During development of the central nervous system, neurons pass through critical periods of vulnerability to environmental factors. Exposure to ethanol during gastrulation or during neuronal generation results in a permanent reduction in the number of neurons in trigeminal-associated cranial nerve nuclei. Normal functioning of the trigeminal system is required for social behavior, the present study examined the effects of acute prenatal exposure to ethanol on social interactions across ontogeny. Pregnant Long-Evans rats were injected with 2.9 g/kg ethanol (i.p., 20% v/v solution; peak blood ethanol concentrations of ~300 mg/dl) or an equivalent volume of saline on gestational day (G) 7 (gastrulation) or G12 (neuronal generation). Subsequently, social investigation, play fighting, contact behavior, social motivation, and overall locomotor activity in the social context were assessed in male and female offspring during early adolescence, late adolescence, or adulthood, on postnatal day (P) 28, P42, or P75, respectively, using a modified social interaction test. Ethanol exposure on G7 resulted in mild changes of social behavior evident in young adolescents only. In contrast, animals exposed to ethanol on G12 demonstrated pronounced behavioral deficits throughout ontogeny, with deficits being most robust in male offspring. Males exposed to ethanol on G12 showed decreases in social investigation, contact behavior, and play fighting, whereas a decrease in social motivation, i.e., transformation of social preference into social avoidance, was evident at P42 and P75 regardless of sex. These findings show that acute exposure to ethanol alters social behavior, and that the timing of the exposure defines the behavioral outcome.
Prenatal ethanol exposure is associated with, and is a risk factor for, developmental disorders with abnormal social behaviors, including autism spectrum disorders. We hypothesize that the specific effects of ethanol on social behavior are defined by the timing of the exposure as well as subsequent changes in brain regions such as the amygdala and ventral striatum. We recently reported that in utero ethanol exposure on gestational day 12 alters social behaviors of weanling [postnatal day (P) 28], adolescent (P42), and young adult (P75) rats. Male, but not female, offspring of the ethanol-exposed dams showed significant decreases in social investigation (sniffing of a social partner), contact behavior (grooming or crawling over/under the partner), and play fighting (following, chasing, nape attacks, or pinning) at all ages tested with maximal effects at P28 and P42. Furthermore, ethanol-exposed males and females showed evidence of social avoidance at P42 and P75. The present study sought to test whether a form of social enrichment could normalize any of the social deficits and what the molecular mechanisms of such effects might be. We found that housing rats with nonmanipulated control rats normalized the social avoidance phenotype normally seen when they are housed with sex-matched prenatal ethanol-exposed littermates. There was no mitigation of the other ethanol-induced behavioral deficits. Conversely, male control-treated rats housed with nonlittermates showed deficits in play fighting, social investigation and contact behavior. Molecular analyses of the amygdala and ventral striatum of adolescent rats following fetal ethanol exposure indicated several specific neurotransmitter systems and pathways that might underlie the social avoidance phenotype as well as its reversal.
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