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Event-related potentials reflect impaired temporal interval learning following haloperidol administration

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Abstract

Background

Signals carried by the mesencephalic dopamine system and conveyed to anterior cingulate cortex are critically implicated in probabilistic reward learning and performance monitoring. A common evaluative mechanism purportedly subserves both functions, giving rise to homologous medial frontal negativities in feedback- and response-locked event-related brain potentials (the feedback-related negativity (FRN) and the error-related negativity (ERN), respectively), reflecting dopamine-dependent prediction error signals to unexpectedly negative events. Consistent with this model, the dopamine receptor antagonist, haloperidol, attenuates the ERN, but effects on FRN have not yet been evaluated.

Methods

ERN and FRN were recorded during a temporal interval learning task (TILT) following randomized, double-blind administration of haloperidol (3 mg; n = 18), diphenhydramine (an active control for haloperidol; 25 mg; n = 20), or placebo (n = 21) to healthy controls. Centroparietal positivities, the Pe and feedback-locked P300, were also measured and correlations between ERP measures and behavioral indices of learning, overall accuracy, and post-error compensatory behavior were evaluated. We hypothesized that haloperidol would reduce ERN and FRN, but that ERN would uniquely track automatic, error-related performance adjustments, while FRN would be associated with learning and overall accuracy.

Results

As predicted, ERN was reduced by haloperidol and in those exhibiting less adaptive post-error performance; however, these effects were limited to ERNs following fast timing errors. In contrast, the FRN was not affected by drug condition, although increased FRN amplitude was associated with improved accuracy. Significant drug effects on centroparietal positivities were also absent.

Conclusions

Our results support a functional and neurobiological dissociation between the ERN and FRN.

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Notes

  1. Uncorrected p values are reported for follow-up comparisons controlling for effects of overall accuracy.

  2. Repetition of this analysis with difference waves derived for fastest fast errors and slowest slow errors (as previously defined for response-locked ERP analysis) also revealed a main effect of electrode (F(1, 56) = 57.30, p < 0.001), as well as an interaction between electrode and error type (F(1, 56) = 6.34, p = 0.015) for peak FRN amplitude; main and interaction effects of group were also nonsignificant. A main effect of error type was noted with respect to FRN latency (F(1, 56) = 5.90, p = 0.018), with fastest fast error FRNs somewhat delayed relative to slowest slow error FRNs across all groups (t(58) = 2.34, p = 0.023); main and interaction effects with group were again nonsignificant for FRN latency.

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Acknowledgements

Dr. Forster was partially supported by funding from the VISN 4 Mental Illness Research, Education and Clinical Center (MIRECC, Director: D. Oslin; Pittsburgh Site Director: G. Haas), VA Pittsburgh Healthcare System. The contents do not represent the views of the Department of Veterans Affairs, Department of Defense, or the United States Government. We would like to thank Samuel Bartley for providing laboratory management support during data analysis and manuscript preparation.

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Authors and Affiliations

  1. Department of Psychological and Brain Sciences, Indiana University, Bloomington, IN, USA

    Sarah E. Forster, Patrick Zirnheld, Brian F. O’Donnell & William P. Hetrick

  2. VA Pittsburgh Healthcare System, VISN 4 MIRECC, University Drive C, Building 30, Pittsburgh, USA

    Sarah E. Forster & Stuart R. Steinhauer

  3. Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, USA

    Sarah E. Forster & Stuart R. Steinhauer

  4. Department of Psychiatry, Indiana University School of Medicine, Indianapolis, IN, USA

    Patrick Zirnheld, Anantha Shekhar, Brian F. O’Donnell & William P. Hetrick

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  1. Sarah E. Forster
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  2. Patrick Zirnheld
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  3. Anantha Shekhar
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  5. Brian F. O’Donnell
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Correspondence to Sarah E. Forster.

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All participants provided informed consent in accordance with the Indiana University–Purdue University Indianapolis Institutional Review Board.

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Forster, S.E., Zirnheld, P., Shekhar, A. et al. Event-related potentials reflect impaired temporal interval learning following haloperidol administration. Psychopharmacology 234, 2545–2562 (2017). https://doi.org/10.1007/s00213-017-4645-2

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