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Published in final edited form as: Exp Clin Psychopharmacol. 2023 Sep 14;32(3):255–262. doi: 10.1037/pha0000679

Response-Contingent Cocaine Increases the Reinforcing Effectiveness of Social Contact

Mark A Smith 1, Jacob D Camp 1, Alexandra N Johansen 1, Justin C Strickland 2
PMCID: PMC10937325  NIHMSID: NIHMS1923495  PMID: 37707472

Abstract

Epidemiological studies report a high concordance rate of drug use within groups, suggesting an interplay between drug reinforcement and social cohesion. Preclinical studies reveal that (1) contingent access to a social partner increases cocaine intake and (2) experimenter-delivered cocaine increases the reinforcing effects of social contact. The purpose of this study was to determine if response-contingent cocaine increases the reinforcing effectiveness of social contact. Male rats were implanted with intravenous catheters and trained on a fixed ratio (FR1) schedule for 30-s access to a social partner. The reinforcing effectiveness of social contact was then determined using a progressive ratio (PR) schedule. After the PR test, rats were divided into two groups in which each response on an FR1 schedule produced social access and either response-contingent cocaine (0.5 mg/kg/infusion) or saline. After nine days, the reinforcing effectiveness of social contact in the absence of infusions was determined again on the PR schedule. The cocaine and saline reinforcers were then switched between groups and the latter procedures were repeated. Recent exposure to response-contingent cocaine increased the reinforcing effectiveness of social contact on the PR schedule. This effect was transient, and the reinforcing effectiveness of social contact returned to baseline levels once response-contingent cocaine was replaced with saline. These data indicate that recent exposure to response-contingent cocaine transiently increases the reinforcing effectiveness of social contact and suggest that cocaine use may strengthen social cohesion by increasing the reinforcing effects of social contact with other individuals.

Keywords: addiction, progressive ratio, social behavior, social learning, substance use

Epidemiological studies reveal a high concordance rate of drug use within groups. This effect is consistent within familial (Biederman et al., 2000; Chassin et al., 1996) and peer groups (Alves et al., 2021; Bahr et al., 2005; Ramirez et al., 2012), as well as between close acquaintances (e.g., best friends, Schinke et al., 2008; Schuler et al., 2019; Sieving et al., 2000; Urberg, 1992) and intimate partners (Bartel et al., 2017; Desrosiers et al., 2016; Etcheverry and Agnew, 2008). The close correspondence in drug use within these groups suggest an interplay between social factors contributing to social cohesion and behavioral factors contributing to drug use. Not surprisingly, several theoretical models based on self-selection and socialization have been proposed to explain these high concordance rates (e.g., Andrews and Hops, 2010; Kandel, 1986; Pandina et al., 2010).

Preclinical studies have explored some of the mechanisms that may contribute to drug use within groups. For instance, rats prefer (i.e., self-select) social partners with a similar cocaine history as themselves (Smith et al., 2015) and choose to self-administer cocaine in close proximity to another rat self-administering cocaine (Smith and Pitts, 2014). Rats also acquire cocaine self-administration more rapidly and have higher levels of cocaine intake in the presence of a social partner that also self-administers cocaine (Peitz et al., 2013; Robinson et al., 2017; Smith, 2012; Smith et al., 2014a). Moreover, patterns of cocaine self-administration between members of social dyads become more similar over time (Lacy et al., 2014), suggesting that social learning processes related to modeling and imitation may be operating in laboratory settings.

Preclinical evidence suggests social contact and drugs may mutually reinforce one another, functioning to increase both social cohesion and drug use within groups. For instance, response-contingent social contact increases cocaine intake by greater than 50% (Smith et al., 2021) on a fixed ratio (FR1) schedule of reinforcement, suggesting that contingent access to a social partner reinforces cocaine use. Moreover, experimenter-delivered cocaine enhances the reinforcing efficacy of social contact on a progressive ratio (PR) schedule (Sharp and Smith, 2021), suggesting a reciprocal relationship between the reinforcing effects of social contact and cocaine.

We note, however, the relationship between drugs and social contact is subject to procedural variables and sensitive to parametric manipulations. For instance, remifentanil intake is reduced when social contact is available in a forced-choice procedure, and this effect is sensitive to changes in schedule of reinforcement, duration of social access, peer familiarity, and housing condition (Chow et al., 2022). These and other recent findings are contributing to a rapidly growing body of literature on the relationship between social factors and drug self-administration (see Pelloux et al., 2019 for review).

The purpose of this study was to determine whether response-contingent cocaine administration increases the reinforcing effectiveness of social contact. As such, we tested the hypothesis that responding maintained by social contact on a PR schedule would be elevated following exposure to a social-cocaine compound stimulus operating on an FR1 schedule relative to a control group that was not exposed to cocaine. Withingroup manipulations involving the timing of the introduction of the cocaine stimulus and its removal were also performed; these latter manipulations were included for exploratory purposes to determine whether the effects of response-contingent cocaine were dependent on behavioral history and/or sensitive to reversal.

Method

Subjects

Twenty male, Long-Evans rats were obtained at ~7 weeks of age from Charles River Laboratories (Raleigh, NC) and housed individually in a colony room maintained under a 12-hr light/dark cycle. Except during the period of lever-press training (see below), food and water were provided ad libitum. Additionally, each experimental rat was assigned one age-matched male partner to serve as the reinforcing social stimulus throughout testing. All procedures were approved by the Davidson College Animal Care and Use Committee and followed the guidelines described in the Guide for the Care and Use of Laboratory Animals (Institute for Laboratory Animal Research, 2011). Sample size was determined from previous studies (Sharp and Smith, 2021; Smith et al., 2021). This study was not preregistered.

Materials

Experimental events took place in operant conditioning chambers from Med Associates, Inc. (St. Albans, VT, USA). Each chamber contained a houselight, a retractable response lever, a stimulus light located above the response lever, and a guillotine door leading to a smaller, adjacent compartment housing a social partner (Figure 1). The two compartments were separated by a metal screen affixed to the wall of the main chamber that covered the opening and permitted full visual, auditory, and olfactory contact, as well as limited tactile contact between the two rats, but prevented each subject from traversing to the opposite compartment (Sharp and Smith, 2021). Cocaine HCl was obtained from Sigma-Aldrich (St. Louis, MO, USA).

Figure 1. Operant Conditioning Chamber for Drug and Social Reinforcement.

Figure 1.

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Overhead (upper panel) and side (lower panel) view of interior of the operant conditioning chamber showing an experimental rat and its social partner.

Lever-Press Training

Rats were restricted to 90% of the free-feeding body weight via light food restriction and trained to lever press on an FR1 schedule of food reinforcement over the course of 5 days as described previously (Strickland et al., 2016).

Surgery

After lever-press training, rats were implanted with intravenous catheters into the right jugular vein under isoflurane anesthesia as described previously (Smith et al., 2021).

Social Partnering

One day before testing commenced, each experimental rat was partnered with one, age-matched peer that would serve as the social stimulus during testing. A single partnering session occurred during which the two rats were placed together in a neutral cage and allowed unlimited social interaction for 15 min. The stimulus rat that was partnered with a given experimental subject served as the social reinforcer for the that subject for the duration of testing.

Behavioral Procedure

Sessions 1–5.

Behavioral testing commenced one day after social partnering. An FR1 schedule was used to establish responding reinforced by social contact and to introduce response-contingent cocaine later in the experiment. Prior to each session, a social partner was placed in the adjacent side compartment of each operant conditioning chamber (Figure 1). Sessions began with illumination of the house light and opening of the guillotine door to allow noncontingent access to the social partner. After 30 s, the guillotine door closed, the retractable lever was inserted into the chamber, and the stimulus light above the response lever was illuminated. For the remainder of the session, each lever press resulted in retraction of the lever, turning off the stimulus light, and opening of the guillotine door. After 30 s of social access, the guillotine door closed, the retractable lever was reinserted, and the stimulus light was reilluminated. These conditions remained in effect for the remainder of the session. Test sessions terminated automatically after 60 min. No infusions were delivered during these initial sessions.

Session 6.

The reinforcing effectiveness of social contact was assessed on a PR schedule. Similar to the initial FR sessions, each PR test began with illumination of the house light and opening of the guillotine door to allow noncontingent access to the social partner. After 30 s, the guillotine door closed, the retractable response lever was inserted into the chamber, and the stimulus light above the response lever was illuminated. For the remainder of the session, responding was reinforced on a PR schedule of reinforcement in which the ratio value systematically increased following each reinforcer: 1, 3, 6, 9, 12, 17, 24, 32, 42, 56, 73, 95, 124, 161, 208, and 268. The session terminated when 60 min elapsed before a reinforcer was delivered. All other conditions were as described for Sessions 1–5.

Sessions 7–15.

After the initial PR test, experimental rats were divided into two groups that were matched according to average number of daily reinforcers earned during the initial five FR sessions. Matching the two groups based on responding on the FR schedule ensured the two groups had similar baseline rates of responding prior to introducing the compound stimulus that included response-contingent cocaine or saline. For both groups, each response on an FR1 schedule delivered the social stimulus according to the conditions described above and a simultaneous infusion of either 0.5 mg/kg cocaine (Group A) or saline (Group B). Under these conditions, each lever press resulted in retraction of the lever, turning off the stimulus light, opening of the guillotine door, and activation of the infusion pump that delivered the intravenous infusion of cocaine or saline. Activation of the infusion pump did not interfere with the opening of the guillotine door, nor did opening of the guillotine door interfere with activation of the infusion pump and subsequent infusion.

Session 16.

After nine consecutive sessions in which responding was reinforced with social contact and an intravenous infusion of either cocaine or saline, the reinforcing effectiveness of social contact was redetermined on the PR schedule. All conditions during this test were as described for the PR test conducted during Session 6. No infusions were delivered during this test.

Sessions 17–24.

After the PR test, stimulus conditions were switched between the two groups. Group A, which initially received response-contingent cocaine, then received response-contingent saline, whereas Group B, which initially received response-contingent saline, then received response-contingent cocaine (0.5 mg/kg/infusion). Otherwise, all conditions were as described for Sessions 7–15.

Session 25.

After eight consecutive sessions in which responding in each group was reinforced with the new stimulus, the reinforcing effectiveness of social contact was redetermined on the PR schedule. All conditions during this test were as described for the previous PR tests. No infusions were delivered during this test.

Schedule of Testing.

Rats were run concurrently, and testing was conducted across consecutive days with two exceptions: (1) a one-day break was scheduled after Session 6, permitting time off for the research technicians, and (2) a three-day break was scheduled after Session 16, corresponding to a long holiday weekend.

Data Analysis

Any rat that lost catheter patency before the conclusion of testing (i.e., Session 25) was removed from the study and its data were not included in the statistical analysis.

Data from each block of testing on the FR1 schedule were operationalized as number of reinforcers (i.e., social contacts) and analyzed via a linear mixed effect model with group serving as a between-subjects predictor and session serving as a linear repeated-measure predictor. Main effects and interactions were evaluated through effect coding. Interactions were followed with linear mixed effect models within each group. Data from the PR tests were operationalized as the number of reinforcers (i.e., social contacts) and initially analyzed via repeated-measures ANOVA for each group, followed be paired-samples t-tests. Data collected during each PR session were also compared between groups using independent-samples t-tests. Finally, breakpoints were analyzed by collapsing across groups and comparing data obtained during analogous sessions (i.e., baseline, after cocaine, after saline). These latter data were analyzed via repeated-measures ANOVA followed by paired-samples t-tests. All statistical tests used a twotailed alpha level of .05.

All raw data from this study are included in Supplemental File 1. Statistical outputs from all linear mixed effect models are included in Supplemental File 2.

Results

All rats responded on the first day in which social access was available on the FR1 schedule, and responding showed no increasing or decreasing trends across days. Importantly, no differences were apparent in rats that would be transitioned to cocaine versus rats that would be transitioned to saline (Figure 2A: Sessions 1–5). Breakpoints maintained by social contact on a PR schedule did not differ between groups prior to the introduction of the compound stimulus (Figure 2B: Session 6).

Figure 2. Response-Contingent Cocaine and the Reinforcing Effects of Social Contact.

Figure 2.

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A: Number of reinforcers obtained on a fixed ratio (FR1) schedule during 60-min test sessions. Circles represent data collected from Group A that was reinforced with 30-s access to a social partner only (Sessions 1–5: white), social access + 0.5 mg/kg cocaine (Sessions 7–15: black), and social access + saline (Sessions 17–24: gray). Triangles represent data collected from Group B that was reinforced with 30-s access to a social partner only (Sessions 1–5: white), social access + saline (Sessions 7–15: gray), and social access + 0.5 mg/kg cocaine (Sessions 17–24: black). B: Responding maintained by social contact on a PR schedule in the absence of response-contingent infusions in Groups A and B during Sessions 6, 16, and 25. Left axis depicts breakpoints as number of reinforcers obtained; right axis depicts total number of responses emitted. White bars represent data obtained prior to response-contingent cocaine or saline. Black bars represent data following recent exposure to response-contingent cocaine. Gray bars represent data following recent exposure to response-contingent saline. Asterisks (*) indicate significant difference relative to baseline. Pound signs (#) indicate significant difference relative to Session 25 (Group A) or Session 16 (Group B). At sign (@) indicates significant difference between Groups A and B. C: Responding maintained by social contact on a PR schedule in the absence of response-contingent infusions. Left axis depicts breakpoints as number of reinforcers obtained; right axis depicts total number of responses emitted. White bar represents data obtained prior to response-contingent cocaine or saline. Black bar represents data following recent exposure to response-contingent cocaine. Gray bar represents data following response-contingent saline. Asterisk (*) indicates significant different relative to baseline. Pound sign (#) indicates significant difference relative to data collected following recent exposure to response-contingent saline. For all panels, n = 20.

A significant Session × Group interaction was observed when cocaine (Group A) or saline (Group B) was introduced as a compound stimulus on the FR1 schedule (Figure 2A, Sessions 7–15; group by session interaction: b = 2.47, p = .001). Follow-up testing in the cocaine compound stimulus group showed a nonsignificant decrease of approximately one reinforcer per session (b = −1.10, p = .055), whereas the saline compound stimulus group showed a significant increase of approximately one reinforcer per session (b = 1.37, p = .006). No main effect of group was observed. Relative to breakpoints obtained during Session 6, breakpoints maintained by social contact in Session 16 increased significantly in rats that received response-contingent cocaine during the previous nine sessions (t(10) = 2.725, p = .021, d = 0.822) but not in rats that received response-contingent saline (Figure 2B, Session 16). During this PR test, rats that previously received response-contingent cocaine had significantly greater breakpoints than rats that previously received response-contingent saline (t(18) = 2.940, p = .009, d = 1.320

The type of infusion (cocaine vs. saline) was switched between the two groups in Session 17, such that rats previously exposed to response-contingent cocaine were then exposed to response-contingent saline, and vice versa. Responding was elevated during the first two sessions in both groups following the pause in testing and stimulus switch (see Method: Behavioral Procedure: Schedule of Testing) before leveling off for the final six sessions (Figure 2A: Sessions 17–24: main effect of session: b = −2.25, p < .001). No differences were observed between the two groups across the eight sessions on the FR1 schedule. Relative to breakpoints obtained during Sessions 6 and 16, breakpoints maintained by social contact in Session 25 increased significantly in rats that received response-contingent cocaine during the previous eight sessions (Figure 2B: Session 25: t(8) = 2.774, p = .024, d = 0.925; t(8) = 6.782 p < .001, d = 2.261, respectively). In contrast, breakpoints maintained by social contact decreased significantly in rats that switched from response-contingent cocaine to response-contingent saline (t(10) = 2.480 p = .033, d = 0.748). In the latter group, breakpoints maintained by social contact during Session 25 did not differ from those obtained during Session 6, prior to the introduction of the compound stimulus.

Data from Groups A and B were collapsed to further examine breakpoints maintained by social contact on a PR schedule following recent exposure to response-contingent cocaine and response-contingent saline (Figure 2C). When data were collapsed in this manner, breakpoints maintained by social contact were significantly greater following recent exposure to response-contingent cocaine relative to data obtained during baseline (t(19) = 3.955 p < .001, d = 0.884) and relative to data obtained following recent exposure to response-contingent saline (t(19) = 5.119 p < .001, d = 1.145). The increase in breakpoints following exposure to response-contingent cocaine reflected an increase of ~40 total responses relative to the other two conditions.

Discussion

The purpose of this study was to determine whether response-contingent cocaine increases the reinforcing effectiveness of social contact. Providing response-contingent cocaine did not alter responding maintained by social contact on an FR1 schedule; however, response-contingent cocaine on the FR1 schedule subsequently increased the reinforcing effectiveness of social contact as determined on a PR schedule in the absence of cocaine. These effects were transient, and the reinforcing effectiveness of social contact returned to baseline conditions once response-contingent cocaine was substituted with response-contingent saline.

It is notable that responding on the FR1 schedule was not impacted by the addition of response-contingent cocaine. The dose of cocaine used (0.5 mg/kg/infusion) falls on the descending limb of the dose-effect curve (e.g., Caine et al., 2004; Smith et al., 2013; Strickland et al., 2016), and lower and higher doses of cocaine would be expected to increase and decrease responding on the FR1 schedule, respectively (Morgan et al., 2009; Wise et al., 1995; Zimmer et al., 2013, 2011). Although the single-dose design of the study was a limitation, the failure of this dose to alter responding on the FR1 schedule was advantageous, in that both groups received equal exposure to the response-reinforcer contingency, and both groups received equal pairings of the compound stimulus. This had the effect of avoiding potential confounds that would otherwise be present with asymmetrical histories of response-reinforcer and stimulus-stimulus exposures. Regardless, testing multiple doses of cocaine in future studies remains important because the acute effects of noncontingent cocaine on breakpoints maintained by social contact are dose dependent, producing a linear increase as a function of dose (Sharp and Smith, 2021). Consequently, a recent history of response-contingent cocaine would be expected to produce similar dose-dependent effects under the conditions described in this study.

Multiple mechanisms may be responsible for the increased reinforcing effectiveness of social contact following response-contingent cocaine on the PR schedule (Strickland and Smith, 2014); however, several of these potential mechanisms are unlikely. Some drugs function as reinforcing enhancers, meaning they acutely increase the reinforcing effectiveness of other reinforcers (for example and discussion, see Donny et al., 2003). Experimenter-delivered cocaine acutely increases the reinforcing efficacy of social contact, likely via its ability to increase synaptic concentrations of dopamine (Sharp and Smith, 2021). This potential mechanism can be ruled out, given that cocaine was not administered within 23 hours of the PR test session. A “cocaine-seeking” response, which would be attributed to a persistence of responding at the onset of extinction and after removal of the cocaine stimulus is unlikely, given that responding during the PR sessions was (1) greater than that observed when cocaine was available on the FR1 schedule and (2) greater than that reported in previous studies from our laboratory in which cocaine was maintained on a PR schedule and then replaced with saline (e.g., Smith et al., 2014b, 2013, 2008). Other mechanisms derived from social learning theory (e.g., imitation, stimulus enhancement, etc.) are similarly unlikely because they require the social partner to be performing the same or similar operant response as the experimental subject (see Strickland and Smith, 2014).

Repeated presentations of the social/cocaine compound stimulus likely led to the development of a Pavlovian association between the two stimuli. This is relevant because social contact and drugs can confer their reinforcing effects to other stimuli via Pavlovian associative processes (Arroyo et al., 1998; Donny et al., 2003; Goldberg et al., 1981; Lehner et al., 2016; Neiberg, 1964; Schenk and Partridge, 2001). Importantly, these effects are transient and can be extinguished by removing the unconditioned stimulus during subsequent training trials and thus breaking the Pavlovian association (Arroyo et al., 1998; Goldberg et al., 1981; Stimbert, 1970). In the present study, the increase in reinforcing effectiveness of social contact was eliminated and returned to that observed during baseline conditions once cocaine was replaced with saline. The inclusion of additional control groups, such as a group receiving explicitly unpaired presentations of cocaine and the social stimulus, could further elucidate the behavioral mechanisms responsible for the observed effects; however, this group was explicitly not included because of lethality associated with noncontingent infusions of cocaine (Dworkin et al., 1995). Other control conditions, such as providing contingent cocaine on an FR schedule but non-contingent social contact on a variable time schedule, may be of value, but confounds related to asymmetrical durations of stimulus exposure between pharmacological (non-discrete and dependent on half-life) and nonpharmacological (discrete and programmed by the experimenter) stimuli would need to be addressed.

Additional experimental groups could also shed light on the Pavlovian associations that develop between cocaine and social contact. For example, initial training with cocaine prior to training the social stimulus would be expected to weaken the later development of a Pavlovian association between the two stimuli via latent inhibition processes. Studies such as these would meaningfully advance the current literature on contextual cues and substance use (for reviews, see Crombag et al., 2008; Taylor et al., 2009).

A number of limitations of this study should be addressed in future research. For instance, only male subjects were used, and future studies should include females and mixed-sex dyads. We previously reported that males and females are similarly sensitive to the acute reinforcing-enhancing effects of noncontingent cocaine on social contact (Sharp and Smith, 2021), but similar studies in mixed-sex dyads have not been conducted. As noted above, one limitation of the study was the lack of a dose-response analysis for cocaine. A similar limitation is that the magnitude of the social reinforcer was not varied. A previous study reported that the reinforcing effects of social contact are sensitive to the duration of social access and peer familiarity (Chow et al., 2022), suggesting that quantitative and qualitative dimensions of social contact determine its reinforcing effectiveness. Finally, we used a model in which behavior was relatively stable across sessions. Extended-access and intermittent-access procedures reliably increase drug intake on both FR and PR schedules of reinforcement, and future studies should address if similar procedures might produce analogous effects on responding maintained by social contact.

As noted above (see Introduction), there is growing evidence that social contact and drug use may produce mutually reinforcing effects. The finding that response-contingent cocaine increases the reinforcing effectiveness of social contact supports this possibility and identifies one factor contributing to the high concordance rate of drug use within peer groups. These data support the use of animal models that incorporate the social environment in the study of drug use.

Supplementary Material

Supplemental Material 1
Supplemental Material 2

Public Significance Statement.

One of the most reliable predictors of drug use is whether an individual’s peers use drugs. This study examined whether response-dependent cocaine increases the motivation for social contact. We report that response-dependent cocaine transiently increases the motivation for social contact, suggesting that cocaine use may increase social cohesion under some conditions.

Disclosures and Acknowledgements

This work was supported by the National Institutes of Health (grant numbers DA045364 and DA031725 to MAS). The NIH had no role in study design; in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.

All authors contributed in a significant way to the study and approved the final manuscript prior to submission.

Footnotes

The authors have no conflicts of interest to report.

Data from this study have not been disseminated previously.

All original data are included with this manuscript in a supplemental file.

This study was not preregistered.

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