Therapeutic and protective effect of environmental enrichment against psychogenic and neurogenic stress

Abstract

Environmental enrichment (EE) has beneficial neurobiological, physiological and behavioral effects. The purpose of the present paper is to review the animal research literature pertaining to the impact of EE on altering physiological and behavioral anxiety outcomes. Evidence supports the view that EE attenuates responses to certain anxiety provoking situations, and that these effects persist over time. Specifically, EE attenuates behavioral anxiety-type responses and endocrine responses mediated via the hypothalamic–pituitary–adrenal (HPA) axis evoked by psychogenic and/or neurogenic stressors. EE is not only able to protect from excessive anxiety in response to a present stressor, but also attenuates the enduring or persistent effects engendered by past psychogenic stressor(s) such as prenatal stress or neonatal maternal separation. It is noteworthy that the protective effects of EE are particularly apparent in animals that are highly anxious or when the task is highly challenging for the subject. Various mechanisms of action of EE have been proposed, ranging from behavioral/cognitive to cellular/molecular processes. A pronounced variability in the enrichment protocols used by different investigators may account for some of the inconsistencies noted in the effect of EE on behavioral (e.g. anxiety) and endocrine (e.g. plasma corticosterone) responses. Although the occasional inconsistencies highlight the need for further research, a preponderance of the animal research data indicates that EE exerts therapeutic and protective (anxiolytic) effects against (a) impending threat, (b) enduring effects of past stressor(s) and (c) subsequent stressors.

Introduction

The modern concept of environmental enrichment (EE) was adopted from the early work of pioneers in the field that suggested that environmental manipulation can alter neurobiology and behavior [33], [81], [83]. The original studies constituted the template for the EE design with relatively spacious cages housing rodents in large groups and with ready access to a variety of stimulus-objects.

EE provides enhanced opportunities to interact with complex inanimate and social stimuli and to explore the environment [82], [84]. EE has been described as a continuous enhancement in cognitive, sensorimotor and/or physical activity [60]. In the context of enrichment, the continual introduction of new stimulus objects [99] enables the animal to acquire sensory and cognitive experiences. The availability of running wheels, ropes, ladders, tunnels or bridges enables the animal not only to exercise but also to undergo acrobatic training [50]. Furthermore, EE animals are housed in relatively large cages, typically in groups of 6–12 animals, providing opportunity for social interactions [72], [106].

Research has increasingly indicated that EE induces morphological, neurobiological, physiological and behavioral changes [31], [51], [80], [99], [107]. The environment can affect behavior negatively or positively. Enrichment has been shown to improve cognition, reduce anxiety [4], [10], [67] and facilitate recovery from brain lesions [107]. Even an increase in cage size has been shown to improve general well being and reduce anxiety level of animals [56]. The contribution of inanimate stimulation and social interaction has been investigated [89]. The importance of social stimulation was made even more evident by studies that reported the behaviorally detrimental effect of isolation [74], [108].

EE is beneficial for the physiological well being of the animals. With the exception of one report [11], EE animals gained weight faster and had higher body weight than those in standard conditions [35], [84], [96]. Conversely, removal of enrichment features had adverse effects. Enriched mice lost relatively more body weight than controls after being placed in individual cages for only one night [96]. Animals with septal lesions reared in an enriched environment showed an immediate increase in reactivity when switched to a restricted environment [30]. Altogether, EE appears to be beneficial for the general psychological and physical well being of animals [5], [32], [57].

The purpose of the present manuscript is to review the animal research literature pertaining to the role of EE in attenuating the behavioral and physiological expression of anxiety-type responses. The literature reviewed below suggests that EE may not only protect from the detrimental effects of psychogenic and neurogenic stressors, but may even reverse their effects. Possible mechanisms of action of the therapeutic effect of enrichment are also discussed.