Maternal Exercise during Pregnancy Increases BDNF Levels and Cell Numbers in the Hippocampal Formation but Not in the Cerebral Cortex of Adult Rat Offspring.

Sérgio Gomes Da Silva,Jansen Fernandes,Alexandre Aparecido De Almeida,Ana Virgínia De Oliveira-Pinto,Débora Amado Scerni,Roberto Lent,Francisco Romero Cabral,Glauber Menezes Lopim,Ricardo Mario Arida,Georges Chapouthier

doi:10.1371/journal.pone.0147200

Abstract

Clinical evidence has shown that physical exercise during pregnancy may alter brain development and improve cognitive function of offspring. However, the mechanisms through which maternal exercise might promote such effects are not well understood. The present study examined levels of brain-derived neurotrophic factor (BDNF) and absolute cell numbers in the hippocampal formation and cerebral cortex of rat pups born from mothers exercised during pregnancy. Additionally, we evaluated the cognitive abilities of adult offspring in different behavioral paradigms (exploratory activity and habituation in open field tests, spatial memory in a water maze test, and aversive memory in a step-down inhibitory avoidance task). Results showed that maternal exercise during pregnancy increased BDNF levels and absolute numbers of neuronal and non-neuronal cells in the hippocampal formation of offspring. No differences in BDNF levels or cell numbers were detected in the cerebral cortex. It was also observed that offspring from exercised mothers exhibited better cognitive performance in nonassociative (habituation) and associative (spatial learning) mnemonic tasks than did offspring from sedentary mothers. Our findings indicate that maternal exercise during pregnancy enhances offspring cognitive function (habituation behavior and spatial learning) and increases BDNF levels and cell numbers in the hippocampal formation of offspring.

Highlights

Brain development is a highly plastic process that in humans starts in utero and extends at least through late adolescence
We determined levels of brain-derived neurotrophic factor (BDNF) and absolute cell numbers in the hippocampal formation and cerebral cortex of rat pups born from mothers exercised during pregnancy
The present study assessed some molecular and cellular changes in the hippocampal formation and cerebral cortex of rats born from mothers submitted to treadmill exercise during pregnancy

Summary

Introduction

Brain development is a highly plastic process that in humans starts in utero and extends at least through late adolescence. Studies have shown that exercise during pregnancy affects various brain functions in pups [3,4,5,6,7] and mitigates the effects of an Alzheimer-like pathology in adult offspring [10] These findings result from experiments in which several cognitive tests and models of physical exercise were applied, including forced running on a treadmill, forced swimming, and voluntary wheel running. In a more recent study [7], the offspring of rats with free access to a running wheel throughout gestation were better at discriminating between novel and familiar objects in a memory task than the offspring of sedentary rats Taken together, these data suggest that maternal exercise during gestation enhances offspring brain function throughout life. We evaluated the cognitive abilities of the pups in different behavioral paradigms (exploratory activity and habituation in open field tests, spatial memory in a water maze test, and aversive memory in a step-down inhibitory avoidance task)

Materials and Methods

Results

Discussion