Environmental Enrichment and Aerobic Exercise Enhances Spatial Memory and Synaptophysin Expression in Rats

Diah Ayu Aguspa Dita, Nurul Paramita, Ria Kodariah, Neng Tine Kartinah

Abstract


BACKGROUND: Exposure to environmental enrichment has a positive effect on brain function, including improved cognition. Environmental enrichment has many aspects, including social interactions, object stimulations, and physical activities. Exercise and environmental enrichment can be considered to improve cognitive function with different underlying mechanisms. This study aims to compare the effects of environmental enrichment and aerobic exercise at both synaptic and whole-organism levels using synapyophysin as a measure of synaptic physiology and spatial memory as a measure of cognitive function.

METHODS: A six-week in vivo experimental study on 15, 6-month old male Wistar rats randomly divided into three groups (n=5): aerobic group (A), enriched environment group (EE), and enriched with an aerobic or combined group (EEA). All rats were tested four times in the Water-E maze (WEM) task at weeks 0, 2, 4, and 6 of the study. We used immunohistochemistry to determine the synaptophysin expression in hippocampal CA1 region.

RESULTS: Based on synaptophysin immunostaining, there were higher optical density scores for synaptophysin in hippocampal CA1 region following EEA, but there were no statistically significant differences between groups (ANOVA test, p>0.05). The spatial memory test showed there were significantly reduced travel time and total errors from the 2nd and 4th weeks in the EEA group, respectively (p<0.05).

CONCLUSION: The combination of enriched environment and aerobic exercise seems to rapidly improve spatial memory and enhances the presynaptic protein, synaptophysin in hippocampal CA1 region.

KEYWORDS: aerobic exercise, environmental enrichment, spatial memory, synaptophysin, Water-E maze


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References


Cassilhas RC, Lee KS, Fernandes J, Oliveira MGM, Tufik S, Meeusen R, et al. Spatial memory is improved by aerobic and resistance exercise through divergent molecular mechanisms. Neuroscience. 2012; 202: 309-17, CrossRef.

Triviño-Paredes J, Patten AR, Gil-Mohapel J, Christie BR. The effects of hormones and physical exercise on hippocampal structural plasticity. Front Neuroendocrinol. 2016; 41: 23-43, CrossRef.

Olson AK, Eadie BD, Ernst C, Christie BR. Environmental enrichment and voluntary exercise massively increase neurogenesis in the adult hippocampus via dissociable pathways. Hippocampus. 2006; 16: 250-60, CrossRef.

Van Praag H, Kempermann G, Gage FH. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci. 1999; 2: 266-70, CrossRef.

Ang ET, Dawe GS, Wong PTH, Moochhala S, Ng YK. Alterations in spatial learning and memory after forced exercise. Brain Res. 2006; 1113: 186-93, CrossRef.

Berchtold NC, Castello N, Cotman CW. Exercise and time-dependent benefits to learning and memory. Neuroscience. 2010; 167: 588-97, CrossRef.

Albeck DS, Sano K, Prewitt GE, Dalton L. Mild forced treadmill exercise enhances spatial learning in the aged rat. Behav Brain Res. 2006; 168: 345-8, CrossRef.

Hu S, Ying Z, Gomez-Pinilla F, Frautschy SA. Exercise can increase small heat shock proteins (sHSP) and pre- and post-synaptic proteins in the hippocampus. Brain Res. 2009; 1249: 191-201, CrossRef.

Ferreira AFB, Real CC, Rodrigues AC, Alves AS, Britto LRG. Short-term, moderate exercise is capable of inducing structural, bdnf-independent hippocampal plasticity. Brain Res. 2011; 1425: 111-22, CrossRef.

Nithianantharajah J, Levis HJ, Murphy M. Environmental enrichment results in cortical and subcortical changes in levels of synaptophysin and PSD-95 proteins. Neurobiol Learn Mem. 2004; 81: 200-10, CrossRef.

Valtorta F, Pennuto M, Bonanomi D, Benfenati F. Synaptophysin: Leading actor or walk-on role in synaptic vesicle exocytosis? BioEssays. 2004; 26: 445-53, CrossRef.

Tarsa L, Goda Y. Synaptophysin regulates activity-dependent synapse formation in cultured hippocampal neurons. Proc Natl Acad Sci USA. 2002; 99: 1012-6, CrossRef.

Sze CI, Troncoso JC, Kawas C, Mouton P, Price DL, Martin LJ. Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease. J Neuropathol Exp Neurol. 1997; 56: 933-44, CrossRef.

Fares RP, Kouchi H, Bezin L. Standardized environmental enrichment for rodents in Marlau cage. Protoc Excange [Preprint version]. 2012; 1: n.p, CrossRef.

Furqaani AR. Pengaruh latihan sik terhadap kemampuan belajar dan memori serta kadar serotonin pada hipokampus tikus (Rattus novergicus) galur wistar jantan dewasa [Thesis]. Jakarta: Universitas Indonesia; 2013.

Seyed Jafari SM, Hunger RE. IHC optical density score: a new practical method for quantitative immunohistochemistry image analysis. Appl Immunohistochem Mol Morphol. 2017; 25: e12-3, CrossRef.

Kobilo T, Liu QR, Gandhi K, Mughal M, Shaham Y, van Praag H. Running is the neurogenic and neurotrophic stimulus in environmental enrichment. Learn Mem. 2011; 18: 605-9, CrossRef.

Simpson J, Kelly JP. The impact of environmental enrichment in laboratory rats-Behavioural and neurochemical aspects. Behav Brain Res. 2011; 222: 246-64, CrossRef.

Sale A, Berardi N, Maffei L. Environment and brain plasticity: Towards an endogenous pharmacotherapy. Physiol Rev. 2014; 94: 189-234, CrossRef.

Van Praag H, Shubert T, Zhao C, Gage FH. Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci. 2005; 25: 8680-5, CrossRef.

Wiedenmann B, Franke WW. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell. 1985; 41: 1017-28, CrossRef.

Fang ZH, Lee CH, Seo MK, Cho HY, Lee JG, Lee BJ, et al. Effect of treadmill exercise on the BDNF-mediated pathway in the hippocampus of stressed rats. Neurosci Res. 2013; 76: 187-94, CrossRef.

Lambert TJ, Fernandez SM, Frick KM. Different types of environmental enrichment have discrepant effects on spatial memory and synaptophysin levels in female mice. Neurobiol Learn Mem. 2005; 83: 206-16, CrossRef.

Hescham S, Grace L, Kellaway LA, Bugarith K, Russell VA. Effect of exercise on synaptophysin and calcium/calmodulin-dependent protein kinase levels in prefrontal cortex and hippocampus of a rat model of developmental stress. Metab Brain Dis. 2009; 24: 701-9, CrossRef.

Pozzo-Miller LD, Gottschalk W, Zhang L, McDermott K, Du J, Gopalakrishnan R, et al. Impairments in high-frequency transmission, synaptic vesicle docking, and synaptic protein distribution in the hippocampus of BDNF knockout mice. J Neurosci. 1999; 19: 4972-83, CrossRef.

Vaynman SS, Ying Z, Yin D, Gomez-Pinilla F. Exercise differentially regulates synaptic proteins associated to the function of BDNF. Brain Res. 2006; 1070: 124-30, CrossRef.




DOI: https://doi.org/10.18585/inabj.v12i1.945

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