Voluntary exercise impact on cognitive impairments in sleep-deprived intact female rats
Graphical abstract
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)
- et al.
Sleep loss, learning capacity and academic performance
Sleep Med. Rev.
(2006) - et al.
The compensatory effect of regular exercise on long-term memory impairment in sleep deprived female rats
Behav. Process.
(2015) - et al.
Sleep deprivation impairs object recognition in mice
Neurobiol. Learn. Mem.
(2006) - et al.
Sleep enhances memory consolidation in the hippocampus-dependent object-place recognition task in rats
Neurobiol. Learn. Mem.
(2012) Acquisition impairments following rapid eye movement sleep deprivation in rats
Physiol. Behav.
(1971)- et al.
Role of hippocampal oxidative stress in memory deficits induced by sleep deprivation in mice
Neuropharmacology
(2004) - et al.
Exercise prevents sleep deprivation-associated anxiety-like behavior in rats: potential role of oxidative stress mechanisms
Behav. Brain Res.
(2011) - et al.
Short bouts of mild-intensity physical exercise improve spatial learning and memory in aging rats: involvement of hippocampal plasticity via AKT, CREB and BDNF signaling
Mech. Ageing Dev.
(2011) - et al.
Exercise: a behavioral intervention to enhance brain health and plasticity
Trends Neurosci.
(2002) - et al.
Enhancement of spatial learning in F344 rats by physical activity and related learning-associated alterations in hippocampal and cortical cholinergic functioning
Behav. Brain Res.
(1991)
Bridging animal and human models of exercise-induced brain plasticity
Trends Cogn. Sci.
The effects of forced exercise on hippocampal plasticity in the rat: a comparison of LTP, spatial- and non-spatial learning
Behav. Brain Res.
Voluntary exercise improves both learning and consolidation of cued conditioned fear in C57 mice
Behav. Brain Res.
Exercise improves learning and memory impairments in sleep deprived female rats
Physiol. Behav.
Treadmill running improves spatial memory in an animal model of Alzheimer's disease
Behav. Brain Res.
A comparison of voluntary and forced exercise in protecting against behavioral asymmetry in a juvenile hemiparkinsonian rat model
Behav. Brain Res.
Stress reduces the neuroprotective effect of exercise in a rat model for Parkinson's disease
Behav. Brain Res.
Running wheel exercise enhances recovery from nigrostriatal dopamine injury without inducing neuroprotection
Neuroscience
Female rats are more susceptible to the deleterious effects of paradoxical sleep deprivation on cognitive performance
Behav. Brain Res.
Effect of low frequency electrical stimulation on seizure-induced short- and long-term impairments in learning and memory in rats
Physiol. Behav.
Cannabinoid receptor agonism suppresses tremor, cognition disturbances and anxiety-like behaviors in a rat model of essential tremor
Physiol. Behav.
The therapeutic potential of Berberine chloride hydrate against harmaline-induced motor impairments in a rat model of tremor
Neurosci. Lett.
Sleep deprivation induced by the modified multiple platform technique: quantification of sleep loss and recovery
Brain Res.
Neuroprotective effects of estrogens: potential mechanisms of action
Int. J. Dev. Neurosci.
Running exercise effects on spatial and avoidance tasks in ovariectomized rats
Neurobiol. Learn. Mem.
REM sleep deprivation inhibits LTP in vivo in area CA1 of rat hippocampus
Neurosci. Lett.
The beneficial effects of regular exercise on cognition in REM sleep deprivation: behavioral, electrophysiological and molecular evidence
Neurobiol. Dis.
Sleep deprivation impairs spatial memory and decreases extracellular signal-regulated kinase phosphorylation in the hippocampus
Brain Res.
Paradoxical sleep deprivation impairs acquisition, consolidation, and retrieval of a discriminative avoidance task in rats
Neurobiol. Learn. Mem.
Facilitation of shuttle-box avoidance by the platform method: temporal effects
Physiol. Behav.
Effects of paradoxical sleep deprivation on two-way avoidance acquisition
Physiol. Behav.
Rapid eye movement sleep deprivation disrupts consolidation but not reconsolidation of novel object recognition memory in rats
Neurosci. Lett.
Cited by (27)
The stress of losing sleep: Sex-specific neurobiological outcomes
2023, Neurobiology of StressThe effects of neurosteroid allopregnanolone on synaptic dysfunction in the hippocampus in experimental parkinsonism rats: An electrophysiological and molecular study
2022, NeuropeptidesCitation Excerpt :When a statistical significance was found between the groups, Tukey's post-hoc multiple comparison test was performed to determine the points of significant difference. The data were expressed as mean ± S.E.M., and P < 0.05 was considered statistically significant (Rajizadeh et al., 2018). At the beginning of each experiment, to measure the effect of 6-OHDA or Allo treatment on basal synaptic performance, an input-output (IO) curve was plotted as changes in the slope of fEPSP against increasing stimulus intensities.
Voluntary exercise modulates learning & memory and synaptic plasticity impairments in sleep deprived female rats
2020, Brain ResearchCitation Excerpt :This method also eliminates both the isolation and immobilization stress associated with the other methods (Suchecki and Tufik, 2000). Several studies have confirmed the important correlation between REM sleep and cognitive functions (Diekelmann and Born, 2010; Hajali et al., 2012; Rajizadeh et al., 2018). However, sleep deprivation impairs learning and memory consolidation in several paradigms such as Morris water maze (Hajali et al., 2012; Rajizadeh et al., 2018; Rajizadeh et al., 2019; Saadati et al., 2015; Salari et al., 2015) & radial arm water maze (Zagaar et al., 2012, 2013b) & novel objective recognition test (Chen et al., 2014; Rajizadeh et al., 2018) and passive and active avoidance (Rajizadeh et al., 2018).
Catecholaminergic hippocampal activation is necessary for object recognition memory persistence induced by one-single physical exercise session
2020, Behavioural Brain ResearchCitation Excerpt :In addition, studies suggest that factors such as the duration of exercise, and the type of exercise performed (eg, forced vs. voluntary) could influence the results observed [33]. There are evidences about the benefits of both forced and voluntary aerobic exercise [18,34,35]. In the voluntary exercise the animal has free access to the execution of the activity to perform it on a voluntary basis, such as in activity wheels [36]; while in the forced exercise, the animal is obliged to perform the physical exercise in an intensity and duration determined by the experimenter, such as running on a treadmill [37].