Blunted expected reward value signals in binge alcohol drinkers

Serenella Tolomeo (Lead / Corresponding author), Alex Baldacchino, J. Douglas Steele

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Abstract

Alcohol-related morbidities and mortality are highly prevalent, increasing the burden to societies and health systems with 3 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, modeled using temporal difference theory with an expected reward value (ERV) linked to craving. Clinically, although 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 nonalcohol 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 (nonalcohol 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. A 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, modeled using temporal difference theory with ERV linked to craving. Here, we used an instrumental learning task with non-alcohol-associated stimuli to test hypotheses that the encoding of nonalcohol cue signals (ERV) and reward prediction error signals showed blunting in binge alcohol drinkers. We conclude that fMRI can be used to noninvasively test allostasis and associative learning theory predictions in binge drinkers.

Original languageEnglish
Pages (from-to)5685-5692
Number of pages8
JournalJournal of Neuroscience
Volume43
Issue number31
Early online date30 Jan 2023
DOIs
Publication statusPublished - 2 Aug 2023

Keywords

  • Amygdala-hippocampal complex
  • binge drinking
  • model-based fMRI
  • prediction error signal
  • orbitofrontal
  • reinforcement learning
  • value

ASJC Scopus subject areas

  • General Neuroscience

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