A meta‐analysis of the neural substrates of monetary reward anticipation and outcome in alcohol use disorder

Abstract

The capacity to anticipate and detect rewarding outcomes is fundamental for the development of adaptive decision‐making and goal‐oriented behavior. Delineating the neural correlates of different stages of reward processing is imperative for understanding the neurobiological mechanism underlying alcohol use disorder (AUD). To examine the neural correlates of monetary anticipation and outcome in AUD patients, we performed two separate voxel‐wise meta‐analyses of functional neuroimaging studies, including 12 studies investigating reward anticipation and 7 studies investigating reward outcome using the monetary incentive delay task. During the anticipation stage, AUD patients displayed decreased activation in response to monetary cues in mesocortical‐limbic circuits and sensory areas, including the ventral striatum (VS), insula, hippocampus, inferior occipital gyrus, supramarginal gyrus, lingual gyrus and fusiform gyrus. During the outcome stage, AUD patients exhibited reduced activation in the dorsal striatum, VS and insula, and increased activation in the orbital frontal cortex and medial temporal area. Our findings suggest that different activation patterns are associated with nondrug rewards during different reward processing stages, potentially reflecting a changed sensitivity to monetary reward in AUD.

Neural response to threat and reward among young adults at risk for alcohol use disorder

“…The family history positive group reported feeling less nervous during the anticipation of winning money relative to earning no money, compared to the family history negative group. These results are consistent with the findings of a recent meta‐analysis 11 that found that individuals with alcohol use disorder demonstrated less neural activation in several reward and incentive brain regions, including the ventral striatum, during anticipation of reward and receipt of reward during the MID task. Zeng and colleagues 11 posit that decreased activation in these regions among individuals with alcohol use disorder indicates dysfunction in incentive salience to conventional rewards (e.g., money).…”

“…A region often associated with anticipation of negative outcomes is the anterior insula 12,13 . Numerous studies have examined the neural response of adults with AUD during anticipation of winning money, 14,15 and a meta‐analysis of these studies indicated consistent reductions in activation of the nucleus accumbens among adults with AUD relative to healthy adults 11 . Adults with greater levels of harmful alcohol use showed enhanced startle response during a task with a potentially negative outcome (i.e., a shock) 16 and adults with, relative to without, AUD showed increased activation in the anterior insula during the same task 17 .…”

“…12,13 Numerous studies have examined the neural response of adults with AUD during anticipation of winning money, 14,15 and a meta-analysis of these studies indicated consistent reductions in activation of the nucleus accumbens among adults with AUD relative to healthy adults. 11 Adults with greater levels of harmful alcohol use showed enhanced startle response during a task with a potentially negative outcome (i.e., a shock) 16 and adults with, relative to without, AUD showed increased activation in the anterior insula during the same task. 17 As these studies show, adults with AUD demonstrate altered neural responses to potential positive and negative outcomes, raising the possibility that these neural alterations may be present prior to the onset of AUD.…”

“…6 One of the brain regions most commonly associated with the anticipation of reward is the nucleus accumbens, 7 whereas the medial prefrontal cortex (mPFC) responds to the actual receipt of monetary reward. [8][9][10][11] A region often associated with anticipation of negative outcomes is the anterior insula. 12,13 Numerous studies have examined the neural response of adults with AUD during anticipation of winning money, 14,15 and a meta-analysis of these studies indicated consistent reductions in activation of the nucleus accumbens among adults with AUD relative to healthy adults.…”

Non‐abstinent recovery in alcohol use disorder is associated with greater regional cortical volumes than heavy drinking

“…Similarly, smaller fusiform gyri differentiated RH only from LN. Recent work demonstrated alterations within this region among AUD when anticipating natural rewards (i.e., money;Zeng et al, 2023). The fusiform gyrus is also known to play a role in emotional face processing, which has been shown to be impaired in AUD(Alba-Ferrara et al, 2016; Maurage et al, 2008).Diminished volume in this region may, therefore, correspond to deficits in emotion-and reward-processing dysfunction in those with AUD.…”