The Interaction of Ethanol Ingestion and Social Interaction with an Intoxicated Peer on the Odor‐Mediated Response to the Drug in Adolescent Rats

Abstract

Background Using a social transmission of food preference paradigm in rats, we previously demonstrated that ethanol exposure during adolescence, as either an observer (interaction with an intoxicated conspecific) or demonstrator (intragastric infusion with ethanol), altered the reflexive odor-mediated responses to the drug. The two modes of exposure were equivalent in the magnitude of their effects. Human adolescents, however, are likely to experience the drug in a social setting as both an ethanol observer and demonstrator. That is, both interacting with an intoxicated peer and experiencing ethanol’s post-ingestive consequences in conjunction with hematogenic olfaction. Therefore, we tested whether combined adolescent exposure as both an observer and demonstrator differed from either form of individual experience. Methods Beginning on postnatal day (P) 29, naïve rats received ethanol or water exposures in a social interaction paradigm as either an observer, a demonstrator or combined experience (where each animal in the interaction was, itself, an observer and demonstrator). Exposures occurred four times, once every 48 hours. On P37, the reflexive behavioral response to ethanol odor was tested, using whole-body plethysmography. Results The odor-mediated responses of adolescent ethanol observers, demonstrators and combined exposure animals all significantly differed from controls. Compared to controls, however, the magnitude of the behavioral effect was greatest in the combined exposure animals. Moreover, combined exposure as both an ethanol observer and demonstrator significantly differed from either form of individual ethanol experience. Conclusions Ethanol’s component chemosensory qualities are known to be central contributors to its acceptance and increases in the acceptability of ethanol’s odor, resulting from a social transmission experience, are predictive of enhanced ethanol avidity in adolescence. Our findings demonstrate that combined exposure as an observer and demonstrator, within a socially relevant framework, may represent a higher risk scenario for increased ethanol avidity in adolescence (and by extension adult persistence) as compared to the individual effects of direct ingestion or social experience with the drug.

Social Interaction With an Alcohol‐Intoxicated or Cocaine‐Injected Peer Selectively Alters Social Behaviors and Drinking in Adolescent Male and Female Rats

“…These data indicate that increases in EtOH consumption are specific to social interaction with an alcohol‐intoxicated peer administered 1.5 g/kg EtOH, and this relationship is not generalized to social interaction with a peer in a different state of intoxication, that is, social interaction with a cocaine‐injected peer. Previous research in rats found that when both animals, the demonstrator and the observer (combined exposure), were intoxicated, there was an increase in EtOH consumption, suggesting that when both peers of the dyad are intoxicated, this potentiates the risk for increased adolescent EtOH consumption (Eade et al, ). Recently, it was shown that social instability stress (isolated for 1 hour and then placed with a new cage mate daily) during adolescence (PND 30 to 45) increased intake of EtOH, but not sucrose, when male rats were tested during adolescence (Marcolin et al, ), suggesting that changes in social interaction mediate overall changes in EtOH intake in adolescent male rats.…”

“…However, one of the most common doses of EtOH used when examining passive social influences with the demonstrator–observer paradigm is 1.5 g/kg EtOH administered to the demonstrator. This dose has been shown to alter preferences for EtOH odors, environmental cues, and consumption of EtOH (Eade et al, ; Fernández‐Vidal and Molina, ; Hunt et al, ; Maldonado et al, ; Maldonado‐Devincci et al, ). Specifically, social interaction with a demonstrator administered 1.5 g/kg EtOH, but not 1.0 or 3.0 g/kg, increased EtOH consumption in the adolescent observer (Hunt et al, ).…”

“…Social influences on alcohol drinking have received attention using rodent models (Doremus et al, ; Eade et al, ; Fernández‐Vidal and Molina, ; Gauvin et al, ; Hunt et al, ; Juárez and De Tomasi, ; Marcolin et al, ; Varlinskaya and Spear, ; Varlinskaya et al, ; Varlinskaya et al, ; Varlinskaya et al, ). In animal models of social influence on alcohol drinking, the most commonly studied behaviors include social play, social investigation, and social contact (Maldonado‐Devincci et al, ; Marcolin et al, ; Varlinskaya and Spear, ; Varlinskaya et al, , ).…”

Social interaction with an alcohol-intoxicated or cocaine-injected peer selectively alters social behaviors and drinking in adolescent male and female rats

“…These data indicate that increases in ethanol consumption are specific to social interaction with an alcohol-intoxicated peer, and this relationship is not generalized to social interaction with a peer in a different state of intoxication, i.e., social interaction with a cocaine-injected peer. Previous research conducted in rats found that when both animals, the demonstrator and observer (combined exposure) were intoxicated, there was an increase in alcohol consumption, suggesting that when both peers of the dyad are intoxicated this potentiates the risk for increased adolescent alcohol consumption (Eade, Youngentob and Youngentob, 2016). Recently, it was shown that social instability stress (isolation for one hour then placed with a new cage mate daily) during adolescence (PND 30-45) increased intake of ethanol, but not sucrose, when male rats were tested during adolescence (Marcolin et al , 2019), suggesting that changes in social interaction mediate overall changes in ethanol intake in adolescent males.…”

“…Social influences on alcohol drinking have received attention using rodent models (Gauvin et al , 1994; Juárez and De Tomasi, 1999; Hunt, Holloway and Scordalakes, 2001; Varlinskaya, Spear and Spear, 2001; Varlinskaya and Spear, 2002; Fernández-Vidal and Molina, 2004; Doremus et al , 2005; Varlinskaya, Vogt and Spear, 2013; Varlinskaya, Truxell and Spear, 2015; Eade, Youngentob and Youngentob, 2016; Marcolin et al , 2019). In animal models of social influence on alcohol drinking, the most commonly studied behaviors include social investigation, social play, and social contact (Varlinskaya, Spear and Spear, 2001; Varlinskaya and Spear, 2002; Maldonado-Devincci, Badanich and Kirstein, 2010; Varlinskaya, Truxell and Spear, 2015; Marcolin et al , 2019).…”