Substance-use disorders remain resistant to most forms of clinical treatment. Although preclinical studies have identified many interventions that reliably decrease drug-seeking behavior in laboratory animals, only occasionally have they predicted successful outcomes in clinical trials. One common criticism of preclinical models is that most do not capture the complex social environment in which substance use occurs. The predictive validity of these models might be improved by incorporating relevant features of the social environment known to influence substance use.
Several investigators have recently introduced new models, or refined existing models, to capture aspects of the social environment that may influence drug-seeking behavior. Using the conditioned place preference procedure, a procedure in which a Pavlovian association is formed between a stimulus (eg, interoceptive drug cue, social partner) and a distinct environmental context, investigators have shown that drugs (eg, cocaine, nicotine) and social contact mutually enhance one another’s rewarding effects when paired together (Thiel et al, 2009). Alternatively, social contact prevents and reverses a conditioned place preference for cocaine if the two are conditioned in separate contexts, and social contact reverses cocaine-induced increases in the transcription factor, Zif268, in the nucleus accumbens, amygdala, and ventral tegmental area (Fritz et al, 2011).
Advances in traditional drug self-administration procedures are also allowing investigators to determine how the presence of a social partner influences drug intake. For instance, research with prairie voles, a socially monogamous species, has shown that alcohol intake decreases in the presence of a low-consumption social partner (Anacker et al, 2011). Our laboratory recently developed custom-built, operant conditioning chambers that permit two rats to intravenously self-administer drugs simultaneously in the same chamber. We reported that the acquisition of cocaine self-administration is facilitated in the presence of a partner that is also self-administering cocaine (Smith et al, 2014) and the maintenance of cocaine self-administration is inhibited in the presence of a partner that does not have access to cocaine (Robinson et al, 2016). Interestingly, under conditions in which both partners have access to cocaine, individual patterns of cocaine intake become progressively more similar over time (Lacy et al, 2014). These studies suggest a number of behavioral mechanisms by which social contact may influence drug use. For instance, under conditions in which substance use is a group norm, group members may model drug use and selectively reinforce the drug use of others through social approval/acceptance. In contrast, under conditions in which abstinence is a norm, drug use may be selectively punished through social rejection, and group members may model and differentially reinforce abstinence-related behaviors (see review by Strickland and Smith, 2014 for further examples and discussion).
The development of these animal models will significantly advance our understanding of the neurobiological mechanisms mediating the effects of social contact on substance use. Similar to the reinforcing effects of drugs, the reinforcing effects of social contact are dependent on dopamine transmission within the nucleus accumbens (Manduca et al, 2016), suggesting that this site may be a neuroanatomical locus in which information about social contact and drugs converge to mutually influence one another’s rewarding effects. Consistent with this hypothesis, microinjection of the endogenous neuropeptide oxytocin into the nucleus accumbens increases social contact and affiliation (Yu et al, 2016), and reduces drug self-administration and other measures of drug-seeking behavior (Baracz et al, 2016).
The discovery that information about drugs and the social environment converge on a common neurobiological locus furthers our understanding of preclinical, human laboratory, and epidemiological research showing that social contact can modify the reinforcing effects of drugs. This knowledge may also explain the past failure of preclinical studies (which artificially constrain the social environment) to consistently predict clinical trial outcomes (which generally do not control the social environment). By incorporating relevant features of social contact into our preclinical models, we should be able to better identify which interventions will successfully translate into clinical practice.
Funding and disclosure
Work on this paper was funded by NIH Grant DA031725. The authors declare no conflict of interest.
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Smith, M., Strickland, J. Modeling the Impact of Social Contact on Substance Use. Neuropsychopharmacol 42, 364 (2017). https://doi.org/10.1038/npp.2016.218