Longitudinal change of inhibitory control functional connectivity associated with the development of heavy alcohol drinking

Luis F Antón-Toro; Danylyna Shpakivska-Bilan; Alberto Del Cerro-León; Ricardo Bruña; Marcos Uceta; Luis M García-Moreno; Fernando Maestú

doi:10.3389/fpsyg.2023.1069990

Longitudinal change of inhibitory control functional connectivity associated with the development of heavy alcohol drinking

Front Psychol. 2023 Feb 3:14:1069990. doi: 10.3389/fpsyg.2023.1069990. eCollection 2023.

Authors

Luis F Antón-Toro^{1

2}, Danylyna Shpakivska-Bilan^{1

3}, Alberto Del Cerro-León^{1

3}, Ricardo Bruña^{1

4}, Marcos Uceta^{1

5}, Luis M García-Moreno⁶, Fernando Maestú^{1

3}

Affiliations

¹ Center for Cognitive and Computational Neuroscience (C3N), Complutense University of Madrid (UCM), Madrid, Spain.
² Department of Psychology, University Camilo José Cela (UCJC), Madrid, Spain.
³ Department of Experimental Psychology, Faculty of Psychology, Complutense University of Madrid (UCM), Madrid, Spain.
⁴ Department of Radiology, Faculty of Medicine, Complutense University of Madrid (UCM), Madrid, Spain.
⁵ Department of Cellular Biology, Faculty of Biology, Complutense University of Madrid (UCM), Madrid, Spain.
⁶ Department of Psychobiology and Methodology in Behavioral Science, Faculty of Psychology, Complutense University of Madrid (UCM), Madrid, Spain.

Abstract

Introduction: Heavy drinking (HD) prevalent pattern of alcohol consumption among adolescents, particularly concerning because of their critical vulnerability to the neurotoxic effects of ethanol. Adolescent neurodevelopment is characterized by critical neurobiological changes of the prefrontal, temporal and parietal regions, important for the development of executive control processes, such as inhibitory control (IC). In the present Magnetoencephalography (MEG) study, we aimed to describe the relationship between electrophysiological Functional Connectivity (FC) during an IC task and HD development, as well as its impact on functional neuromaturation.

Methods: We performed a two-year longitudinal protocol with two stages. In the first stage, before the onset of HD, we recorded brain electrophysiological activity from a sample of 67 adolescents (mean age = 14.6 ± 0.7) during an IC task. Alcohol consumption was measured using the AUDIT test and a semi-structured interview. Two years later, in the second stage, 32 of the 67 participants (mean age 16.7 ± 0.7) completed a similar protocol. As for the analysis in the first stage, the source-space FC matrix was calculated, and then, using a cluster-based permutation test (CBPT) based on Spearman's correlation, we calculated the correlation between the FC of each cortical source and the number of standard alcohol units consumed two years later. For the analysis of longitudinal change, we followed a similar approach. We calculated the symmetrized percentage change (SPC) between FC at both stages and performed a CBPT analysis, analyzing the correlation between FC change and the level of alcohol consumed in a regular session.

Results: The results revealed an association between higher beta-band FC in the prefrontal and temporal regions and higher consumption years later. Longitudinal results showed that greater future alcohol consumption was associated with an exacerbated reduction in the FC of the same areas.

Discussion: These results underline the existence of several brain functional differences prior to alcohol misuse and their impact on functional neuromaturation.

Keywords: MEG; adolescence; binge drinking; functional connectivity; heavy drinking; inhibitory control.