Social housing enhances acquisition of task set independently of environmental enrichment: A longitudinal study in the Barnes maze

Abstract

Human studies suggest that healthy social relationships benefit cognition, yet little is known about the underlying neural mechanisms of this protective effect. In rodents, studies on acute isolation and environmental enrichment (EE) confirm the importance of social exposure. Despite the widely recognized importance of sociality, however, rodent models have yet to explore the independent contributions of social housing divorced of other forms of enrichment. This study dissociates the effects of social and physical enrichment on spatial learning and memory from adulthood to old age. Rats were placed in either single or group housing, provided with ample enrichment, and tested at three time points on several phases/versions of the Barnes maze (BM) (standard, retention probes, variable location, and reversal). We found that sustained social housing enhanced cognitive flexibility, as evidenced by superior acquisition of task set (standard BM), adaptability to a new task set (variable BM), and improved reversal learning (reversal BM). Long-term retention (BM retention probes) of spatial memory was unaffected by housing conditions. Recent studies from our lab, including this report, are the first to show that social housing confers cognitive benefits beyond those of physical enrichment. Importantly, our experimental design is ideal for exploring the neural underpinnings of this socially induced cognitive protection. Understanding how sociality influences cognition will be invaluable to translational models of aging, neuropsychiatric disease, and neurological injury.

Cognitive Reserve in Model Systems for Mechanistic Discovery: The Importance of Longitudinal Studies

“…• Sensitive to training or practice effects (Heimer-McGinn et al, 2020). (Harrison et al, 2009;Berdugo-Vega et al, 2020).…”

“…This maze is less stressful than the watermaze (Harrison et al, 2009). However, similar to training on the watermaze, early training on the Barnes maze results in better learning later in life due to preserved procedural memory (Heimer-McGinn et al, 2020). For aged animals, the Barnes maze often is the method of choice, if the watermaze cannot be applied because of its greater physical demands (Berdugo-Vega et al, 2020).…”

Social Reactivation of Fear Engrams Enhances Memory Recall

“…We propose that the capacity of social experiences to reactivate memories contributes to the enriching effects of a social environment on cognition (Heimer-McGinn et al, 2020; Shafto et al, 2019). From an evolutionary perspective, a stressed conspecific or their ambient auditory-olfactory emissions might signal a dangerous situation in which it is adaptive to hone one’s own memories to guide decision making.…”

“…For group-living species such as humans and rodents, conspecific interactions directly impact social learning and memory (Hoppitt and Laland, 2008; Leblanc and Ramirez, 2020), and pervasively shape emotion (Neumann and Strack, 2000; Reavis et al, 2015; Williamson and Austin Williamson), attention (Caplin et al, 2015), and cognitive ability (Dause and Kirby, 2019; Doulames et al, 2014; Heimer-McGinn et al, 2020; Kuhlmann et al, 2005). Higher-order cognitive processes such as memory within a social brain are thus interlaced with social influences.…”

“…For group-living species such as humans and rodents, conspecific interactions pervasively shape emotion (1)(2)(3), attention (4), and cognitive ability (5)(6)(7)(8). Higher-order cognitive processes such as memory within a social brain are thus interlaced with social influences.…”