Elsevier

Neuroscience

Volume 132, Issue 3, 2005, Pages 867-877
Neuroscience

Differential effects of periodic maternal separation on adult stress coping in a rat model of extremes in trait anxiety

https://doi.org/10.1016/j.neuroscience.2005.01.034Get rights and content

Abstract

We studied interactions of genetic and environmental factors shaping adult emotionality and stress coping, and tested the hypothesis that repeated periodic maternal deprivation (PMD) exerts differential effects on adult behavioral and neuroendocrine stress responsiveness in dependence on the genetic predisposition to either hyper- or hypo-anxiety. Exposure of male Wistar rats bidirectionally bred for either high (HAB) or low (LAB) anxiety-related behavior to PMD between postnatal days 2 and 15 resulted in a behavioral approximation of the selected lines. This was reflected by test-dependent signs of reduced anxiety-related behavior in adult HAB rats and of enhanced levels of anxiety in LAB rats compared with their corresponding unstressed controls. In addition to behavioral parameters, differential effects of PMD were also seen with respect to the responsiveness of the hypothalamo—pituitary—adrenocortical axis to acute stressor exposure (novel environment) in adulthood. The corticotrophin (ACTH) and corticosterone hyper-responses seen in control rats of the HAB line compared with those of the LAB line became attenuated in PMD-HAB rats, whereas PMD did not significantly alter neuroendocrine responses in LAB rats. Thus, as a result of PMD, both ACTH and corticosterone responses became indistinguishable between HAB and LAB rats. Although HAB dams spent more time on the nest with the litter compared with LAB dams during the first 5 days postpartum, licking and grooming behavior did not differ between the lines prior to separation, and was found to be increased to the same extent in both HAB and LAB dams during the first hour immediately after reunion with the pups. In contrast to early life stress, exposure of adult HAB and LAB rats to a 10-day unpredictable stress schedule failed to alter their emotional measures. The mitigating effect of PMD on both behavioral and neuroendocrine parameters in rats representing extremes in trait anxiety might reflect an evolutionary benefit as the genetic variability among individuals of a species is sustained while allowing adequate responses to potentially dangerous stimuli in adulthood dependent on early life conditions.

Section snippets

Animals

The animal studies were conducted in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals (NIH Publications No. 80-23) and of the government of Oberbayern/Oberpfalz. All efforts were made to minimize the number of animals used and their suffering. The bidirectional selection and breeding of the two rat lines, started in the 1980s, have recently been reviewed (Landgraf and Wigger, 2002). Briefly, adult Wistar rats were tested on the elevated

Anxiety-related behavior: holeboard

The anxiety on the modified holeboard as reflected by the percentage of time spent on the board (factor line×treatment: F1,42 5.48, P=0.024) and the frequency of stepping onto the board (factor line: F1,42 5.58, P=0.023) differed significantly between the groups. As expected, adult HAB controls showed a higher level of trait anxiety compared with LAB control rats with respect to both of these parameters (P<0.01; Fig. 1A). PMD induced differential effects on anxiety in HAB and LAB offspring.

Discussion

It is no longer controversial, whether nature or nurture shapes the susceptibility to the expression of anxiety including the individual development of behavioral and physiological stress coping styles (Gross and Hen, 2004). The data of this study demonstrate how complex genetic and environmental factors interact in the configuration of a behavioral phenotype such as anxiety-related behavior in parallel with modulating neuroendocrine responses. Repeated exposure to maternal deprivation during

Acknowledgments

We are grateful to Dr. L. Young (Atlanta) for critical discussions and to Mrs. G. Schindler, Mrs. M. Zimbelmann and Mr. A. Varga for excellent technical help. Supported by VolkswagenStiftung (I.D.N.).

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