Socially mediated alcohol preferences in adolescent rats following interactions with an intoxicated peer

Abstract

This study focuses on “passive social influences” (alcohol-related information acquired by an organism that interacts with an intoxicated counterpart) that can potentially affect alcohol preference in adolescent rats. Five experiments were conducted to investigate whether repeated social interactions with an intoxicated peer can generate alcohol-related memories that lead an animal to exhibit heightened alcohol olfactory preference patterns. Juvenile experiences with alcohol were operationalized as follows: interactions with an alcohol-intoxicated peer (Experiment 1), with an alcohol-scented cotton surrogate (Experiment 2) or with an anesthetized alcohol-intoxicated partner (Experiments 3–5). Periadolescents were then evaluated in a two-way location olfactory test where they had the opportunity to investigate a hole scented with alcohol odor or vanilla (an odorant naturally preferred by the strain of rats here utilized). Only juveniles that interacted with an alcohol-intoxicated peer were found to exhibit a significant change in alcohol odor preferences when compared to appropriate controls that interacted with a non-intoxicated peer. Alcohol odor exposure alone or interactions with an anesthetized alcohol-intoxicated peer were not sufficient to establish changes in preference for alcohol sensory cues. Results indicate that social interactions with an intoxicated peer determine heightened preference for alcohol cues in periadolescents. The establishment of this preference seems to require behavioral manifestations of the intoxicated counterpart, instead of just being dependent on an olfactory pre-exposure to alcohol cues.

Introduction

In humans, social influences on alcohol-related behaviors and expectations have been consistently reported. These influences have been classified into two main categories (Graham et al., 1991): “active social influences” that imply the explicit offer to drink alcohol and “passive social influences” that refer to a subject's perception of the reinforcement patterns of alcohol on other peers. It has been argued that social influences (e.g. peer norms, siblings' and parental drinking patterns as well as perceived availability of alcohol) are among the strongest predictors of alcohol initiation, consumption patterns and plans of future drinking (Epstein et al., 1999a, Epstein et al., 1999b, Wood et al., 2001).

Animal studies appear to provide cost-effective models in the examination of neurobehavioral characteristics underlying the rewarding effects of drugs and how social and environmental stimuli modulate drug seeking and self-administration during adolescence (Spear, 2000). Yet, there are relatively few animal studies that have explicitly analyzed how social factors lead to the initiation of alcohol consumption. This social approach could be essential to understand the mechanisms that explain how the indirect perception of alcohol-related effects in an intoxicated peer can modulate latter responsiveness to the drug in young organisms. According to the human literature, active social influences are significantly associated with alcohol use and alcohol-derived problems, but passive social influences constitute the strongest predictors of this phenomena (Wood et al., 2001). Thus, the development of animal models related with passive social influences are particularly important when examining the mechanisms of social-mediated juvenile alcohol acceptance.

Adolescent rats exhibit specific patterns of social interactions that are markedly different from those observed in younger and older subjects. They spend more time interacting with peers when compared with other age groups and reach peak levels in terms of playing behavior. The stimuli derived from social interactions between juveniles aids in the establishment of new behaviors and skills that are essential for independence and lead to social adjustments to the demands of adulthood (van den Berg et al., 1999).

Social interaction in periadolescent rats has been considered as a reinforcer in place preference conditioning (Calcagnetti and Schechter, 1992) and maze-learning (Humphrey and Einon, 1981, Normansell and Panksepp, 1990). Furthermore, in rats as well as in other rodent species, food preferences are established via social interactions (rat: Galef and Whiskin, 2000, Galef et al., 1990, Galef et al., 1994; Acomys cahirinus: McFadyen-Ketchum and Porter, 1989; Meriones unguiculatus: Valsecchi et al., 1996; Mus domesticus: Choleris et al., 1997; Spermophilus beldingi: Peacock and Jenkins, 1988). These studies are based on the cultural transmission of food preferences that can either enhance the consumption or counteract an aversion to a given food. These effects are attained as a function of the interaction between an animal that has had recent access to an unusual food (demonstrator) and a naïve animal, which interacts with the former (observer). The observer is then tested to determine whether a specific affective component of the food has been transmitted or not (Galef and Wigmore, 1983, Galef and Whiskin, 2000, Posadas-Andrews and Roper, 1983).

According to Galef and Wigmore (1983) and Galef et al. (1994), the learning process generating changes in diet preference must take place in association with a conspecific even though physical contact is not necessary. Observer rats that are allowed to smell but not to have physical contact with anesthetized demonstrators still express the preference for the food eaten by the demonstrator (Galef and Stein, 1985, Galef and Wigmore, 1983, Galef et al., 1985). Observers do not exhibit changes in food preference when the odor of the diet is presented in a rat-sized cotton ball (Galef and Stein, 1985, Galef and Wigmore, 1983, Galef et al., 1985).

Social factors modulate alcohol self-administration in rats. Housing conditions as operationalized through complete, partial or null social isolation exert significant effects upon alcohol intake (Wolffgramm, 1990). Isolated rats drink more alcohol when compared with partially isolated or group-housed subjects. When focusing on group-housed animals, subordinate rats consume more alcohol than dominant ones (Wolffgramm and Heyne, 1991). Heightened alcohol consumption in isolated or subordinate rats appears to obey to antianxiety effects of alcohol that alleviate the stress originated by specific social conditions (Wolffgramm, 1990, Wolffgramm and Heyne, 1991). Under this perspective, negative rather than appetitive reinforcing effects of alcohol seem responsible in the modulation of alcohol self-administration patterns.

It has been reported that heightened alcohol consumption results from the interaction of infant (Hunt et al., 2000) and periadolescent observers (Hunt et al., 2001) with an intoxicated age peer. It is unknown whether this effect obeys to social transmission of food preferences or if the interaction with the intoxicated peer generates a stressful condition in the observer, which later utilizes the drug in order to mitigate an aversive emotional state. It seems necessary to note that alcohol strongly affects social interactions. Alcohol dosing parameters seem crucial in determining either social facilitation or inhibition (Panksepp et al., 1987, Stewart and Grupp, 1985, Varlinskaya et al., 2001). It is conceivable that the observer's perception of these pharmacologically driven effects can play a role in the emotional content of the memory acquired while interacting with the intoxicated peer.

Until now, the impact of early social interactions with an intoxicated peer on subsequent alcohol responsiveness has been evaluated using forced or voluntary intake tests (Hunt et al., 2000, Hunt et al., 2001). In the present study, socially mediated changes in alcohol responsiveness were evaluated in periadolescent rats through the use of an olfactory preference test. The test procedure was selected to explicitly avoid positive or negative reinforcing properties of the drug during the evaluation phase. In other words, we intended to address whether social interactions with an alcohol-intoxicated peer generates specific seeking behavior of the drug without the intervention of alcohol's pharmacological properties; a strategy that should contribute clarifying the affective value of the memory that is originally established.

As will be described in detail, the first experiment in this study clearly indicated that heightened predisposition to investigate alcohol odor cues are observed in juveniles following brief interactions with a mildly intoxicated partner. Two additional experiments assessed if these odor preferences are also established through mere pre-exposure to the drug's sensory cues (Experiment 2) or through exposure to an intoxicated conspecific whose behavioral repertoire was absent due to anesthesia (Experiments 3–5). These additional experiments provide information relevant to the extent that alcohol-seeking behavior is dependent upon experience with the drug's sensory cues and/or upon ethological cues derived from the intoxicated demonstrator.