Müller-Oehring EM, Jung Y-C, Pfefferbaum A, Sullivan EV, Schulte T. The resting brain of alcoholics. Cereb Cortex. 2015;25(11):4155-4168.
Zhu X, Cortes CR, Mathur K, Tomasi D, Momenan R. Model-free functional connectivity and impulsivity correlates of alcohol dependence: a resting-state study. Addict Biol. 2017;22(1):206-217.
Camchong J, Stenger A, Fein G. Resting-state synchrony during early alcohol abstinence can predict subsequent relapse. Cereb Cortex. 2013a;23(9):2086-2099.
Everitt BJ, Robbins TW. Drug addiction: updating actions to habits to compulsions ten years on. Annu Rev Psychol. 2016;67(1):23-50.
Vollstädt-Klein S, Wichert S, Rabinstein J, et al. Initial, habitual and compulsive alcohol use is characterized by a shift of cue processing from ventral to dorsal striatum. Addiction. 2010;105(10):1741-1749.
Choi EY, Yeo BTT, Buckner RL. The organization of the human striatum estimated by intrinsic functional connectivity. J Neurophysiol. 2012;108(8):2242-2263.
Di Martino A, Scheres A, Margulies DS, et al. Functional connectivity of human striatum: a resting state fMRI study. Cereb Cortex. 2008;18(12):2735-2747.
Draganski B, Kherif F, Klöppel S, et al. Evidence for segregated and integrative connectivity patterns in the human basal ganglia. J Neurosci. 2008;28(28):7143-7152.
Jeon H-A, Anwander A, Friederici AD. Functional network mirrored in the prefrontal cortex, caudate nucleus, and thalamus: high-resolution functional imaging and structural connectivity. J Neurosci. 2014;34(28):9202-9212.
Robinson JL, Laird AR, Glahn DC, et al. The functional connectivity of the human caudate: an application of meta-analytic connectivity modeling with behavioral filtering. Neuroimage. 2012;60(1):117-129.
Verstynen TD, Badre D, Jarbo K, Schneider W. Microstructural organizational patterns in the human corticostriatal system. J Neurophysiol. 2012;107(11):2984-2995.
Averbeck BB, Lehman J, Jacobson M, Haber SN. Estimates of projection overlap and zones of convergence within frontal-striatal circuits. J Neurosci. 2014;34(29):9497-9505.
Barnes KA, Cohen AL, Power JD, et al. Identifying basal ganglia divisions in individuals using resting-state functional connectivity MRI. Front Syst Neurosci. 2010;4:18.
Jarbo K, Verstynen TD. Converging structural and functional connectivity of orbitofrontal, dorsolateral prefrontal, and posterior parietal cortex in the human striatum. J Neurosci. 2015;35(9):3865-3878.
Jung WH, Jang JH, Park JW, et al. Unravelling the intrinsic functional organization of the human striatum: a parcellation and connectivity study based on resting-state fMRI. PLoS One. 2014;9(9):e106768.
Selemon L, Goldman-Rakic P. Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J Neurosci. 1985;5(3):776-794.
Yeterian EH, Van Hoesen GW. Cortico-striate projections in the rhesus monkey: the organization of certain cortico-caudate connections. Brain Res. 1978;139(1):43-63.
First MB, Spitzer RL, Gibbon M, Williams JB. Structured Clinical Interview for DSM-IV Axis I Disorders: Patient Edition (February 1996 Final), SCID-I/P. Biometrics Research Department, New York State Psychiatric Institute; 1998.
Anton RF. Obsessive-compulsive aspects of craving: development of the obsessive compulsive drinking scale. Addiction. 2000;95:211-217.
DiClemente CC, Carbonari JP, Montgomery RP, Hughes SO. The alcohol abstinence self-efficacy scale. J Stud Alcohol. 1994;55(2):141-148.
Skinner HA, Horn JL, Ontario ARF. Alcohol Dependence Scale (ADS) User's Guide. Addiction Research Foundation; 1984.
Bohn MJ, Krahn DD, Staehler BA. Development and initial validation of a measure of drinking urges in abstinent alcoholics. Alcohol Clin Exp Res. 1995;19(3):600-606.
Becker A, Gerchen MF, Kirsch M, Hoffmann S, Kiefer F, Kirsch P. Striatal reward sensitivity predicts therapy-related neural changes in alcohol addiction. Eur Arch Psychiatry Clin Neurosci. 2018;268(3):231-242.
Becker A, Kirsch M, Gerchen MF, Kiefer F, Kirsch P. Striatal activation and frontostriatal connectivity during non-drug reward anticipation in alcohol dependence. Addict Biol. 2017;22(3):833-843.
Buuren M, Gladwin TE, Zandbelt BB, et al. Cardiorespiratory effects on default-mode network activity as measured with fMRI. Hum Brain Mapp. 2009;30:3031-3042.
Winkler AM, Ridgway GR, Webster MA, Smith SM, Nichols TE. Permutation inference for the general linear model. Neuroimage. 2014;92:381-397.
Smith SM, Nichols TE. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage. 2009;44(1):83-98.
Brown MB, Forsythe AB. Robust tests for the equality of variances. J Am Stat Assoc. 1974;69(346):364-367.
Olejnik SF, Algina J. Type I error rates and power estimates of selected parametric and nonparametric tests of scale. J Educ Stat. 1987;12(1):45-61.
Volkow ND, Fowler JS. Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex. Cereb Cortex. 2000;10(3):318-325.
Park SQ, Kahnt T, Beck A, et al. Prefrontal cortex fails to learn from reward prediction errors in alcohol dependence. J Neurosci Off J Soc Neurosci. 2010;30(22):7749-7753.
Hampshire A, Chamberlain SR, Monti MM, Duncan J, Owen AM. The role of the right inferior frontal gyrus: inhibition and attentional control. Neuroimage. 2010;50(3):1313-1319.
Aron AR, Robbins TW, Poldrack RA. Inhibition and the right inferior frontal cortex: one decade on. Trends Cogn Sci. 2014;18(4):177-185.
Zang YF, He Y, Zhu CZ, et al. Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev. 2007;29(2):83-91.
Volkow ND, Koob GF, McLellan AT. Neurobiologic advances from the brain disease model of addiction. N Engl J Med. 2016;374(4):363-371.
Peters S, Jolles DJ, Van Duijvenvoorde AC, Crone EA, Peper JS. The link between testosterone and amygdala-orbitofrontal cortex connectivity in adolescent alcohol use. Psychoneuroendocrinology. 2015;53:117-126.
Peters S, Peper JS, Van Duijvenvoorde ACK, Braams BR, Crone EA. Amygdala-orbitofrontal connectivity predicts alcohol use two years later: a longitudinal neuroimaging study on alcohol use in adolescence. Dev Sci. 2017;20(4).
Lin F, Zhou Y, Du Y, et al. Aberrant corticostriatal functional circuits in adolescents with internet addiction disorder. Front Hum Neurosci. 2015;9.
Gerchen MF, Kirsch M, Bahs N, et al. The SyBil-AA real-time fMRI neurofeedback study: protocol of a single-blind randomized controlled trial in alcohol use disorder. BMC Psychiatry. 2018;18(1):12.
Kirsch M, Gruber I, Ruf M, Kiefer F, Kirsch P. Real-time functional magnetic resonance imaging neurofeedback can reduce striatal cue-reactivity to alcohol stimuli. Addict Biol. 2016;21(4):982-992.

Auteurs

Martin Fungisai Gerchen (MF)

Department of Clinical Psychology, Central Institute of Mental Health, University of Heidelberg/Medical Faculty Mannheim, Mannheim, Germany.
Bernstein Center for Computational Neuroscience Heidelberg/Mannheim, Mannheim, Germany.

Alena Rentsch (A)

Department of Clinical Psychology, Central Institute of Mental Health, University of Heidelberg/Medical Faculty Mannheim, Mannheim, Germany.

Martina Kirsch (M)

Department of Addiction Behavior and Addiction Medicine, Central Institute of Mental Health, University of Heidelberg/Medical Faculty Mannheim, Mannheim, Germany.

Falk Kiefer (F)

Department of Addiction Behavior and Addiction Medicine, Central Institute of Mental Health, University of Heidelberg/Medical Faculty Mannheim, Mannheim, Germany.

Peter Kirsch (P)

Department of Clinical Psychology, Central Institute of Mental Health, University of Heidelberg/Medical Faculty Mannheim, Mannheim, Germany.
Bernstein Center for Computational Neuroscience Heidelberg/Mannheim, Mannheim, Germany.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH