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Alcohol impairs brain reactivity to explicit loss feedback

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Abstract

Rationale

Alcohol impairs the brain's detection of performance errors as evidenced by attenuated error-related negativity (ERN), an event-related potential (ERP) thought to reflect a brain system that monitors one's behavior. However, it remains unclear whether alcohol impairs performance-monitoring capacity across a broader range of contexts, including those entailing external feedback.

Objective

This study sought to determine whether alcohol-related monitoring deficits are specific to internal recognition of errors (reflected by the ERN) or occur also in external cuing contexts. We evaluated the impact of alcohol consumption on the feedback-related negativity (FRN), an ERP thought to engage a similar process as the ERN but elicited by negative performance feedback in the environment.

Methods

In an undergraduate sample randomly assigned to drink alcohol (n = 37; average peak BAC = 0.087 g/100 ml, estimated from breath alcohol sampling) or placebo beverages (n = 42), ERP responses to gain and loss feedback were measured during a two-choice gambling task. Time–frequency analysis was used to parse the overlapping theta-FRN and delta-P3 and clarified the effects of alcohol on the measures.

Results

Alcohol intoxication attenuated both the theta-FRN and delta-P3 brain responses to feedback. The theta-FRN attenuation was stronger following loss than gain feedback.

Conclusions

Attenuation of both theta-FRN and delta-P3 components indicates that alcohol pervasively attenuates the brain's response to feedback in this task. That theta-FRN attenuation was stronger following loss trials is consistent with prior ERN findings and suggests that alcohol broadly impairs the brain's recognition of negative performance outcomes across differing contexts.

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Notes

  1. A regression model that included the TD FRN gain–loss difference score as the DV, and theta-gain, theta-loss, delta-gain, and delta-loss as the IVs (all measured at FCz), yielded a multiple R of 0.85, F(4,74) = 49.57, p < 0.001. Theta-gain, theta-loss, delta-gain, and delta-loss each contributed uniquely to the amplitude of the TD FRN (ts[74] = −2.31, 9.47, 5.80, and −5.97, respectively, all ps < 0.03). A second regression model predicting TD P3 amplitude from these differing theta and delta component measures (measured at electrode Cz) yielded a similar outcome, F(4,74) = 181.63, p < 0.001, R = 0.95, with theta-loss, delta-gain, and delta-loss each contributing uniquely to the TD P3, ts(74) = 3.00, 4.87, and 5.06, respectively, all ps < 0.01. The predictive contribution of the theta-gain component in this case was non-significant, t(74) = 0.96, p = 0.340.

  2. To test for possible moderating effects of gender on these primary ERP variables of interest, we re-ran the feedback × group GLMs for theta-FRN and delta-P3 with gender included as an additional between-subjects factor. For delta-P3, no interactions involving gender were found, feedback × gender, group × gender, and feedback × group × gender, Fs(1,75) = 2.41, 1.00, and 2.79, all ps ≥ 0.10. For theta-FRN, a significant three-way feedback × group × gender interaction was evident, F(1,75) = 4.72, p = 0.03. However, in two-way GLMs conducted separately for men and women, the feedback × group interaction emerged as significant in each analysis, F(1,35) = 9.58, p = 0.004 for women and F(1,40) = 4.63, p = 0.038 for men—with the three-way interaction attributable not to a difference in the nature of the two-way interaction but only to a difference in the relative magnitude of alcohol's effect on loss versus gain differentiation, with women showing greater attenuation of loss/gain differentiation as a function of alcohol (relative to placebo) than men.

  3. Although possible differences in sample and study characteristics necessitate tentative conclusions regarding comparisons between these studies, it is worth noting that direct comparison of the theta-FRN amplitude across this and the Bernat et al. (2011) samples supports the claim that theta-FRN is more strongly affected by alcohol than trait disinhibition. Specifically, substituting the high-disinhibited subgroup (n = 94) from the Bernat et al. (2011) sample for the placebo control group indicated that, like the placebo group in the current study (both of whom completed the same experimental task), intoxicated individuals had attenuated theta-FRN in comparison to high-disinhibited participants, group F(1,92) = 21.09, p < 0.001, with relatively greater amplitude reduction for loss vs. gain trials, gain/loss × group, F(1,92) = 15.35, p < 0.001.

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Acknowledgements

This work was supported by grant AA12164 from the National Institute on Alcohol Abuse and Alcoholism and grants MH088143 and MH072850 from the National Institute of Mental Health.

Conflicts of interest

We have no conflicts of interest to report.

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Authors and Affiliations

  1. Department of Psychology, Florida State University, 1107 West Call Street, Tallahassee, FL, 32306-4301, USA

    Lindsay D. Nelson, Christopher J. Patrick, Alan R. Lang & Edward M. Bernat

  2. Department of Psychology, University of Minnesota, 75 E. River Road, Minneapolis, MN, 55455, USA

    Paul Collins

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  1. Lindsay D. Nelson
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  2. Christopher J. Patrick
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  3. Paul Collins
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  4. Alan R. Lang
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  5. Edward M. Bernat
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Correspondence to Lindsay D. Nelson or Christopher J. Patrick.

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Nelson, L.D., Patrick, C.J., Collins, P. et al. Alcohol impairs brain reactivity to explicit loss feedback. Psychopharmacology 218, 419–428 (2011). https://doi.org/10.1007/s00213-011-2323-3

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