Trait sensation seeking is associated with heightened beta-band oscillatory dynamics over left ventrolateral prefrontal cortex during reward expectancy.

Beta-band Electroencephalography Left Hemisphere Reward Anticipation Sensation Seeking Ventrolateral Prefrontal Cortex

Journal

Journal of affective disorders
ISSN: 1573-2517
Titre abrégé: J Affect Disord
Pays: Netherlands
ID NLM: 7906073

Informations de publication

Date de publication:
01 09 2021
Historique:
received: 10 03 2021
revised: 14 05 2021
accepted: 21 05 2021
pubmed: 9 6 2021
medline: 5 8 2021
entrez: 8 6 2021
Statut: ppublish

Résumé

Sensation Seeking, the proclivity toward novel and stimulating experiences, is associated with greater left ventrolateral prefrontal cortex (vlPFC) activity during uncertain reward expectancy. Here, we examined relationships between sensation seeking and vlPFC oscillatory dynamics using electroencephalography (EEG). In 26 adolescents/young adults (16 female; 22.3 ± 1.7yrs), EEG was measured during uncertain reward expectancy. Event-related spectral perturbations (ERSP) from 15-80 Hz (beta/gamma bands) were compared as a function of uncertain reward expected value and assessed for relationships with feedback-related negativity (FRN) response to outcome feedback and response tendency measures of risk for BD. Event-related synchronization (ERS) between 15-25 Hz (beta) over left vlPFC was sensitive to the expected value of uncertain reward (rho=0.46; p = 0.048), and correlated with sensation seeking (r = 0.49, p < 0.01) and feedback-related negativity (FRN), where greater beta ERS was related to larger FRN (r = -0.39, p = 0.047). FRN was also related to behavioral inhibition (r = 0.49, p < 0.01). It is unknown whether results may extrapolate to clinical populations, given the healthy sample used here. Further, although we have confidence that the beta-band signal we measure in this study arises from left prefrontal cortex, we largely infer a left vlPFC source. These findings highlight the role of left vlPFC in evaluation of immediate rewards. We now provide a link between reward expectancy-related left vlPFC activity and the well-characterized FRN, with a known role in attentive processing. These findings can guide treatment development for mania/hypomania at-risk individuals, including transcranial alternating current stimulation.

Sections du résumé

BACKGROUND
Sensation Seeking, the proclivity toward novel and stimulating experiences, is associated with greater left ventrolateral prefrontal cortex (vlPFC) activity during uncertain reward expectancy. Here, we examined relationships between sensation seeking and vlPFC oscillatory dynamics using electroencephalography (EEG).
METHODS
In 26 adolescents/young adults (16 female; 22.3 ± 1.7yrs), EEG was measured during uncertain reward expectancy. Event-related spectral perturbations (ERSP) from 15-80 Hz (beta/gamma bands) were compared as a function of uncertain reward expected value and assessed for relationships with feedback-related negativity (FRN) response to outcome feedback and response tendency measures of risk for BD.
RESULTS
Event-related synchronization (ERS) between 15-25 Hz (beta) over left vlPFC was sensitive to the expected value of uncertain reward (rho=0.46; p = 0.048), and correlated with sensation seeking (r = 0.49, p < 0.01) and feedback-related negativity (FRN), where greater beta ERS was related to larger FRN (r = -0.39, p = 0.047). FRN was also related to behavioral inhibition (r = 0.49, p < 0.01).
LIMITATIONS
It is unknown whether results may extrapolate to clinical populations, given the healthy sample used here. Further, although we have confidence that the beta-band signal we measure in this study arises from left prefrontal cortex, we largely infer a left vlPFC source.
CONCLUSIONS
These findings highlight the role of left vlPFC in evaluation of immediate rewards. We now provide a link between reward expectancy-related left vlPFC activity and the well-characterized FRN, with a known role in attentive processing. These findings can guide treatment development for mania/hypomania at-risk individuals, including transcranial alternating current stimulation.

Identifiants

pubmed: 34102550
pii: S0165-0327(21)00473-0
doi: 10.1016/j.jad.2021.05.029
pii:
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

67-74

Informations de copyright

Copyright © 2021. Published by Elsevier B.V.

Auteurs

Brian A Coffman (BA)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, United States. Electronic address: coffmanb@upmc.edu.

Natasha Torrence (N)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, United States.

Timothy Murphy (T)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, United States.

Genna Bebko (G)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, United States.

Simona Graur (S)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, United States.

Henry W Chase (HW)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, United States.

Dean F Salisbury (DF)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, United States.

Mary L Phillips (ML)

Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, United States.

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