Elsevier

Physiology & Behavior

Volume 188, 1 May 2018, Pages 58-66
Physiology & Behavior

Voluntary exercise impact on cognitive impairments in sleep-deprived intact female rats

https://doi.org/10.1016/j.physbeh.2017.12.030Get rights and content

Highlights

  • Sleep deprivation (SD) impaired learning in intact female rats.

  • SD impaired long term memory in intact female rats.

  • Voluntary exercise alleviated the SD-induced cognitive impairments in female rats.

  • There was no significant change in the plasma corticosterone level of all groups.

Abstract

Sleep loss is a common problem in modern societies affecting different aspects of individuals' lives. Many studies have reported that sleep deprivation (SD) leads to impairments in various types of learning and memory. Physical exercise has been suggested to attenuate the cognitive impairments induced by sleep deprivation in male rats. Our previous studies have shown that forced exercise by treadmill improved learning and memory impairments following SD. The aim of the current study was to investigate the effects of voluntary exercise by running wheel on cognitive, motor and anxiety-like behavior functions of female rats following 72 h SD.

Intact female rats were used in the present study. The multiple platform method was applied for the induction of 72 h SD. The exercise protocol was 4 weeks of running wheel and the cognitive function was evaluated using Morris water maze (MWM), passive avoidance and novel object recognition tests. Open field test and measurement of plasma corticosterone level were performed for evaluation of anxiety-like behaviors. Motor balance evaluation was surveyed by rotarod test. In this study, remarkable learning and long-term memory impairments were observed in sleep deprived rats in comparison to the other groups. Running wheel exercise ameliorated the SD-induced learning and memory impairments. Voluntary and mandatory locomotion and balance situation were not statistically significant among the different groups.

Our study confirmed the negative effects of SD on cognitive function and approved protective effects of voluntary exercise on these negative effects.

Introduction

Sleep is defined as an active state characterized by reduced alertness and responsiveness that is rapidly reversible [1]. Epidemiological studies show a positive association between adequate sleep and good health [2].

Animal studies have demonstrated the positive effects of sleep on declarative and procedural memory in various behavioral tasks [3,4]. It has been shown that sleep contributes to acquisition and consolidation of memory [5,6]. “Sleep” has been considered as a time window through which the acquired information is processed without any disturbance from the sensory system [7]. It has been identified as a state that optimizes the consolidation of newly acquired information in memory, depending on the specific conditions of learning and timing of sleep. Consolidation during sleep promotes both quantitative and qualitative changes of memory representations [7]. Fragmented sleep and sleep deprivation (SD) in long period can lead to mood changes, impaired mental ability, and disturbed performance [8]. In other studies, SD showed a destructive effect on Morris water maze (MWM) [10], open field [9], novel objective recognition [11,12] and passive avoidance [13,14] tasks. Several clinical studies demonstrate that the absence of periods of sleep is closely related to occurrence of anxiety symptoms [15,16]. Widespread studies suggest that sleep facilitates several phases of learning process and memory in human and rodents while sleep deprivation impairs this process [17,18].

On the other hand, physical exercise has shown to improve learning and memory in both MWM [19,20] and passive avoidance task paradigms [21]. Physical exercise elicits functional and structural changes throughout the brain; however, its effects on the hippocampus are of particular interest as this is a brain area crucial for memory formation and spatial memory [22]. The beneficial effects of exercise on many physiological systems, including the central nervous system and brain health, are well demonstrated [22]. Exercise has been revealed to enhance hippocampus-dependent spatial memory in rodents in different paradigms such as MWM, Y maze and radial arm maze [23,24]. Running also enhances performance in tasks with low motor command such as contextual fear conditioning, passive avoidance learning, spatial pattern separation and novel object recognition [[25], [26], [27]].

SD has negative effects on learning and memory and it appears that exercise protects rats against these negative effects [10]. Our previous studies demonstrated that forced and regular exercise by treadmill ameliorated spatial learning and memory impairments in female sleep deprived rats [10,28]. Exercise also plays a protective role against memory impairments observed in neurodegenerative diseases such as Alzheimer's disease [29].

A recent review from the literature suggests that forced exercise and voluntary exercise have different effects on brain neurochemistry and behavior [30,31]. In contrast, either treadmill exercise or wheel running improves hippocampus-dependent spatial learning and memory [32]. It has been shown that voluntary exercise causes reductions in both dopamine neuron degeneration and behavioral deficits [33].

Considering the effect of voluntary exercise on learning and memory, in this study, we surveyed the effects of voluntary exercise on learning and memory in sleep deprived female rats.

Section snippets

Animals

All experimental protocols and treatments were approved by the Ethics Committee of the Kerman Neuroscience Research Center. We attempted to minimize the discomfort for the animals at all stages of the study (Ethics code: KNRC-95-30). Female Wistar rats (3–4 months old, weighing 200–250 g) were used for the current study. Animals (n = 7 in each group) were caged in groups of four with ad libitum access to food and water. They were housed under controlled temperature (23 ± 1 °C) and 12-h

Effects of sleep deprivation (SD) and voluntary exercise on spatial learning and memory

During the acquisition phase, animals in all the groups except the SD group learned to find a hidden platform as observed by the reduction in their swimming distance and their escape latency across blocks of training (Fig. 2A and B).

Two-way analysis of ANOVA with repeated measures test indicated that the distance and escape latency of the SD group significantly increased in block 2 (Fig.2A: F(5,36) = 7.909 & p < 0.001 and Fig. 1B: F(5,36) = 2.676 & p < 0.05) and block 3 (Fig. 2A:

Discussion

This study was initiated with the aim of assessing the importance of voluntary exercise as a non-pharmacological interference on learning and memory impairments in sleep deprived female rats.

This study investigated the effects of four weeks of wheel running exercise on learning and memory, anxiety like behaviors and motor activity following SD and voluntary exercise in female rats. In this study, as our previous studies, we approved that SD can disrupt learning and memory. Results also

Conclusion

In conclusion, the findings of this study demonstrated that voluntary wheel running exercise attenuated SD-induced impairments of spatial learning as well as memory and recognition memory. The exercise was also shown to improve SD-induced impairments of passive avoidance learning and memory in the female rats. Moreover, voluntary exercise could ameliorate anxiety-like behaviors in the sleep deprived female rats. However, our findings revealed that SD and voluntary exercise had no effect on

Limitations

In this study, we did not measure esterous cycle, which is intended to be investigated in detail in our future work.

Acknowledgement

This research article is part of the first author's MSc thesis. We would like to acknowledge the Neuroscience Research Center of Kerman, Iran (Grant No: KNRC-95-30) for financial support. We would also like to express our gratitude to faculty members of the department of physiology and pharmacology and neuroscience research center in Kerman University of Medical Sciences.

References (65)

  • M.W. Voss et al.

    Bridging animal and human models of exercise-induced brain plasticity

    Trends Cogn. Sci.

    (2013)
  • R.M. O'Callaghan et al.

    The effects of forced exercise on hippocampal plasticity in the rat: a comparison of LTP, spatial- and non-spatial learning

    Behav. Brain Res.

    (2007)
  • W.A. Falls et al.

    Voluntary exercise improves both learning and consolidation of cued conditioned fear in C57 mice

    Behav. Brain Res.

    (2010)
  • H. Saadati et al.

    Exercise improves learning and memory impairments in sleep deprived female rats

    Physiol. Behav.

    (2015)
  • R. Hoveida et al.

    Treadmill running improves spatial memory in an animal model of Alzheimer's disease

    Behav. Brain Res.

    (2011)
  • M.R. Landers et al.

    A comparison of voluntary and forced exercise in protecting against behavioral asymmetry in a juvenile hemiparkinsonian rat model

    Behav. Brain Res.

    (2013)
  • F.M. Howells et al.

    Stress reduces the neuroprotective effect of exercise in a rat model for Parkinson's disease

    Behav. Brain Res.

    (2005)
  • S.J. O'Dell et al.

    Running wheel exercise enhances recovery from nigrostriatal dopamine injury without inducing neuroprotection

    Neuroscience

    (2007)
  • V. Hajali et al.

    Female rats are more susceptible to the deleterious effects of paradoxical sleep deprivation on cognitive performance

    Behav. Brain Res.

    (2012)
  • K. Esmaeilpour et al.

    Effect of low frequency electrical stimulation on seizure-induced short- and long-term impairments in learning and memory in rats

    Physiol. Behav.

    (2017)
  • H. Abbassian et al.

    Cannabinoid receptor agonism suppresses tremor, cognition disturbances and anxiety-like behaviors in a rat model of essential tremor

    Physiol. Behav.

    (2016)
  • Z. Vaziri et al.

    The therapeutic potential of Berberine chloride hydrate against harmaline-induced motor impairments in a rat model of tremor

    Neurosci. Lett.

    (2015)
  • R.B. Machado et al.

    Sleep deprivation induced by the modified multiple platform technique: quantification of sleep loss and recovery

    Brain Res.

    (2004)
  • P.S. Green et al.

    Neuroprotective effects of estrogens: potential mechanisms of action

    Int. J. Dev. Neurosci.

    (2000)
  • J. Ben et al.

    Running exercise effects on spatial and avoidance tasks in ovariectomized rats

    Neurobiol. Learn. Mem.

    (2010)
  • E.Y. Kim et al.

    REM sleep deprivation inhibits LTP in vivo in area CA1 of rat hippocampus

    Neurosci. Lett.

    (2005)
  • M. Zagaar et al.

    The beneficial effects of regular exercise on cognition in REM sleep deprivation: behavioral, electrophysiological and molecular evidence

    Neurobiol. Dis.

    (2012)
  • Z. Guan et al.

    Sleep deprivation impairs spatial memory and decreases extracellular signal-regulated kinase phosphorylation in the hippocampus

    Brain Res.

    (2004)
  • T.A. Alvarenga et al.

    Paradoxical sleep deprivation impairs acquisition, consolidation, and retrieval of a discriminative avoidance task in rats

    Neurobiol. Learn. Mem.

    (2008)
  • M. Coll-Andreu et al.

    Facilitation of shuttle-box avoidance by the platform method: temporal effects

    Physiol. Behav.

    (1991)
  • Z.J. van Hulzen et al.

    Effects of paradoxical sleep deprivation on two-way avoidance acquisition

    Physiol. Behav.

    (1982)
  • L. Chen et al.

    Rapid eye movement sleep deprivation disrupts consolidation but not reconsolidation of novel object recognition memory in rats

    Neurosci. Lett.

    (2014)
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