Theta oscillatory dynamics serving cognitive control index psychosocial distress in youth

Mikki Schantell; Brittany K Taylor; Amirsalar Mansouri; Yasra Arif; Anna T Coutant; Danielle L Rice; Yu-Ping Wang; Vince D Calhoun; Julia M Stephen; Tony W Wilson

doi:10.1016/j.ynstr.2023.100599

Theta oscillatory dynamics serving cognitive control index psychosocial distress in youth

Neurobiol Stress. 2023 Dec 15:29:100599. doi: 10.1016/j.ynstr.2023.100599. eCollection 2024 Mar.

Authors

Mikki Schantell^{1

2

3}, Brittany K Taylor^{1

3

4}, Amirsalar Mansouri¹, Yasra Arif^{1

3}, Anna T Coutant^{1

3}, Danielle L Rice^{1

3}, Yu-Ping Wang⁵, Vince D Calhoun⁶, Julia M Stephen⁷, Tony W Wilson^{1

2

3

4}

Affiliations

¹ Institute for Human Neuroscience, Boys Town National Research Hospital, Boys Town, NE, USA.
² College of Medicine, University of Nebraska Medical Center, Omaha, NE, USA.
³ Center for Pediatric Brain Health, Boys Town National Research Hospital, Boys Town, NE, USA.
⁴ Department of Pharmacology & Neuroscience, Creighton University, Omaha, NE, USA.
⁵ Department of Biomedical Engineering, Tulane University, New Orleans, LA, USA.
⁶ Tri-institutional Center for Translational Research in Neuroimaging & Data Science (TReNDS), Georgia State University, Georgia Institute of Technology, Emory University, Atlanta, GA, USA.
⁷ Mind Research Network, Albuquerque, NM, USA.

Abstract

Background: Psychosocial distress among youth is a major public health issue characterized by disruptions in cognitive control processing. Using the National Institute of Mental Health's Research Domain Criteria (RDoC) framework, we quantified multidimensional neural oscillatory markers of psychosocial distress serving cognitive control in youth.

Methods: The sample consisted of 39 peri-adolescent participants who completed the NIH Toolbox Emotion Battery (NIHTB-EB) and the Eriksen flanker task during magnetoencephalography (MEG). A psychosocial distress index was computed with exploratory factor analysis using assessments from the NIHTB-EB. MEG data were analyzed in the time-frequency domain and peak voxels from oscillatory maps depicting the neural cognitive interference effect were extracted for voxel time series analyses to identify spontaneous and oscillatory aberrations in dynamics serving cognitive control as a function of psychosocial distress. Further, we quantified the relationship between psychosocial distress and dynamic functional connectivity between regions supporting cognitive control.

Results: The continuous psychosocial distress index was strongly associated with validated measures of pediatric psychopathology. Theta-band neural cognitive interference was identified in the left dorsolateral prefrontal cortex (dlPFC) and middle cingulate cortex (MCC). Time series analyses of these regions indicated that greater psychosocial distress was associated with elevated spontaneous activity in both the dlPFC and MCC and blunted theta oscillations in the MCC. Finally, we found that stronger phase coherence between the dlPFC and MCC was associated with greater psychosocial distress.

Conclusions: Greater psychosocial distress was marked by alterations in spontaneous and oscillatory theta activity serving cognitive control, along with hyperconnectivity between the dlPFC and MCC.

Keywords: Cognitive control; Magnetoencephalography; Psychosocial distress; Research domain criteria (RDoC); Youth.

Abstract

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