Linking Impulsivity to Activity Levels in Pre-Supplementary Motor Area during Sequential Gambling

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Impulsivity refers to the tendency to act prematurely or without forethought, and excessive impulsivity is a key problem in many neuropsychiatric disorders. Since the pre-supplementary motor area (pre-SMA) has been implicated in inhibitory control, this region may also contribute to impulsivity. Here, we examined whether functional recruitment of pre-SMA may contribute to risky choice behavior (state impulsivity) during sequential gambling and its relation to self-reported trait impulsivity. To this end, we performed task-based functional MRI (fMRI) after low-frequency (1Hz) repetitive transcranial magnetic stimulation (rTMS) of the pre-SMA. We expected low-frequency rTMS to modulate task-related engagement of the pre-SMA and, hereby, tune the tendency to make risky choices. Twenty-four healthy volunteers (12 females; age range, 19-52years) received real or sham-rTMS on separate days in counterbalanced order. Thereafter, participants performed a sequential gambling task with concurrently increasing stakes and risk during whole-brain fMRI. In the sham-rTMS session, self-reported trait impulsivity scaled positively with state impulsivity (riskier choice behavior) during gambling. The higher the trait impulsivity, the lower was the task-related increase in pre-SMA activity with increasingly risky choices. Following real-rTMS, low-impulsivity participants increased their preference for risky choices, while the opposite was true for high-impulsivity participants, resulting in an overall decoupling of trait impulsivity and state impulsivity during gambling. This rTMS-induced behavioral shift was mirrored in the rTMS-induced change in pre-SMA activation. These results provide converging evidence for a causal link between the level of task-related pre-SMA activity and the propensity for impulsive risk-taking behavior in the context of sequential gambling.

OriginalsprogEngelsk
TidsskriftJournal of Neuroscience
Vol/bind43
Udgave nummer8
Sider (fra-til)1414-1421
Antal sider8
ISSN0270-6474
DOI
StatusUdgivet - 2023

Bibliografisk note

Funding Information:
This work was supported by the Danish Parkinson Foundation (Parkinsonforeningen), The Capital Region of Denmark (Region Hovedstaden), Amager and Hvidovre Hospitals, Bispebjerg and Frederiksberg Hospitals, and The Danish Movement Disorder Society. D.M. was supported by the Novo Nordisk Foundation (Grant NNF16OC0023090) and by a Collaborative Alliance grant from the Lundbeck Foundation awarded to H.R.S. (“ADAPT-PD”, Grant R336-2020-1035). H.R.S. holds a 5-year professorship in precision medicine at the Faculty of Health Sciences and Medicine, University of Copenhagen, which is sponsored by the Lundbeck Foundation (Grant R186-2015-2138). None of the funding sources were involved in the undertaking of the study.

Funding Information:
This work was supported by the Danish Parkinson Foundation (Parkinsonforeningen), The Capital Region of Denmark (Region Hovedstaden), Amager and Hvidovre Hospitals, Bispebjerg and Frederiksberg Hospitals, and The Danish Movement Disorder Society. D.M. was supported by the Novo Nordisk Foundation (Grant NNF16OC0023090) and by a Collaborative Alliance grant from the Lundbeck Foundation awarded to H.R.S. (“ADAPT-PD”, Grant R336-2020-1035). H.R.S. holds a 5-year professorship in precision medicine at the Faculty of Health Sciences and Medicine, University of Copenhagen, which is sponsored by the Lundbeck Foundation (Grant R186-2015-2138). None of the funding sources were involved in the undertaking of the study. A. Løkkegaard has received speaking fees from Abbvie. H.R.S. has received honoraria as a speaker from Lundbeck AS (Denmark), Sanofi Genzyme (Denmark), and Novartis (Denmark); as a consultant from Lundbeck AS (Denmark) and Sanofi Genzyme (Denmark); and as a senior editor (NeuroImage) and editor-in-chief (NeuroImage Clinical) from Elsevier Publishers (Amsterdam, The Netherlands) H.R.S. has also received royalties as a book editor from Springer Publishers (Stuttgart, Germany).

Publisher Copyright:
Copyright © 2023 Lohse et al.

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