Enriched Environment Exposure Enhances Social Interactions and Oxytocin Responsiveness in Male Long-Evans Rats.

Steven Neal,Massimo Bardi,Molly Kent,Kelly G Lambert

doi:10.3389/fnbeh.2018.00198

Abstract

Both social and physical stimuli contribute to the complexity of an animal’s environment, influencing biobehavioral responses to subsequent challenges. In the current study, male Long-Evans rats were randomly assigned to an isolate (ISO), social control (SC) or social enriched (SE) group (n = 8 per group). The SC and SE conditions were group housed with the SE group exposed to physical enrichment stimuli that were natural as opposed to manufactured (e.g., hollowed out log instead of plastic hiding place). On three occasions during their 40-day enriched environment exposure, night/dark phase videos were obtained for 1 h during the early part of the dark phase. During this time, the SE animals exhibited significantly more social grooming with no differences between the SE and SC in the frequency of play or self-grooming bouts. Subsequently, all animals were assessed in social interaction and problem-solving escape tasks during the last week of the enriched environment exposure. SE rats exhibited increased digging bouts toward the restrained conspecific in the social interaction task whereas the other groups exhibited more escape responses. In the problem-solving task, SE animals exhibited a decreased latency to cross the barrier to escape from the predator odor (i.e., cat urine and fur). Neural analyses indicated increased oxytocin-immunoreactive (OT-ir) tissue in the SE supraoptic and paraventricular nuclei of the hypothalamus compared to the other groups. Interestingly, blood samples indicated lower peripheral corticosterone (CORT) and higher OT levels in the ISO animals when compared to the SC and SE animals, an effect retrospectively attributed to separation anxiety in the SE and SC animals in preparation for histology procedures. When the behavioral, neural and endocrine data were visualized as a multifaceted dataset via a multidimensional scaling analysis, however, an association between social enrichment and higher OT involvement was observed in the SE animals, as well as heightened stress responsivity in the ISO and SC groups. In sum, the SE animals exhibited a facilitation of social responses, problem-solving ability and OT immunoreactive responsiveness. These findings provide new information about the influences of both physical and social stimuli in dynamic and enriched environments.

Highlights

In the late 18th century, Italian anatomist, Michele Vincenzo Malacarne, reported that when animals underwent extensive training, they developed more cerebellar folds than untrained animals
Animals were housed in habitats designed to yield varying amounts of social engagement (i.e., isolatehoused (ISO; no social contact); social-control (SC; moderate social contact) and contact) and social-enriched (SE; high social contact)) to explore the effects of environmental variables on social- and predator-stress responsiveness
The social interaction task used in the current study revealed that social enriched (SE) animals demonstrated more digging directed toward the stimulus animal, as well as fewer attempts to escape, whereas the ISO animals engaged in more exploratory sniffing

Summary

Introduction

In the late 18th century, Italian anatomist, Michele Vincenzo Malacarne, reported that when animals underwent extensive training, they developed more cerebellar folds than untrained animals (described in Rosenzweig et al, 1972) These provocative findings were controversial and, laid dormant until the mid-20th century when a prominent Canadian neuroscience researcher, Donald Hebb, reported that rats raised in an engaging environment in his own home exhibited enhanced learning compared to his standard laboratory raised animals (Hebb, 1949). Instead of spending an inordinate amount of time training the animals, it was assumed that the animals would engage in a form of self-training if they were housed in engaging environments (Rosenzweig and Bennett, 1996) These complex environments became known as ‘‘enriched environments’’ to contrast with the typical cages used in the laboratory (Krech et al, 1960; Diamond et al, 1965). The terms enriched and complex are used interchangeably throughout this manuscript to refer to engaging laboratory environments that include social and physical stimuli

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