Epidemiological studies reveal that one of the most reliable predictors of whether an adolescent or young adult will use drugs is whether his or her friends use drugs (Wills and Cleary, 1999; Bahr et al., 2005; Simons-Morton and Chen, 2006; Tompsett et al., 2013; Barnett et al., 2014; Schuler et al., 2019). Consequently, drug use among an individual’s peers represents a major vulnerability factor determining whether an individual will use drugs and develop a substance use disorder. Theoretical approaches to explain the high concordance rate of drug use among peers have focused on the roles of (1) selection, in which an individual self-selects peers based on shared interests (e.g., drug use), and (2) social learning, in which peers establish and maintain drug use amongst one another via associative learning mechanisms (see reviews by Kandel, 1986; Andrews and Hops, 2010; Pandina et al., 2010 further discussion of selection and socialization theories). Although these theoretical approaches are not mutually exclusive, only the latter lends itself to behavioral interventions that may reduce drug use among vulnerable populations.

Social learning models of drug use posit that drug use is established and maintained by contingencies operating in an individual’s social environment (Akers, 1977; Strickland and Smith, 2014). For instance, drug use is established by observing and modeling the behavior of a peer using drugs, and drug use is maintained by social reinforcement provided by the peer. This reinforcement could be in the form of verbal encouragement or simply by continued access to the peer. Unfortunately, empirical support for the role of social learning in drug use is limited. Ethical constraints limit the degree to which drug use, particularly illicit drug use, can be modeled and reinforced in humans, and animal models, particularly those that use intravenous drug self-administration, have traditionally been limited by the necessity of testing animals in isolation.

Recently, several studies have described the use of modified operant conditioning chambers that permit one or more animals to intravenously self-administer drugs in proximity to a social partner, which has rapidly advanced our understanding of how social contact can increase or decrease drug intake. For instance, these studies have shown that drug intake is increased in the presence of a partner self-administering drugs (Smith, 2012; Smith et al., 2014; Robinson et al., 2016, 2017), drug intake is decreased in the presence of a partner without access to drugs (Smith, 2012; Smith et al., 2014; Peitz et al., 2013; Robinson et al., 2016, 2017), patterns of drug intake between partners become more similar over time (Lacy et al., 2014), and subjects will maintain voluntary abstinence when given a choice between drugs and access to a social partner (Venniro et al., 2018, 2019, 2021). Importantly, social contact serves as a positive reinforcer in laboratory animals, and contingent access to a social partner can establish responding in experimentally naïve rats (Angermeier, 1960) and maintain rates of responding similar to those of consummatory reinforcers (e.g., food; Evans et al., 1994). The extent to which social reinforcement increases drug intake in these models has not been examined.

The aim of this study was to establish an animal model in which drug intake is positively reinforced by access to a social partner. To this end, male rats were implanted with intravenous catheters and trained to self-administer cocaine in modified operant conditioning chambers in which a solid guillotine door could be opened to an adjacent compartment housing either a social partner or a non-social (i.e., negative control) stimulus behind a metal screen. Once cocaine self-administration was established, the guillotine door was activated, and cocaine intake was reinforced by brief access to either the social or non-social stimulus. We predicted that cocaine intake would be greater in the social than non-social condition, thus supporting a role for social reinforcement in the facilitation of drug use.

All rats responded on the first day of cocaine availability, receiving approximately 9 infusions per session (Figure 1: Sessions –5 to –1). The number of reinforcers was consistent over 5 consecutive days in which responding was maintained by cocaine, and no differences were observed between rats that would later by assigned to the social and non-social conditions (no main effect of group, main effect of session, or group × session interaction was observed).

Cocaine intake was selectively impacted by the social stimulus when operant contingencies changed and responding resulted in opening the guillotine door (Figure 1: Sessions 1 to 10). Cocaine intake progressively increased in rats in the social partner condition [main effect of session: F(9,171) = 4.691, p < 0.001], resulting in significantly greater cocaine intake in this group relative to rats in the non-social condition [main effect of group: F(1,19) = 5.530, p = 0.030]. In contrast, cocaine intake did not increase in the non-social condition [group × session interaction: F(9,171) = 1.984, p = 0.044], resulting in significant between-group differences in cocaine intake during sessions 6 through 10.

Across a 100-fold dose range, cocaine intake was characterized by an inverted, U-shaped dose-effect curve in both groups (Figure 2), with ascending and descending limbs converging at 0.1 mg/kg [main effect of dose: F(4,76) = 15.851, p < 0.001]. Across all doses, cocaine intake ranged from 2- to 3-fold higher in the social group than in the non-social group [main effect of group: F(1,19) = 13.421, p = 0.002]. Importantly, responding was greater in the social than non-social group during a saline substitution test [t(19) = 9.661, p = 006], reflecting the differential reinforcing effects of the social/non-social stimuli in the absence of cocaine.

The dose-effect curve was redetermined after reducing the magnitude of the social and non-social stimuli (Figure 3). Reducing the duration of door opening from 30 to 5 s did not impact the dose-effect curve in either group (compare Figures 2 and 3). Similar to the original determination, cocaine intake was characterized by an inverted, U-shaped dose-effect curve [main effect of dose: F(4,76) = 13.793, p < 0.001], and intake ranged from 2- to 3-fold greater in the social than non-social group [main effect of group: F(1,19) = 11.647, p = 0.003]. Responding was also greater in the social than non-social group during a saline substitution test [t(19) = 5.191, p = 034].

Following determinations of the cocaine dose-effect curve, conditions were switched (Figure 4), such that rats in the original social condition were switched to the non-social condition (i.e., partners were switched for socks), and rats in the original non-social condition were switched to the social condition (i.e., socks were switched for partners). Cocaine intake increased across 10 consecutive sessions [main effect of session: F(9,144) = 4.326, p < 0.001], and this was driven by selective increases in intake in the new social group [group × session interaction: F(9,144) = 2.645, p = 0.007]. Cocaine intake was significantly less in the new social group during the first session, but the groups did not differ during the final nine sessions. Notably, cocaine intake remained high and stable in the new non-social group, reflecting the persisting effects of exposure to the social stimulus.

This study used a novel preclinical model to determine whether access to a social partner positively reinforces cocaine self-administration and thus facilitates cocaine intake. We found that contingent access to a social partner, but not a non-social stimulus, rapidly increases cocaine intake resulting in a 2- to 3-fold escalation of cocaine intake relative to both baseline and control conditions. These data emphasize the importance of social peers in the escalation of drug intake and demonstrate the role of social reinforcement in vulnerability to drug abuse.

Responding was under control of both reinforcers. Lever pressing was readily established with cocaine, and cocaine intake in both groups was characterized by an inverted, U-shaped dose-effect curve, which is typical of responding maintained by cocaine on simple FR schedules of reinforcement (Lynch and Carroll, 2001). Lever pressing increased rapidly when the social stimulus was introduced, both at the beginning of the study in the original social group, and toward the end of the study in the non-social group after the stimulus switch. Moreover, twice as many reinforcers were obtained during a saline substitution test in the social group than the non-social group, revealing the effects of the social contingency in the absence of cocaine. Finally, it is notable that high doses of cocaine markedly reduced responding relative to vehicle (i.e., saline) control values, thus functioning as a positive punisher to reduce responding otherwise maintained by social contact.

Recent studies have used several experimental designs to examine how social contact interacts with drug reward. For instance, studies using the conditioned place preference procedure report that social contact increases the conditioned rewarding effects of a drug if the stimuli are conditioned in the same compartment (Thiel et al., 2008; Reyna et al., 2021). In contrast, social contact can block the conditioned rewarding effects of a drug if social contact is provided exclusively in the opposite compartment (Fritz et al., 2011; Zernig and Pinheiro, 2015). Drug self-administration studies demonstrate the presence of a partner that is also self-administering drugs enhances drug intake, whereas the presence of a partner that is not self-administering drugs inhibits drug intake (Smith, 2012; Robinson et al., 2016). Unlike the present study, the presence of the partner was not contingent on drug intake in those previous studies. Finally, a social partner can inhibit drug intake in a discrete-choice procedure when selection of that partner specifically excludes drug delivery (Venniro et al., 2018, 2019).

Several behavioral mechanisms have been used to explain how drug use may be established and maintained among peers, and they include classic learning phenomena such as imitation/modeling, social reinforcement, emulation, social facilitation, local enhancement, stimulus enhancement, and reinforcement enhancement (Strickland and Smith, 2014). Although this study was not designed to systematically test all possible mechanisms, the current data may be used in conjunction with data collected previously to rule out several possibilities. Explanations based on imitation/modeling, emulation, local enhancement, and stimulus enhancement require a model to be engaged in behavior that increases a subject’s attention to (or engagement with) a discriminative stimulus, behavioral action, or reinforcing stimulus. Social partners did not have access to either response levers or intravenous cocaine, thus limiting their ability to increase the salience of any component of the lever-press/cocaine infusion contingency. Social facilitation or reinforcement enhancement represent two potential explanations for these findings, but multiple studies report the presence of a non-intoxicated social partner reliably decreases drug intake across a range of experimental conditions (Smith, 2012; Peitz et al., 2013; Smith et al., 2014; Robinson et al., 2016, 2017; Venniro et al., 2018, 2019, 2021). The experimental design of the present study specified that social contact was contingent on pressing a response lever and self-administering cocaine; consequently, social reinforcement reflects the most parsimonious explanation for the observed findings, especially after other explanations are ruled out. Importantly, the non-social (i.e., negative control) condition ruled out the possibility that extraneous components of the reinforcing stimulus (e.g., guillotine door opening, presence of novel stimulus) was responsible for the escalation of cocaine intake.

One observation that questions the role of social reinforcement in the maintenance of elevated responding is that cocaine intake was not responsive to either a reduction in the magnitude of the social stimulus (i.e., a decrease in the duration of social access) or the removal of the social stimulus (i.e., replacing a social partner for an athletic sock). Previous studies examining social reinforcement reveal that greater social contact (visual plus partial physical contact > only visual contact; Angermeier, 1960) and greater social deprivation (longer deprivation > shorter deprivation; Achterberg et al., 2016) increase the reinforcing effects of social contact. We do not know of any studies that manipulated the duration of social contact when measuring social reinforcement; however, studies using conditioned place preference report that longer durations of social contact do not lead to greater reward (10 min contact = 30 min contact; Thiel et al., 2008). In the present study, the elevated levels of cocaine intake in the social group were remarkably stable and not responsive to further manipulations, including the removal of the social stimulus. These data suggest that other behavioral mechanisms were also recruited to produce long lasting increases in drug intake that were resilient to further behavioral manipulations. This observation is of translational concern because it indicates that once drug use increases in response to social reinforcement from others, it will persist even in the absence of those individuals and may be less responsive to some first-line psychosocial interventions.

Collecting additional measures of behavior would help identify the mechanisms contributing to the differences in responding between social and non-social conditions. For instance, responding on an inactive lever would reveal the degree to which a social partner increased general levels of activity. Alternatively, the presence of a second active lever that resulted in only cocaine delivery (or only social access) would determine the preference for each stimulus individually relative to the compound stimulus. Furthermore, the presence of a second active lever that resulted in a different stimulus (e.g., sucrose, electric shock) would determine the extent to which social contact could differentially reinforce behaviors maintained at high rates (e.g., food-maintained responding) versus low rates (e.g., shock-maintained responding). Our hypothesis would be that the effects of social reinforcement would generalize broadly to other behaviors, particularly those maintained at low rates (Herrnstein, 1961).

We did not collect within-session patterns of responding or videotape the rats during test sessions. In the former case, we made a programming error that prevented the creation of cumulative records; in the latter case, video cameras were not available to us at the time of data collection. Consequently, we do not know the extent to which the subjects interacted with the social and non-social stimuli, nor do we know the nature of the interaction (e.g., active exploratory, passive avoidance). Relating the temporal pattern of lever-pressing to behaviors emitted during the 30-s stimulus presentation would provide further insight into the mechanisms responsible for the stimulus control of cocaine self-administration.

Females should be tested in future iterations of this model, especially when considering that male and female adolescents respond differently to social pressure on measures of drug use (Dick et al., 2007; Schulte et al., 2009; Mason et al., 2014; McMillan et al., 2018). An additional area ripe for investigation involves the effects of male-female interactions on measures of drug intake. There is nothing about the present model that would prevent the use of sexually mature male and female subjects as social partners, including female subjects during various phases of behavioral estrous. Although sex is frequently included as a biological variable in behavioral assays, interactions with the opposite sex are frequently ignored outside of studies specifically examining courtship/mating behavior.

The experimental design intentionally limited cocaine intake by restricting cocaine availability. Levers were retracted during periods of social/non-social stimulus presentation to encourage engagement with the reinforcing stimuli, and sessions were limited to 60 min to prevent satiation of the social stimulus. Limited access procedures do not model problematic patterns of drug intake that characterize addictive behavior (Smith, 2020), so data from this study are more translationally relevant to social drug use than drug abuse and addiction. This study also only examined the effects of social reinforcement on intravenous cocaine self-administration. Future studies must examine other drugs and routes of administration, particularly drugs and routes of administration that are more relevant to adolescent and young adult populations (e.g., oral alcohol consumption, inhaled nicotine/cannabinoid consumption).

The most obvious translational implication of this study is that social reinforcement escalates cocaine use, identifying it as a vulnerability factor for drug abuse and addiction. Prevention programs for at-risk groups (e.g., younger adolescents involved in predelinquent behavior) should target group norms that are permissive or even encouraging of drug use. Alternatively, it is equally likely that abstinence-related behaviors (e.g., attending school, involvement in religious and community activities, showing up for work) could be differentially reinforced by non-drug rewards, including social activities with abstinent individuals. Community reinforcement programs often make use of social reinforcement (e.g., integrating the person in a social network that engages in non-drug recreational activities) to encourage abstinence, and these programs have higher success rates than standard-care control groups (see review by Meyers et al., 2011). This could easily be modeled in future studies by using a differential reinforcement of other behavior (DRO) schedule in which social reinforcement is contingent on behavior that excludes drug self-administration. Indeed, previous studies have successfully modeled “voluntary abstinence” by providing rats with a discrete choice between drug delivery and social contact after a history of drug self-administration. Those studies reveal that social contact decrease drug intake, prevents the incubation of craving, and decreases measures of relapse in both males and females (Venniro et al., 2017, 2019).

This study describes a preclinical model in which cocaine self-administration is positively reinforced by contingent access to either a social (age- and sex-matched rat) or non-social (black-and-white athletic sock) stimulus. Contingent access to a social partner rapidly increased cocaine intake 2- to 3-fold across an extensive dose range. These increases in cocaine intake were persistent over time and resistant to later reductions in and removal of the social stimulus. Data collected in this model suggest that social reinforcement may contribute to the escalation of drug intake among peers and represents a vulnerability factor that may be particularly resistance to psychosocial interventions once established.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The animal study was reviewed and approved by Davidson College Animal Care and Use Committee.

MS conceived the study and wrote the manuscript. HC, AG, and JS collected the data. MS and JS analyzed the data. All authors approved the final draft and are accountable for the work.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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