Neural mechanisms of sexual decision-making in women with alcohol use disorder

Abstract

Rationale: The co-occurrence of alcohol consumption and sexual activity is associated with increased risk for sexual assault, sexually transmitted disease, and unplanned pregnancy among young adult women with alcohol use disorder (AUD). There is considerable previous work demonstrating neural reactivity to alcohol cues in AUD. Because alcohol consumption and sexual behavior are both rewarding and tend to co-occur, sexual cues may produce similar neural reactivity in women with AUD, possibly indicating a shared mechanism underlying reactivity to both types of cues. Alternatively, reactivity to alcohol versus sexual cues may be distinct, suggesting domain-specific mechanisms.

Objectives: We investigated whether the decision vulnerabilities in AUD women regarding sexual activity were related to differences in brain activation compared to control women.

Methods: Women with (n = 15) and without (n = 16) AUD completed a hypothetical decision-making task during fMRI that presented low- or high-risk scenarios involving visual sexual, appetitive, and neutral cues.

Results: Results showed that sexual cues were more often endorsed by women with AUD compared to controls and elicited differential brain activation patterns in frontal, visual, and reward regions. During high-risk decisions, women with AUD failed to downregulate activation, causing hyperactivation compared to controls.

Conclusions: Visual sexual cues produced reactivity like that previously demonstrated for alcohol cues, suggesting a shared or domain-general mechanism for alcohol and sexual cue reactivity in women with AUD. Riskier sexual decisions in women with AUD may be a consequence of repeatedly pairing alcohol use and sexual activity, a characteristic behavior of this population.

Keywords: Alcohol use disorder; Alcohol use disorder reward networks; Co-sensitization; Cue reactivity; Decision-making; Female sexual risk; Incentive sensitization; fMRI.

Fig. 1

Sample stimuli and risk scenarios. Each panel is a single trial. The word ‘yes’ indicated low risk and ‘no’ indicated high risk. In sexual decisions the number indicated number of total sexual partners and the yes/no answered whether or not the individual had an STD. In food decisions the number referred to caloric content and the yes/no answered whether the food had passed health safety inspection. In item decisions the number referred to price and the yes/no answered whether or not the store had a return policy.

Fig. 2

Significant behavioral effects on endorsement likelihood, or the self-reported probability of participation in sexual activity. It can clearly be seen that risky sexual decision making is uniquely affected for the AUD population, shown by less reduction in endorsement likelihood. The main effect of risk is also apparent, with endorsements decreasing significantly for high risk decisions.

Fig. 3

Statistical map for high-risk sexual decisions minus low-risk sexual decisions. Specifically, the contrast (SEX^High-risk - SEX^Low-risk). Bar along the top indicates z-threshold values. a) Importantly, controls show widespread deactivation of limbic/reward and sensory regions in addition to key regions of the CEN, DMN, and SN. b) AUDs show a similar pattern but fail to deactivate DMN regions, some CEN regions, and some SN regions (e.g. left AIC). c) The difference map of AUD-Controls

Fig. 4

Statistical map for low risk sexual decisions minus low risk food and item decisions. Specifically, the contrast (SEX^Low-risk) - (FOOD^Low-risk + ITEM^Low-risk)]. Bar along the top indicates z-threshold values. In low risk, controls show widespread activation of key reward/limbic, visual, and decision making areas. Specifically, there is activation of the CEN, DMN, and SN. Some deactivation of the left fusiform is observed. AUDs show a similar but attenuated pattern of activation. c) The difference map of AUD-Controls

Fig. 5

Statistical map for sexual decisions minus food and item decisions. Specifically, the contrast 2 x (SEX^High-risk - SEX^Low-risk) - [(FOOD^High-risk - FOOD^Low-risk ) + (ITEM^High-risk - ITEM^Low-risk)]. Bar along the top indicates z-threshold values. It is clear that controls deactivate regions of the DMN, CEN, SN, reward regions, and visual regions whereas AUDs show attenuated deactivation in visual, DMN, and CEN regions. c) The difference map of AUD-Controls

Fig. 6

Results of post-hoc ROI analysis, the difference of high-lo risk for each condition shown in the bars. Red bars represent AUDs and blue represent controls. Standard error bars shown. a) ROI regions. Shaded coloration used to identify Harvard-Oxford ROIs, red indicates activations from AUDs > HCs contrast maps of sexual decisions. Blue shading represents left caudate, purple is left putamen, pale orange is frontal pole, yellow is medial prefrontal. b) In the putamen, an important reward processing region, AUD subjects fail to reduce activation in response to high-risk sexual decisions whereas controls show no difficulty. c) During high-risk sexual decisions, AUDs maintain high activation of the caudate, a region known to process both substance and natural reward. d) AUD subjects modulate their response to appetitive and neutral stimuli in the medial prefrontal cortex, but fail to modulate their response to high risk sexual decisions. e) In this important decision region, it is found that participants have an increased response to sexual decisions, and that AUD participants fail to modulate neural activation.