Elsevier

Behavioural Brain Research

Volume 241, 15 March 2013, Pages 185-190
Behavioural Brain Research

Research report
Prenatal Enriched Environment improves emotional and attentional reactivity to adulthood stress

https://doi.org/10.1016/j.bbr.2012.12.019Get rights and content

Abstract

Environmental factors seem to play a key role in brain and behavioral development, both in humans and animals. Different environmental manipulations, either pre- or post-natal, have been shown to exert long-term physiological and behavioral effects. While studies in the field of Enriched Environment mainly focus on the post weaning period and provide enrichment as a post adverse-experience manipulation, the preceding effects of prenatal Enriched Environment have rarely been investigated. In this study, we investigated the effects of prenatal Enriched Environment (through the entire pregnancy) followed by adulthood acute stress. In the prenatal Enriched Environment offspring, we found anxiety and depressive-like behaviors with poor attentional performance. Surprisingly, when prenatal Enriched Environment was followed by adulthood stress, we observed a dramatic restoration of these behavioral deficits. Our results suggest that prenatal Enriched Environment may substrate resiliency to adulthood stress.

Highlights

► Wister pregnant dams housed in standard or enriched cages. ► Offspring were exposed to adulthood stress according to experimental groups. ► In offspring, prenatal EE had deteriorating emotional and attentional effects. ► In offspring, prenatal EE followed by adulthood stress resulted in beneficial emotional, attentional and hormonal effects.

Introduction

The concept of Enriched Environment (EE) was first described by Hebb [1]. Over the years data have accumulated which indicate experience dependent changes in both behavioral and physiological dimensions. The aforementioned changes suggest an active interaction between the animal and its environment [2].

Environmental enrichment involves alterations to the animal's home cage or secondary exploratory area which provide enhanced sensory, motor, cognitive and potentially social opportunities. Although different protocols exist, they all share the same concept of novelty and complexity of the environment. A large space within which the animal experiences exploration and introduction to a variety of objects, varying in shape, size, weight, smell and texture, renders stimulation of visual, somatosensory, and olfactory systems [3].

Many studies in the field of EE investigated the rehabilitative or protective effects of EE in different animal models and multiple implementations. Specifically, EE treatment was found to counteract neurophysiological and behavioral deficits, induced by pharmacological or environmental manipulations [4], [5], [6]. Moreover, EE was found to rescue abnormal behaviors, such as emotional reactivity and spatial learning, as well as motor skills deficits, induced by prenatal stress [7], [8], [9]. In addition, it was shown that high secretion of corticosterone in response to stress, in the prenatal stressed animals, can be reversed by postnatal EE treatment [8], [10]. Furthermore, the exposure to a stressful experience was observed to disrupt sensorimotor gating, often considered a crucial component of normal information processing [11], [12], [13]. On the other hand, the exposure to EE, at different ages, has been shown to have a beneficial effect on spontaneously hypertensive rats’ performance in attention tasks [14] and prevent the degradation of attention performance detected in aged rats [15].

An extensively discussed topic of in utero early programming in animal models, revealed the long lasting impact of various fetal manipulations (e.g. maternal stress; exposure to synthetic glucocorticoid, etc.) on different developmental axes such as the neuroendocrine system and its associated behaviors [16]. Given the rehabilitative effects of post-natal (and later) EE and the reported long lasting changes of the various pre-natal manipulations, a question may be raised as for the behavioral and hormonal consequences of implementing a pre-natal EE manipulation. Specifically, how this manipulation may affect the offspring's ability to cope with a stressful experience after birth.

Only a few studies have investigated the effects of prenatal EE. These reports provide evidence of beneficial effects on offspring's behavioral and cognitive performance, specifically on learning and memory [17], [18], [19], with indications of brain structural changes [19]. A recently published study has shown that the exposure to prenatal EE has long-term emotional and hormonal effects [20].

In the current study, we aimed to further explore the long-term effects of prenatal EE on both behavioral and hormonal manifestations. We concentrated on better understanding the potential predispositional effect of prenatal EE followed by adulthood stress and the process of prenatal adaptation, by which offspring are perhaps prepared to the environment into which they are to be born. Thus, we investigated rats’ hormonal, emotional and attentional reactivity to acute stress in adulthood, following a prenatal EE manipulation.

Section snippets

Animals

Twenty male rats (PND 22) and 10 pregnant female Wistar rats (at the first week of pregnancy weighting between 260-290 gr) were purchased from Harlan (Harlan, Israel). Male rats were housed 4 per cage in standard plastic cages (30 cm × 30 cm × 18 cm) with sterilized sawdust bedding. In order to estimate a possible litter effect, we examined the behavioral heterogeneity between the subjects in each group. Indeed, a considerable standard error of the means (S.E.M.) in the groups and normal distribution

Anxiety-like behavior

To examine the level of anxiety-like behavior in the different groups, we examined freezing duration measured in the plus-maze (Fig. 2). A significant effect was found for group [F(3.36) = 35.68, P < 0.0001). The prenatal Enriched Environment (pEE) group, demonstrated the highest freezing behavior compared with the control (P < 0.0001) or adulthood stress (P < 0.006) groups. As expected, the exposure to adulthood stress lead to increased freezing behavior (P < 0.003). Interestingly, rats that were

Behavioral and attentional reactivity

The long-term effects of “negative” prenatal stress manipulations on offspring's brain and behavioral development are extensively discussed in the literature. In the current study, given the alleged rehabilitative and protective emotional effects of EE, we aimed to investigate the assumed “positive” prenatal EE manipulation on the offspring's emotional and attentional reactivity to adulthood stress.

Our results are consistent with a recently published article by Rosenfeld and Weller [20],

Conclusions

To conclude, this study emphasizes the relation between maternal environmental factors and the adult offspring's emotional and attentional reactivity to adulthood stress. Although the pEE by itself has resulted in stress-like symptoms and overall impaired behavioral performance, when the rats were introduced to a stressful experience in adulthood, a positive effect appeared in all measures.

Postulating that the common life trajectory often includes exposure to a stressful experience in

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