Maternal swimming exercise during pregnancy attenuates anxiety/depressive-like behaviors and voluntary morphine consumption in the pubertal male and female rat offspring born from morphine dependent mothers

doi:10.1016/j.neulet.2017.08.074

Neuroscience Letters

Volume 659, 17 October 2017, Pages 110-114

https://doi.org/10.1016/j.neulet.2017.08.074 Get rights and content

Highlights

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Morphine during pregnancy produces behavioral deficits in rat offspring.
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Maternal swimming decreases behavioral deficits following prenatal morphine in offspring.
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Maternal swimming decreases voluntary morphine consumption in rat offspring.

Abstract

This study was designed to examine whether maternal swimming exercise during pregnancy would attenuate prenatally morphine-induced anxiety, depression and voluntary consumption of morphine in the pubertal male and female rat offspring. Pregnant rats during the development of morphine dependence were allowed to swim (30–45 min/d, 3 days per a week) on gestational days 11–18. Then, the pubertal male and female rat offspring were tested for the elevated plus-maze (EPM), sucrose preference test (SPT) and voluntary morphine consumption using a two-bottle choice (TBC) paradigm. The results showed that male and female rat offspring born of the swimmer morphine-dependent mothers exhibited an increase in EPM open arm time and entries, higher levels of sucrose preference than their sedentary control mothers. Voluntary consumption of morphine was less in the male and female rat offspring born of the swimmer morphine-dependent mothers as compared with their sedentary control mothers during three periods of the intake of drug. Thus, swimming exercise in pregnant morphine dependent mothers decreased anxiety, depressive-like behavior and also the voluntary morphine consumption in the pubertal male and female offspring, which may prevent prenatally morphine-induced behavioral sensitization in offspring.

Introduction

Prenatal morphine exposure can cause developmental delay in the fetal cerebrum [17] neurobehavioral deficits in offspring such as morphine tolerance [5], morphine-induced conditioned place preference (CPP) and behavioral sensitization [24], vulnerability to drug abuse in future generations [22], the anxiety [9], depressive [10]-like behavior, voluntary consumption of morphine [9]. It has shown that prenatal morphine exposure on gestational days 11–18 alter the development of brain systems that involved in reward and motivation- related behaviors [22], [23].

We have already observed that voluntary exercise during chronic oral administration of morphine in pregnant rats decreases the anxiety-like behavior and voluntary consumption of morphine in male offspring [9]. It has been shown that maternal exercise during pregnancy enhanced short-term memory, hippocampal neurogenesis [11], antioxidant activity and mitochondriogenesis in brain [13], spatial learning acquisition [3], and decreased anxiety [4] of rat offspring. Moreover, we have previously observed that regular swimming exercise reduces the severity of physical and psychological dependence and voluntary morphine consumption in morphine-dependent and withdrawn rats [7] and morphine-induced reward and behavioral sensitization in maternally-separated rat offspring [1]. Swimming might be one of the most suitable exercises during the gestational period [12] to activation of antioxidant mechanisms under thermal stress [15], with no harm to the fetus [12]. On the other hand, the effect of exercise during pregnancy in morphine dependent rat mothers has been less studied. Given the well-known beneficial effects of swimming exercise, the aim of the present study was to investigate whether regular swimming exercise as forced exercise during induction of morphine dependence on gestational days 11–18 would attenuate prenatally morphine-induced anxiety/depressive-like behaviors and voluntary morphine consumption in the pubertal male and female rat offspring.

Section snippets

Animals and induction of morphine dependence

Male Wistar rats (250 ± 10 g, n = 16) were allowed to mate with female virgin Wistar rats (250 ± 10 g, n = 16) during a 24 h period. Observation of vaginal plug was considered as gestational day 0 (G0) [9]. Then, pregnant rats were randomly divided into four groups of control-sedentary (Cont/No Swim), control −swimming exercise (Cont/Swim), morphine dependent- sedentary (D/No Swim), morphine dependent-swimming exercise (D/Swim), and were housed individually in cages with a 12 h light/dark cycle at 22–24 °C

Anxiety-like behavior

The results of the EPM testing in the pubertal male and female rat offspring born from morphine-dependent mothers are shown in Fig. 2. Three-way ANOVA in the percentage of time spent in the open arms in the pubertal male and female rat offspring born from morphine-dependent mothers revealed a significant effect of treatment (F_1,56 = 22.95, P = 0.0001), and exercise (F_1,56 = 25.147, P = 0.0001), sex (F_1,56 = 4.183, P = 0.046), and treatment × exercise (F_1,56 = 9.89, P = 0.003), and treatment × exercise × sex (F_1,56 =

Discussion

This study has shown that the development of morphine dependence in the sedentary rat mothers on gestational days 11–18 exhibited anxiety/depressive-like behaviors and voluntary consumption of morphine in the pubertal male and female rat offspring which is consistent with our previous results [9]. These results could be due to increased sensitivity this period in the development of brain circuits that sensitized the pubertal male and female rat offspring to the rewarding effect of morphine.

Conclusion

This study provides novel evidence that swimming exercise in pregnant rat mothers during the development of morphine dependence decreased anxiety/depressive-like behaviors and voluntary consumption of morphine in the pubertal male and female offspring. Our findings could be exploited in the development of therapeutic approaches in the prevention of prenatally morphine-induced behavioral sensitization after first postnatal morphine exposure.

Conflict of interest

The authors report no conflicts of interest.

Acknowledgments

This work was supported by grants from University of Semnan (Semnan, Iran) and Cognitive Science and Technologies Council of Iran (CSTC).

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Research articleMaternal swimming exercise during pregnancy attenuates anxiety/depressive-like behaviors and voluntary morphine consumption in the pubertal male and female rat offspring born from morphine dependent mothers

Highlights

Abstract

Introduction

Section snippets

Animals and induction of morphine dependence

Anxiety-like behavior

Discussion

Conclusion

Conflict of interest

Acknowledgments

Neurosci. Lett.

Eur. J. Pharmacol.

Neurosci. Lett.

Eur. J. Pharmacol.

Brain Dev.

Early Hum. Dev.

Neuroscience

J. Pain

Comp. Biochem. Physiol. C: Toxicol. Pharmacol.

Neuropharmacology

Brain Res.

Neurosci. Biobehav. Rev.

Research article
Maternal swimming exercise during pregnancy attenuates anxiety/depressive-like behaviors and voluntary morphine consumption in the pubertal male and female rat offspring born from morphine dependent mothers