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RationalSmoking typically begins during adolescence or early adulthood in a social context, yet the role of social context in animal models is poorly understood. Objectives
The present study examined the effect of social context on acquisition of nicotine self-administration. Methods
Sixty-day-old male and female Sprague-Dawley rats were trained to...
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... Studies using rodent models have shown that the social context of drug use might impact drug effects, acquisition, seeking, or relapse [40,53]. In the case of nicotine, it has been demonstrated that the presence of a social partner facilitates nicotine self-administration in adolescent male rats, suggesting that a social context enhances the initial reinforcement effects of nicotine [41]. ...
Adolescents exhibit great sensitivity to nicotine and social interaction; accordingly, when both stimuli are presented together, they interact to enhance the incentive value of the context in which they occur. Noteworthy, most studies assessing the interaction between nicotine and social reward have used isolated-reared rats. Adolescent isolation is an adverse condition that impacts brain development and behavior, so it is not known if the interaction also occurs in rats without social deprivation. The present study used a conditioned place preference model (CPP) to examine the interaction between nicotine and social reward in group-reared male adolescent rats. At weaning, Wistar rats were randomly assigned to four groups: vehicle, vehicle and a social partner, nicotine (0.1mg/Kg s.c.), and nicotine and a social partner. Conditioning trials occurred on eight consecutive days followed by a test session in which the preference change was assessed. Besides the establishment of CPP, we examined the effects of nicotine on (1) social behaviors during CPP trials and (2) tyrosine hydroxylase (TH) and oxytocin (OT) as markers of changes in the neuronal mechanisms for reward and social affiliation. Similar to previous results, the joint presentation of nicotine and social reward induced CPP, whereas either nicotine or social interaction presented alone did not. This finding coincided with an increase in TH levels observed after nicotine administration only in socially conditioned rats. The interaction between nicotine and social reward is not related to the effects of nicotine on social investigation or social play.
... Finally, it is worth noting that the study was conducted with male rats. Previous research has demonstrated differential effects of social isolation between females and males on drugrelated behavior (Cheeta et al., 2001;McCormick et al., 2004;Peartree et al., 2017). More studies are needed to explore the effects of social isolation on nicotine effects in adolescent female subjects to gain a better understanding of the interplay between adolescence, social isolation, and nicotine addiction. ...
Adolescent social conditions profoundly affect vulnerability to drug abuse. Preclinical studies have shown that preventing social interactions during adolescence increases the rewarding effects of drugs like alcohol, cocaine, or amphetamines, however, little data exist regarding the impact of social isolation on nicotine effects. The current study evaluated the effects of differential rearing conditions during adolescence (isolation or group rearing) on (1) conditioned place preference induced by low nicotine doses (0.1 or 0.3 mg/kg) and (2) sensitization to the locomotor effects of nicotine after sub-chronic administration (3) and accumulation of ΔFosB in nucleus accumbens (NAc). Results showed that nicotine induced place preference in isolated and grouped rats, but the effect was more persistent for the rats reared in isolation. Isolated reared rats also exhibited lower levels of ΔFosB accumulation in NAc. No differences were found in the behavioral sensitization to nicotine effects between rearing conditions. The results suggest that isolation engenders a more robust incentive value of nicotine-related contexts. This effect could be related to the basal expression of ΔFosB: lower levels of this transcription factor seem to impair the motivation of isolated reared rats and increase their vulnerability to the effects of drugs like nicotine.
... Estrous cycle phases were determined by daily vaginal cytology (Becker et al., 2005;Byers et al., 2012) using the procedures described in Peartree et al. (2017). ...
Background: Previous research showed that the 5-HT 1B receptor agonist CP94253 enhanced cocaine reinforcement rate during maintenance of daily self-administration (SA), but inhibited reinforcement rate after 21 days of abstinence in male rats. Here we examined whether female rats show similar effects of CP94253 during maintenance as males across estrous cycle phases.
Methods: Female rats trained on a fixed ratio 5 (FR5) cocaine reinforcement schedule were tested for the effects of CP94253 (5.6 mg/kg, s.c.) on cocaine reinforcement rate during each phase of the estrous cycle, with access to either low (0.075 and 0.1875) or high (0.375 and 0.75) cocaine doses available for 1 h sequentially in descending dose order. Other female and male rats trained on a progressive ratio (PR) schedule of cocaine or sucrose reinforcement were tested for CP94253 (0, 3.2, 5.6, and 10 mg/kg, s.c.) effects on reinforcement rate in 3-h sessions. CP94253 effects on responding during sucrose cue-reactivity were also examined post-abstinence.
Results: Regardless of sex, CP94253 enhanced breakpoints on the PR schedule during maintenance of cocaine SA but attenuated breakpoints for sucrose reinforcement and decreased responding during sucrose cue-reactivity. FR results showed that CP94253 attenuated cocaine reinforcement rate during all estrous cycle phases except metestrus.
Conclusions: Overall, we suggest that CP94253 increased incentive motivation for cocaine during maintenance of SA in female and male rats, yet decreased motivation for sucrose. We also suggest that 5-HT 1B Rs modulate motivation similarly across sexes except when females are in metestrus.
... For example, it has been reported that rats tested with a drug-experienced partner were faster to acquire cocaine self-administration (Gipson et al., 2011;Smith et al., 2014), and social learning facilitated nicotine self-administration (Chen et al., 2011). Although physical isolation is required to preserve the intravenous catheters used for drug delivery, these studies used specially constructed operant chambers that isolated individual rats but allowed limited social contact via either a mesh (Peartree et al., 2017) or several small windows (Chen et al., 2011). ...
The social environment has long been recognized to play an important role in substance abuse disorders (SUD). Operant conditioning is the most widely used rodent model of SUD. However, most operant chambers do not accommodate more than one rat at a time. Here, we introduce PeerPub; a novel social operant chamber. PeerPub uses a touch sensor to record the number of licks on drinking spouts. It then delivers a drop of solution with a fixed volume as the reward to the tip of the spout when the number of licks meets the requirement of a reinforcement schedule. A radio-frequency identification (RFID) chip implanted on top of each rat's skull tracks the identity of the rat. The system is controlled by a Raspberry Pi computer. We tested PeerPub using male Wistar Kyoto rats in daily one-hour sessions where supersac, a solution containing glucose and saccharin, was delivered under a fixed ratio 5 schedule. We found that male rats consumed more supersac in group housing rather than in isolated conditions. These data demonstrated the utility of PeerPub in modeling the interaction between motivated behavior and social context. We anticipate devices like PeerPub will help demonstrate the role of the social environment in SUD phenotypes. The design of PeerPub is available at http://github.com/nijie321/PeerPub .
... Most experiments have been conducted on adult males but increasing studies are comparing the influence of sex or development stages. Social isolation initially reduces self-administration of nicotine in males, but enhances nicotine intake during later sessions especially in females (Peartree et al., 2017). Adolescent Sprague-Dawley rats female rats consumed more sweetener-supplemented alcohol in isolation than when group-housed while in the same studies adolescent and adult male consume more alcohol in triads versus when isolate-housed (Varlinskaya et al., 2015). ...
... Marked sex differences have been found in the acquisition and maintenance of selfadministration for other drugs of abuse (see review by Roth et al., 2004), however, few studies have utilized behavioral economics to examine sex differences (Grebenstein et al., 2013). As well, inconsistent sex differences in acquisition of nicotine self-administration and intake have been found for rodents, which may be dose-and reinforcement schedule-dependent (Chaudhri et al., 2005;Donny et al., 2000;Feltenstein et al., 2012;Peartree et al., 2017;Swalve et al., 2016). ...
... Similarly, Elliott and Grunberg found that physical or social enrichment reduced habituation time in an open field task, and therefore increased information-processing, in males compared to females (Elliott and Grunberg, 2005). Alternatively, nicotine intake during acquisition can be enhanced in males, but not females, during the initial self-administration training session when a social partner is introduced (Peartree et al., 2017). The results seen here indicate that housing environment may induce differential effects on nicotine demand intensity and elasticity by sex, and that a within-session dose-reduction protocol can detect such differences. ...
... Most experiments have been conducted on adult males but increasing studies are comparing the influence of sex or development stages. Social isolation initially reduces self-administration of nicotine in males, but enhances nicotine intake during later sessions especially in females (Peartree et al., 2017). Adolescent Sprague-Dawley rats female rats consumed more sweetener-supplemented alcohol in isolation than when group-housed while in the same studies adolescent and adult male consume more alcohol in triads versus when isolate-housed (Varlinskaya et al., 2015). ...
This review aims to demonstrate how social science and behavioral neurosciences have highlighted the influence of social interactions on drug use in animal models. In neurosciences, the effect of global social context that are distal from drug use has been widely studied. For human and other social animals such as monkeys and rodents, positive social interactions are rewarding, can overcome drug reward and, in all, protect from drug use. In contrast, as other types of stress, negative social experiences facilitate the development and maintenance of drug abuse. However, interest recently emerged in the effect of so-called "proximal" social factors, that is, social interactions during drug-taking. These recent studies have characterized the role of the drug considered, the sharing of drug experience and the familiarity of the peer which interaction are made with. We also examine the few studies regarding the sensorial mediator of social behaviors and critically review the neural mediation of social factors on drug use. However, despite considerable characterization of the factors modulating distal influences, the mechanisms for proximal influences on drug use remain largely unknown.
... Indomethacin is a broad spectrum NSAID that inhibits cyclooxigenase (Cox)-1 and -2 activity, although hippocampal mRNA expression of Cox-1 and -2 was not modified under our experimental conditions. The use only of male mice is a limitation of this study since several reports show evidences for sex differences in the central effects of nicotine in rodent models Peartree et al., 2017). Although social factors are crucial in smoking dependence in humans, differences in the pharmacokinetic properties of nicotine or the effect of gonadal hormones may underlie some of the sex differences observed (Pogun and Yararbas, 2009). ...
Nicotine withdrawal is associated with cognitive deficits including attention, working memory, and episodic memory impairments. These cognitive deficits are a hallmark of nicotine abstinence which could be targeted in order to prevent smoking relapse. The underlying mechanisms, however, are poorly understood. In this study, memory impairment was observed in mice 4 days after the precipitation of nicotine withdrawal by the nicotinic antagonist mecamylamine. The presence of cognitive deficits correlated with microglial activation in the hippocampus and the prefrontal cortex. Moreover, an increased expression of neuroinflammatory markers including IL1β, TNFα and IFNγ was found in both memory-related brain regions. Notably, flow cytometric analysis also revealed an enhancement of TNFα and IFNγ plasmatic levels at the same time point during nicotine withdrawal. Impaired neurogenesis, as shown by reduction in the expression of the endogenous cell proliferation marker Ki67 and the early neuron marker doublecortin, was also associated with nicotine abstinence. Treatment with the non-psychoactive cannabinoid cannabidiol abolished memory impairment of nicotine withdrawal and microglia reactivity, reduced the expression of IL1β and IFNγ in the hippocampus and the prefrontal cortex, respectively, and normalized Ki67 levels. The nonsteroidal anti-inflammatory drug indomethacin also prevented cognitive deficits and microglial reactivity during withdrawal. These data underline the usefulness of anti-inflammatory agents to improve cognitive performance during early nicotine abstinence.
... A more recent study examining social context in the acquisition and maintenance of nicotine self-administration found that social interaction among pair-housed males transitioning into adulthood enhances the initial reinforcing effects of nicotine during the early phases of acquisition. However, this social interaction appears to protect against nicotine intake during the later sessions of nicotine self-administration, which is more pronounced in females (Peartree et al., 2017). Thus, age and sex are likely important factors that shape the modulatory role of social influence over nicotine-seeking behavior. ...
Cigarette smoking is the leading preventable cause of death in the United States. The number of new smokers, specifically among adolescents, has risen rapidly in recent years. Thus, understanding the role of social influences on patterns of nicotine and tobacco use is important. Clinical studies have addressed the impact social relationships such as family members and peers have on smoking acquisition and susceptibility. As well, preclinical animal models have examined the impact of social factors on drug intake, acquisition, maintenance, and relapse. For example, environmental enrichment (EE) is a multi-faceted model that includes social factors, exercise, and novelty, among others. This model has elucidated addiction-related neurobehavioral effects of these different factors. However, there is a dearth of literature examining the impact of social partners on nicotine addiction and underlying neural mechanisms. Here we discuss the importance of social factors on nicotine addiction vulnerability, and propose new directions for addiction research that integrate social aspects of nicotine use.
... Donny et al. 32 showed that nicotine intake was similar between males and females but the motivation to obtain nicotine was higher in females (no effect of estrous cycle). More recently, Peartree et al. 33 showed that a social context enhances the initial reinforcing effects of nicotine in males, but protects against nicotine intake during later sessions especially in females (again, estrous cycle had no effect). We have shown that in adolescent Sprague-Dawley rats, there was no sex difference in nicotine IVSA using either a 23-h access paradigm (lever pressing) 34 or the socially acquired model 8 . ...
Both social environment and genetic factors are critical for smoking initiation and nicotine addiction. We reported that rats developed conditioned flavor (i.e., taste and odor) aversion to intravenously self-administered (IVSA) nicotine, and that social learning promoted nicotine IVSA with flavor cues. We thus tested the hypothesis that socially acquired nicotine IVSA is a heritable trait by using female rats of six inbred strains and six F1 hybrids. Each strain was tested for 10 daily IVSA sessions. We found that the intake of nicotine (15 and 30 μg/kg/inf) varied among these strains by 33.7–56.6-fold. The heritability of nicotine intake was estimated to be 0.54–0.65. Further, there was a strong correlation in nicotine intake (R² = 0.85, p < 0.0001) between the two nicotine doses. Another cohort of rats was given three daily IVSA sessions followed by five sessions that tested conditioned flavor aversion. Nicotine intake was highly correlated with the extinction of the conditioned aversion (R² = 0.58, p < 0.005). These data showed that nicotine intake in the socially acquired nicotine self-administration model is controlled by genetic factors and that the role of social learning is likely in facilitating the extinction of conditioned aversive response to nicotine.
