Effects of dopamine and opioid receptor antagonism on the neural processing of social and nonsocial rewards

Abstract

Rewards are a broad category of stimuli inducing approach behavior to aid survival. Extensive evidence from animal research has shown that wanting (the motivation to pursue a reward) and liking (the pleasure associated with its consumption) are mostly regulated by dopaminergic and opioidergic activity in dedicated brain areas. However, less is known about the neuroanatomy of dopaminergic and opioidergic regulation of reward processing in humans, especially when considering different types of rewards (i.e., social and nonsocial). To fill this gap of knowledge, we combined dopaminergic and opioidergic antagonism (via amisulpride and naltrexone administration) with functional neuroimaging to investigate the neurochemical and neuroanatomical bases of wanting and liking of matched nonsocial (food) and social (interpersonal touch) rewards, using a randomized, between-subject, placebo-controlled, double-blind design. While no drug effect was observed at the behavioral level, brain activity was modulated by the administered compounds. In particular, opioid antagonism, compared to placebo, reduced activity in the medial orbitofrontal cortex during consumption of the most valued social and nonsocial rewards. Dopamine antagonism, however, had no clear effects on brain activity in response to reward anticipation. These findings provide insights into the neurobiology of human reward processing and suggest a similar opioidergic regulation of the neural responses to social and nonsocial reward consumption.

Keywords: dopamine; fMRI; food; opioids; reward; social touch.

FIGURE 1

Trial sequence of the reward task. Participants could obtain social and nonsocial rewards in three levels (high, low, very low). Social rewards consisted of skin‐to‐skin caresses delivered to the forearm from a trained same‐gender confederate at three speeds: 6, 21, and 27 cm/s. Nonsocial rewards consisted of milk with three different concentrations of cocoa: chocolate milk, a 4:1 mix of milk and chocolate milk, and milk. At the beginning of each trial, a cue announced the attainable reward (high or low), and participants were asked to rate their wanting of the announced reward. Then, participants exerted effort by squeezing a hand dynamometer to obtain the announced reward. The applied force, displayed via online visual feedback, was expressed as percentage of the participants' maximum voluntary contraction (MVC, measured immediately before the task) and translated into the probability of obtaining the announced reward (0%–100%). The obtained reward was then announced (high, low, or very low in case of low effort) and delivered. Following a relaxation phase, participants rated their liking of the stimulus. At the end of nonsocial trials, participants received water to rinse their mouth.

FIGURE 2

No significant drug effects on the ratings of (a) wanting and (b) liking. (c) Ratings of wanting did not differ for food and touch, but (d) ratings of liking were higher for low food rewards compared to low touch rewards (p = .04), regardless of the drug group. *p < .05. The violin plots depicted here consist of box plots, representing the median (thick horizontal line), the interquartile range (box), and the lower/upper adjacent values (whiskers) and kernel density plots, representing kernel probability density of the data at different values. AMI, amisulpride; NAL, naltrexone; PLA, placebo.

FIGURE 3

No significant drug effects on the effort exerted (% of maximum voluntary contraction, MVC) to obtain rewards of different (a) levels (high, low) and (b) types (food, touch). (c) Effort exerted also did not differ for food and touch, regardless of the drug group. The violin plots depicted here consist of box plots, representing the median (thick horizontal line), the interquartile range (box), and the lower/upper adjacent values (whiskers), and kernel density plots, representing kernel probability density of the data at different values. AMI, amisulpride; NAL, naltrexone; PLA, placebo.

FIGURE 4

Brain regions showing greater activity during high compared to low reward (a) anticipation and (b) consumption (GLM.3) in the placebo group. (c) Reduced activity in the medial orbitofrontal cortex following naltrexone (Nal) administration compared to placebo (Pla) during reward consumption (GLM.3). (d) Reduced activity in middle frontal and precentral gyri, thalamus, and caudate following amisulpride (Ami) administration compared to placebo (Pla) during reward consumption (GLM.3). Images are thresholded at p < .001 uncorrected.