The Effects of Environmental Enrichment on Depressive and Anxiety-Relevant Behaviors in Socially Isolated Prairie Voles

Abstract

Objectives Social isolation is associated with depression, anxiety and negative health outcomes. Environmental enrichment, including environmental and cognitive stimulation with inanimate objects and opportunities for physical exercise, may be an effective strategy to include in treatment paradigms for affective disorders as a function of social isolation. In a rodent model – the socially monogamous prairie vole – we investigated the hypothesis that depression- and anxiety-related behaviors following social isolation would be prevented and remediated with environmental enrichment. Methods Experiment 1 investigated the preventive effects of environmental enrichment on negative affective behaviors when administered concurrently with social isolation. Experiment 2 investigated the remediating effects of enrichment on negative affective behaviors when administered following a period of isolation. Behaviors were measured in 3 operational tests: open field; forced swim test; and elevated plus maze. Results In isolated prairie voles, enrichment prevented depression- (immobility in FST, group × housing interaction, P=0.049) and anxiety-relevant behaviors (exploration in open field, group × housing interaction, P=0.036; exploration in elevated plus maze, group × housing interaction, P=0.049). Delayed enrichment also remediated these behaviors in isolated animals (immobility in forced swim test, main effect of housing, P=0.001; exploration in open field, main effect of housing, P=0.047; exploration in elevated plus maze, main effect of housing, P=0.001), and was slightly more effective than physical exercise alone in remediating anxiety-relevant behaviors. Conclusions These findings provide insight into the beneficial effects of an enriched environment on depression- and anxiety-relevant behaviors using a translational rodent model of social isolation.

The Neuroendocrinology of Social Isolation

“…The perception of isolation from others—of being on the social perimeter—is not only unhappy but also signals danger across phylogeny. Fish have evolved to swim to the middle of the group when predators approach (Ioannou et al 2012), mice housed in social isolation rather than in pairs show sleep disruptions and reduced slow wave sleep (Kaushal et al 2012), and prairie voles when isolated from their partner and subsequently placed in an open field show less exploratory behavior and more predator evasion (Grippo et al 2014). These behaviors reflect an increased emphasis on self-preservation when on the social perimeter, an emphasis that increases the likelihood of survival.…”

Implicit attention to negative social, in contrast to nonsocial, words in the Stroop task differs between individuals high and low in loneliness: Evidence from event-related brain microstates

“…Social isolation from a preferred partner has been shown to increase vigilance for threats in mammals, as well. For instance, prairie voles when isolated from their pairbonded partner and subsequently placed in an open field, show less exploratory behavior and more predator evasion than prairie voles who have been housed with their partner (Grippo et al, 2014). Life on the social perimeter is dangerous for social animals and has detectable effects on attention and behavior, and perceived social isolation (or what has been termed loneliness in humans) activates neural, neuroendocrine, and behavioral responses that promote short-term survival (Cacioppo, Cacioppo, Capitanio, & Cole, 2015;.…”

Voluntary locomotor activity mitigates oxidative damage associated with isolation stress in the prairie vole (Microtus ochrogaster)

“…A non-mutually exclusive alternative is that the ability to perform locomotor activity could be a form of displacement behaviour or a coping mechanism, which lessens the stress of social isolation [16]. Previous studies have found that environmental enrichment prevents and remediates behavioural consequences that result from social isolation and also decreases corticosterone levels in isolated individuals [12]. It is possible that voles that ran more had longer interactions with this form of environmental enrichment; though, regardless of distance run, IW voles spent time interacting with the wheel during isolation This study is unique in that it attempts to determine whether routine voluntary exercise is able to mitigate the negative effects of isolation stress on oxidative balance.…”

“…Prairie voles represent an excellent model system to study these relationships because they live in structured groups [11] and respond to chronic periodic social isolation with increased glucocorticoids [2]. In addition, metabolic activity can be easily manipulated in prairie voles through voluntary wheel running [12].…”