The imposition of, but not the propensity for, social subordination impairs exploratory behaviors and general cognitive abilities

Abstract

Imposed social subordination, such as that which accompanies physical defeat or alienation, has been associated with impaired cognitive function in both human and non-human animals. Here we examined whether domain-specific and/or domain-general learning abilities (c.f. general intelligence) are differentially influenced by the imposition of social subordination. Furthermore, we assessed whether the impact of subordination on cognitive abilities was the result of imposed subordination per se, or if it reflected deficits intrinsically expressed in subjects that are predisposed to subordination. Subordinate and dominant behaviors were assessed in two groups of CD-1 male mice. In one group (Imposed Stratification), social stratification was imposed (through persistent physical defeat in a colonized setting) prior to the determination of cognitive abilities, while in the second group (Innate Stratification), an assessment of social stratification was made after cognitive abilities had been quantified. Domain-specific learning abilities were measured as performance on individual learning tasks (odor discrimination, fear conditioning, spatial maze learning, passive avoidance, and egocentric navigation) while domain-general learning abilities were determined by subjects’ aggregate performance across the battery of learning tasks. We observed that the imposition of subordination prior to cognitive testing decreased exploratory tendencies, moderately impaired performance on individual learning tasks, and severely impaired general cognitive performance. However, similar impairments were not observed in subjects with a predisposition toward a subordinate phenotype (but which had not experienced physical defeat at the time of cognitive testing). Mere colonization, regardless of outcome (i.e., stratification), was associated with an increase in stress-induced serum corticosterone (CORT) levels, and thus CORT elevations were not themselves adequate to explain the effects of imposed stratification on cognitive abilities. These findings indicate that absent the imposition of subordination, individuals with subordinate tendencies do not express learning impairments. This observation could have important ramifications for individuals in environments where social stratification is prevalent (e.g., schools or workplace settings).

Performance on a strategy set shifting task in rats following adult or adolescent cocaine exposure

“…Though speculative, this finding suggests that when cocaine use is coerced via peer-pressure during adolescence, some aspects of executive function may be hindered in adulthood. Some support for this idea includes research showing that imposed subordination in young mice produces impaired exploratory behaviors and general learning disability compared to mice with dominant status (Colas-Zelin et al 2012) and research showing that an animal’s social rank (dominant or subordinate) influences behavioral responses to a variety of psychoactive drugs (Czoty and Nader 2013; Nesher et al 2013). Human laboratory tests show that one’s relative perceived rank in a social hierarchy (lower or higher) influences cortical activation patterns differently (Zink et al 2008) and that the perception of social hierarchy cues in monkeys modulates adaptive behavior, including the direction of visual attention (Deaner et al 2005) that may be mediated in part by the OFC (Marsh et al 2009).…”

Individual differences in behavioural plasticities

“…whether various types of behavioural plasticities are themselves developmentally plastic. For instance, one might ask whether within-individual variation in courtship behaviour as a function of variation in current light intensity depends upon the light intensity an individual experienced in its rearing environment (Chapman, Morrell & Krause, 2009), or whether learning rates for a given task at a given age are affected by exposure to stressful events earlier in life (Colas-Zelin et al, 2012). The question of whether a given type of behavioural plasticity is itself developmentally plastic is important because if this is true, at least some of the variation across individuals or across genotypes in that type of behavioural plasticity at a given age could be due to differences among those individuals in experiences earlier in life (Stamps & Groothuis, 2010b;Dingemanse & Wolf, 2013;Snell-Rood, Davidowitz & Papaj, 2013).…”

Social dominance differentially alters gene expression in the medial prefrontal cortex without affecting adult hippocampal neurogenesis or stress and anxiety‐like behavior

“…Additionally, it has been established that belonging to the top or bottom part of the social rank has an impact on other dimensions of behavior. Several studies have demonstrated the influence of social status in decision making (15), cognitive performance (16,17), and even health (18). Among the traits that could be influenced by the allocation of higher or lower position in a social hierarchy, anxiety and stress-like behaviors are the ones most addressed.…”