Effects of prenatal alcohol exposure on social competence: Asymmetry in play partner preference among heterogeneous triads of male and female rats

Abstract

Social behavior deficits associated with prenatal alcohol exposure (PAE) are frequently described in terms of impaired social competence, which can be defined as the effectiveness in social interaction and the ability to employ social skills successfully within different interpersonal contexts. Play behavior—which peaks during adolescence—is critical for developing social competence, as well as for motor, cognitive, and emotional development. Studies of play behavior typically utilize protocols where animals interact in dyads. However, less is understood about how the social environment may shape PAE‐related social behavior deficits, particularly in more complex social contexts. Here, we assess play partner preference utilizing a novel approach in which adolescent male and female animals interact within same‐sex triads comprised of animals from mixed prenatal treatments to determine how play partner identity and social group composition interact to shape behavior. When triads included one PAE animal and two control animals (i.e., control animals had the option to play either with a fellow control or a PAE playmate), we observed play target asymmetry whereby controls preferentially played with fellow controls. Notably, these results were consistent for triads of both males and females, with subtle differences in frequency of initiations versus reciprocations. We found no play target asymmetry, however, when triads included two PAE animals and one control animal or different configurations of control and pair‐fed animals. Taken together, play target asymmetry resulting from ineffective social interactions, including a failure to engage with, respond to, and/or solicit play from control play partners appropriately, suggests that PAE negatively impacts the development of social competence.

Effect of social instability stress in adolescence or adulthood on sensitivity to sucrose concentration in a social context in male and female Long‐Evans rats

“…We predicted that CTL rats would discriminate between SS rats and CTL rats in a social interaction test involving two CTL and one SS rat, such that they would initiate social interaction more with another CTL rat than with an SS rat. The triad interaction test was modeled after that of Holman and colleagues (2019) who found that CTL rats preferred to initiate play with other CTL rats rather than with the prenatal alcohol‐exposed rat. In contrast to our prediction, for females stressed as adults and tested long after, CTL rats initiated interaction with SS rats more so than SS rats initiated interaction with CTL rats.…”

“…Based on our hypothesis and evidence of reduced social interaction in SS rats, we predicted that CTL rats would initiate more social interaction with each other than with the SS rat. To test this prediction, rats underwent a triad social interaction test (based on Holman et al., 2019) in age‐ and sex‐matched groups of two CTL rats and one SS rat.…”

Prenatal alcohol exposure and developmental programming of mental illness

“…identified that male offspring of Sprague-Dawley dams exposed to this dose of alcohol throughout pregnancy (with a gradual increase of dosage in a liquid diet early in pregnancy of E1 diet containing 66% control and 34% ethanol diet; E2 diet containing 34% control and 66% ethanol diet; E3 to E22 diet containing 100% ethanol diet, final BAL of 95.85 ± 10.79 to 135.5 ± 50.8 mg/dL) displayed delays in adolescent male offspring social behaviour, deficits in recognition memory and were less effective at engaging and responding in playful interaction with control rats 122,123 . Similarly, a study treating Long-Evans rat dams with 5% v/v ethanol (BAL of 84 ± 5.5 mg/dL, liquid diet) throughout gestation resulted in altered social interaction in female but not male offspring 127 .…”

Prenatal Adversity Alters the Epigenetic Profile of the Prefrontal Cortex: Sexually Dimorphic Effects of Prenatal Alcohol Exposure and Food-Related Stress

“…Until recently, most studies utilizing animal models often excluded or failed to analyze data from females. Nevertheless, of those studies that probed for sex-specific changes, differential effects of PAE on males and females were reported in both rodent and primate models, including differences in hippocampal microglia and cytokine expression [16], hypothalamic-pituitary-adrenal (HPA) activity and regulation [9], dopaminergic regulation [17], immune responses [18], social behavior [19][20][21], and depressive-and anxiety-like behaviors [12,[22][23][24]. By contrast, clinical research in the FASD field has typically included children of both sexes, and sex differences in prevalence of FASD, brain maturation, cognitive function, and mental health, among other outcomes, have been reported [25][26][27][28][29].…”