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. 2019 Aug 7;39(32):6354-6364.
doi: 10.1523/JNEUROSCI.0508-19.2019. Epub 2019 Jun 12.

Posterior Cingulate Cortical Response to Active Avoidance Mediates the Relationship Between Punishment Sensitivity and Problem Drinking

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Free PMC article

Posterior Cingulate Cortical Response to Active Avoidance Mediates the Relationship Between Punishment Sensitivity and Problem Drinking

Thang M Le et al. J Neurosci. .
Free PMC article

Abstract

Many people drink to alleviate negative affect, reflecting an avoidance strategy which can lead to alcohol misuse. Individuals with heightened sensitivity to punishment (SP) are especially susceptible to problem drinking via this maladaptive coping mechanism. As imaging studies have largely focused on sensation-seeking traits and approach behavior, the neural substrates underlying behavioral avoidance as well as their relationship with punishment sensitivity and alcohol use remain unclear. Here, we examined in humans the cerebral correlates of response inhibition to avoid a penalty in relation to both problem drinking and SP, as evaluated by the Alcohol Use Disorders Identification Test and the Sensitivity to Punishment and Sensitivity to Reward Questionnaire, respectively. Seventy nondependent female and male drinkers performed a reward go/no-go task with approximately two-thirds go and one-third no-go trials. Correct go and no-go responses were rewarded, and incorrect responses were punished. The results showed that SP and Alcohol Use Disorders Identification Test scores were both positively correlated with brain activations during response inhibition, and these activations overlapped in the posterior cingulate cortex (PCC). Thus, the PCC may represent a shared neural substrate for avoidance, punishment sensitivity, and problem drinking. Mediation analyses further suggested that PCC response to avoidance completely and bidirectionally mediated the relationship between SP and hazardous alcohol use. These findings substantiated the role of the PCC in behavioral avoidance and its link to problem drinking in punishment-sensitive nondependent drinkers.SIGNIFICANCE STATEMENT Many people drink to alleviate negative affect, reflecting an avoidance strategy that can lead to alcohol misuse. Individuals with heightened punishment sensitivity (SP) trait are particularly vulnerable to this maladaptive coping mechanism. The current study examined the neural substrates underlying behavioral avoidance and their relationship with SP and problem drinking. Using a reward go/no-go task, we showed both SP and drinking severity were positively correlated with the posterior cingulate cortex (PCC) activation during action inhibition. Thus, the PCC may represent a shared neural substrate for avoidance behavior, punishment sensitivity, and problem drinking. Further, PCC response to avoidance mediated the relationship between SP and alcohol use. These findings substantiated the neural processes linking avoidance tendency to alcohol misuse in punishment-sensitive drinkers.

Keywords: alcohol; avoidance; go/no-go; posterior cingulate cortex; problem drinking; punishment sensitivity.

Figures

Figure 1.
Figure 1.
Behavioral task and results. Participants performed a GNG task with the dollar reward on the left (A) or on the right (B), with the order counterbalanced across subjects. A, A successful go trial and failed no-go trial. B, A successful no-go and failed go trials. Fore-period varied from 1 to 5 s. Response window for go trials was titrated with data obtained from a prescan session to ∼85% success. Intertrial interval (ITI) was fixed at 3 s. Behavioral results (mean ± SE) showed the correct rate (C) and RT (D) across trial types. Correct rate was significantly higher for dollar than nickel go trials. The opposite pattern was observed for no-go trials. GS nickel trials showed slower RT than GS dollar trials. NGE nickel trials showed slower RT than NGE dollar trials. **p ≤ 0.001.
Figure 2.
Figure 2.
Pearson correlations show the relationship between personality traits and problem drinking across all subjects. Each data point represents one subject. AUDIT score was positively correlated with SP (A) but not SR (B).
Figure 3.
Figure 3.
A, AUDIT score positively modulated activity during inhibition of action in the dollar trials (NGS_dollar > GS_dollar) in the PCC and right middle frontal gyrus (MFG). B, SP score positively modulated activity during inhibition of action in dollar trials in the PCC, left insula (Ins), bilateral precentral gyrus (PrC), postcentral gyrus (PoC), paracentral lobule (PCL), and right thalamus/parahippocampal gyrus (Thal/PHG).
Figure 4.
Figure 4.
A, Overlapping voxels (yellow) in the PCC were identified from two contrasts involving AUDIT (green) and SP (red) correlations with activity for NGS dollar > GS dollar. PCC activity was positively correlated with (B) AUDIT and (C) SP scores across all subjects. D, Mediation analysis. Model 1: SP → AUDIT → PCC activity; Model 2: AUDIT → SP → PCC activity; Model: 3 SP → PCC activity → AUDIT; Model 4: AUDIT → PCC activity → SP; Model 5: PCC activity → SP → AUDIT; and Model 6: PCC activity → AUDIT → SP. Both Model 3 and Model 4 showed a significant and complete mediation effect. * p < .05, ** p < .01.

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