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Variants of the P3 event-related potential operate as indicators of distinct mechanisms contributing to problematic alcohol use

Neuropsychopharmacology (2024)Cite this article

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Abstract

Considerable research has linked relative reduction in the amplitude of the P3 event-related potential (ERP) during cognitive task performance (i.e., Target-P3) with increased risk of alcohol-related problems. A separate literature indicates that a relative increase in the amplitude of the P3 elicited by cues signaling alcohol availability (i.e., ACR-P3) also is associated with alcohol use and problems. To date, no research has integrated these seemingly discrepant findings. Here, we aimed to demonstrate that P3 amplitudes elicited in different task contexts reflect distinct domains of functioning relevant to problematic alcohol involvement (PAI), and therefore can inform heterogeneity in the etiology of PAI. 156 emerging adults (61% women; 88% White/Non-Hispanic) completed a mental rotation task and a picture-viewing task while ERPs were recorded. Participants also completed questionnaire measures of trait disinhibition, alcohol use, and alcohol-related problems. Findings from regression analyses indicated that (a) Target-P3 was negatively associated and ACR-P3 was positively associated with a PAI latent variable; (b) the two P3s accounted for unique variance in PAI, beyond that accounted for by recent drinking; and (c) the association between Target-P3 and PAI—but not ACR-P3 and PAI—was statistically mediated by trait disinhibition. The present findings highlight the unique contributions of distinct functional domains associated with disinhibition and incentive salience in the etiology of PAI. Moreover, findings are consistent with a nuanced understanding of the P3 ERP, whereby its specific meaning varies according to the task context in which it is elicited.

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Fig. 1: Waveform plots for variants of the P3 brain response from the picture-viewing and rotated heads oddball tasks.
Fig. 2: Opposing associations for Target-P3 and ACR-P3 with problematic alcohol involvement.
Fig. 3: Indirect effects of P3 variants (Target, ACR) on PAI through trait disinhibition.
Fig. 4: Model demonstrating a unique association for ACR-P3 with PAI, distinct from its association with a general P3 factor.

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Notes

  1. The YAACQ was added part-way into the study, and thus scores for this measure were available for 103 rather than all participants.

  2. A Heywood case emerged in this model, involving the loading of the YAACQ total score onto the latent alcohol problems factor; thus, the model was re-run fixing this loading to 1.0. Model fit statistics and further modeling analyses utilized this revised model.

  3. In response to a helpful anonymous reviewer comment concerning divergent validity, we also tested indirect pathways through alcohol expectancies as assessed by the Comprehensive Effects of Alcohol Questionnaire (Fromme, Stroot, & Kaplan, 1993). None of this measure’s 7 subscales (Sociability, Tension Reduction, Liquid Courage, Sexuality, Cognitive and Behavioral Impairment, Risk and Aggression, Self-Perception) emerged as a significant mediator when used in place of ESI-Disinhibition in the current model (all indirect effect p’s > 0.12). For completeness, expectancy, and valuation scores were calculated separately for each of the subscales and tested as mediators; again, no significant indirect effects emerged in any of the 14 models for these scores (all indirect effect p’s > 0.11).

  4. Magnitude of loadings and prediction of the ACR-P3 from the general factor did not differ appreciably when including mean P3 response to pleasant pictures [47] as a fourth indicator of the general P3 factor. The λs for Target-P3, NNB-P3, NAB-P3, and Pleasant-P3 in this alternative model were 0.51, 0.59, 0.86, and 0.74, respectively, and the β for prediction of ACR-P3 from the four-indicator general P3 factor was 0.72, p < 0.001.

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Funding

Data collection was supported by grants R01 AA025451 (PI: Bartholow) and T32 AA013526 (PI: McCarthy) from the National Institute on Alcohol Abuse and Alcoholism (NIAAA) and R01 AA019546 from NIAAA/the Office of Social Sciences and Behavioral Research (PI: McCarthy). Preparation of this article was supported by NIAAA grants R01 AA030728 (PI: Bartholow) and R01 AA030914 (PI: Bartholow), grant R36 DA050049 from the National Institute on Drug Abuse (PI: Joyner), and grant W911NF-14-1-0018 from the US Army (PI: Patrick). The content of this article is solely the responsibility of the authors and does not necessarily represent the official views of the U.S. Government, Department of Defense, Department of the Army, Department of Veterans Affairs, or U.S. Recruiting Command.

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Authors and Affiliations

  1. Department of Psychology, University of California, Berkeley, CA, USA

    Keanan J. Joyner

  2. Department of Psychology, Florida State University, Tallahassee, FL, USA

    Christopher J. Patrick

  3. Alvin J. Siteman Cancer Center, Washington University in St. Louis, St. Louis, MO, USA

    David H. Morris

  4. Department of Psychological Sciences, University of Missouri, Columbia, MO, USA

    Denis M. McCarthy

  5. Department of Psychological and Brain Sciences, University of Iowa, Iowa City, IA, USA

    Bruce D. Bartholow

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KJJ leads conceptualization, analysis, and results interpretation, and co-leads initial drafting and edits. CJP co-leads initial drafting and edits. DHM led data collection and management and contributed edits. DMM contributed edits. BDB co-led conceptualization, initial drafting, and edits, supervised data collection and management, and secured funding for primary data collection.

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Joyner, K.J., Patrick, C.J., Morris, D.H. et al. Variants of the P3 event-related potential operate as indicators of distinct mechanisms contributing to problematic alcohol use. Neuropsychopharmacol. (2024). https://doi.org/10.1038/s41386-024-01874-7

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