Neural representation of prediction error signals in substance users

Abstract

Abnormal decision making can result in detrimental outcomes of clinical importance, and decision making is strongly linked to neural prediction error signalling. Activation likelihood estimation (ALE) meta‐analyses were used to examine the neural correlates of prediction error signals of individuals taking different types of substances and healthy controls with contrast and conjunction analyses. Twenty‐eight studies were included in the meta‐analysis, representing 424 substance users' individuals and 834 healthy control individuals. Robust brain activity associated with prediction error signals in substance users was found for the bilateral striatum and insula. Healthy control subjects also activated bilateral striatum, midbrain, right insula and right medial‐inferior frontal gyrus. Compared with healthy controls, substance users showed blunted activity in the bilateral putamen, right medial‐inferior frontal gyrus and insula. The current meta‐analysis of cross‐sectional findings investigated neural prediction error signals in substance users. PE abnormalities in substance users might be related to poor decision making. In conclusion, the present study helps identify the pathophysiological underpinnings of maladaptive decision making in substance users.

Translational models of addiction phenotypes to advance addiction pharmacotherapy

“…74 Overall, a recent meta-analysis of 28 studies of RPE studies in substance-using populations found that while substance users robustly activate the striatum and insula during RPEs, they show blunted activation in the putamen, inferior frontal gyrus, and right insula, relative to controls. 75 Differences in findings between and across substance-using populations may also be attributed to the satiation state of the population, (i.e., acute abstinence, active use, and acute use 76 ) and by belief or expectation state. 77,78 While understanding the neural mechanisms underlying RPEs and decision-making in SUDs holds promise for furthering treatment and medication development, few studies have directly used RPE tasks or models to evaluate pharmacological or psychosocial treatments.…”

“…However, another study found that during cocaine deprivation, individuals with a cocaine use disorder had heightened neural RPE activity in the striatum, which mediated the relationship between chronicity of substance use and the desire to use cocaine 74 . Overall, a recent meta‐analysis of 28 studies of RPE studies in substance‐using populations found that while substance users robustly activate the striatum and insula during RPEs, they show blunted activation in the putamen, inferior frontal gyrus, and right insula, relative to controls 75 . Differences in findings between and across substance‐using populations may also be attributed to the satiation state of the population, (i.e., acute abstinence, active use, and acute use 76 ) and by belief or expectation state 77,78 …”

Evaluating instrumental learning and striatal–cortical functional connectivity in adolescent alcohol and cannabis use

“…4,15 A recent meta-analysis has also indicated that substance use more broadly is characterized by reduced representation of a range of prediction error signals (covert factors of learning) in both striatal and lateral prefrontal regions. 16 To our knowledge, only one study has examined functional relationships among striatal and cortical regions during instrumental learning in the context of substance use. 17 There, adults with alcohol use disorder demonstrated weaker functional connectivity between ventral striatal and dlPFC regions during an instrumental learning task, as well as behaviour consistent with slower learning of instrumental contingencies (i.e., cue-action-outcome associations) relative to adults without this disorder.…”

“…Regarding frontoparietal regions, fMRI findings have indicated reduced representation of reward prediction error (RPE) and expected value signals (covert factors of reinforcement learning models) by brain activations in these regions during instrumental learning associated with adolescent alcohol and/or cannabis use 4,15 . A recent meta‐analysis has also indicated that substance use more broadly is characterized by reduced representation of a range of prediction error signals (covert factors of learning) in both striatal and lateral prefrontal regions 16 …”

Abnormal prediction error processing in schizophrenia and depression

“…For example, a previous meta-analysis by Garrison and colleagues reported prediction error signals encoded in the striatum and insula (Garrison, Erdeniz, & Done, 2013). A recent metaanalysis on the neural representation of prediction error signals in substance users concluded that substance users showed blunted activity in the striatum, medial-frontal gyrus, and insula in comparison with controls (Tolomeo, Yaple, & Yu, 2020). With respect to the neuroimaging data in schizophrenia and depression, inconsistencies have been reported.…”