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Research Articles, Behavioral/Cognitive

Blunted Expected Reward Value Signals in Binge Alcohol Drinkers

Serenella Tolomeo, Alex Baldacchino and J. Douglas Steele
Journal of Neuroscience 30 January 2023, JN-RM-2157-21; DOI: https://doi.org/10.1523/JNEUROSCI.2157-21.2022
Serenella Tolomeo
1Institute of High Performance Computing, Agency for Science, Technology and Research (A*STAR), Singapore, Singapore;
2Department of Pharmacology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore;
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Alex Baldacchino
3Division of Population and Behavioral Science, Medical School, University of St Andrews, United Kingdom;
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J. Douglas Steele
4Division of Imaging Science and Technology, Medical School, University of Dundee, United Kingdom.
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Abstract

Alcohol-related morbidities and mortality are highly prevalent increasing the burden to societies and health systems, with three million deaths globally each year in young adults directly attributable to alcohol. Cue induced alcohol craving has been formulated as a type of aberrant associative learning, modelled using temporal difference theory with expected reward value (ERV) linked to craving. Clinically, whilst harmful use of alcohol is associated with increased time spent obtaining and using alcohol, it is also associated with self-neglect. The latter implies that the motivational aspects of non-alcohol stimuli are blunted. Using an instrumental learning task with non-alcohol related stimuli, here we tested hypotheses that the encoding of cue signals (ERV) predicting reward delivery would be blunted in binge alcohol drinkers in both sexes. We also predicted that for the binge drinking group alone, ratings of problematic alcohol use would correlate with abnormal ERV signals consistent with between groups (i.e. binge drinkers vs controls) abnormalities. Our results support our hypotheses with the ERV (non-alcohol cue) signal blunted in binge drinkers and with the magnitude of the abnormality correlating with ratings of problematic alcohol use. This implies that consistent with hypotheses, the motivational aspects of non-alcohol related stimuli are blunted in binge drinkers. Better understanding of the mechanisms of harmful alcohol use will, in time, facilitate the development of more effective interventions, which should aim to decrease the motivational value of alcohol and increase the motivational value of non-alcohol related stimuli.

SIGNIFICANCE STATEMENT:

Allostasis theory predicts specific abnormalities in brain function and subjective experiences that occur when people develop drug problems including addiction. Cue induced alcohol craving has been formulated as a type of aberrant associative learning, modelled using temporal difference theory with expected reward value (ERV) linked to craving. Here we used an instrumental learning task with non-alcohol associated stimuli to test hypotheses that the encoding of non-alcohol cue signals (ERV) and reward prediction error (RPE) signals showed blunting in binge alcohol drinkers. We conclude that fMRI can be used to non-invasively test allostasis and associative learning theory predictions in binge drinkers.

Footnotes

  • The funding sources played no part in the design of the study, analyses and interpretation of the data, nor manuscript preparation. The authors have no competing financial interests. The authors declare no financial or other conflicts of interest with regard to this work.

  • This work was supported by Dundee University Medical School Grant Number AT27 to ST and JDS. Spectroscopy was supported by an unrestricted work in progress agreement with Siemens Healthcare AG. We thank Dr Kent Berridge for comments on an earlier version of this manuscript.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Blunted Expected Reward Value Signals in Binge Alcohol Drinkers
Serenella Tolomeo, Alex Baldacchino, J. Douglas Steele
Journal of Neuroscience 30 January 2023, JN-RM-2157-21; DOI: 10.1523/JNEUROSCI.2157-21.2022

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Blunted Expected Reward Value Signals in Binge Alcohol Drinkers
Serenella Tolomeo, Alex Baldacchino, J. Douglas Steele
Journal of Neuroscience 30 January 2023, JN-RM-2157-21; DOI: 10.1523/JNEUROSCI.2157-21.2022
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