Aerobic exercise combined with environmental enrichment improves spatial memory and enhances neuroligin 1 expression: an animal study

Authors

  • Faizah Abdullah Djawas Physiotherapy Study Program, Vocational Education Program, Universitas Indonesia, Depok, Indonesia; Master Program in Biomedical Sciences, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia https://orcid.org/0000-0003-3565-6109
  • Sri Redjeki Department of Medical Physiology, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia
  • Ria Kodariah Department of Anatomical Pathology, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia
  • Neng Tine Kartinah Department of Medical Physiology, Faculty of Medicine, Universitas Indonesia, Jakarta, Indonesia

DOI:

https://doi.org/10.13181/mji.v28i3.2109

Keywords:

aerobic exercise, neuroligin 1, neuroplasticity, spatial memory

Abstract

BACKGROUND Numerous studies have revealed that aerobic exercise (AE) or environmental enrichment (EE) exert positive effects on the molecular, cellular, and structural changes responsible for functional plasticity. Therefore, this study was aimed to investigate whether the combination of AE and EE yields a greater effect on spatial memory and increases the expression of the adhesion molecule neuroligin 1 compared with either of the therapies alone.

METHODS Twenty 6-month-old male Wistar rats were randomly divided into four groups: (1) the control group (C), (2) the AE group, (3) the EE group, and (4) the AE-EE group. Escape latency in a Water-E-maze (WEM) task was used as a parameter to assess spatial memory function. Neuroligin 1 protein expression was examined via the immunohistochemistry (IHC) technique followed by IHC optical density (OD) score analysis of the CA1 hippocampal region.

RESULTS Data acquired from the WEM task show that escape latency progressively decreased over time in all groups. However, animals in the AE-EE group required less time to complete the task compared with those in the control, AE, and EE groups. IHC OD scores revealed that the combination of AE and EE caused the highest expression of neuroligin 1 in the CA1 hippocampal region among the therapies studied. Statistical analysis indicated significant differences in OD score between the AE-EE and control, AE, and EE groups (p ≤ 0.001).

CONCLUSIONS The combination of AE and EE rats increased neuroligin 1 expression and improved the spatial memory of male Wistar rats compared with application of either therapy alone.

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References

Salthouse TA. When does age-related cognitive decline begin? Neurobiol Aging. 2009;30(4):507-14. https://doi.org/10.1016/j.neurobiolaging.2008.09.023

Horvath G, Kiss P, Nemeth J, Lelesz B, Tamas A, Reglodi D. Environmental enrichment increases PACAP levels in the CNS of adult rats. Neuro Endocrinol Lett. 2015;36(2):143-7.

Voss MW, Vivar C, Kramer AF, van Praag H. Bridging animal and human models of exercise-induced brain plasticity. Trends Cogn Sci. 2013;17(10):525-44. https://doi.org/10.1016/j.tics.2013.08.001

Kondo M. Molecular mechanisms of experience-dependent structural and functional plasticity in the brain. Anat Sci Int. 2017;92(1):1-17. https://doi.org/10.1007/s12565-016-0358-6

Fang ZH, Lee CH, Seo MK, Cho H, 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(4):187-94. https://doi.org/10.1016/j.neures.2013.04.005

Shih PC, Yang YR, Wang RY. Effects of exercise intensity on spatial memory performance and hippocampal synaptic plasticity in transient brain ischemic rats. PLoS One. 2013;8(10):e78163. https://doi.org/10.1371/journal.pone.0078163

Schapitz IU, Behrend B, Pechmann Y, Lappe-Siefke C, Kneussel SJ, Wallace KE, et al. Neuroligin 1 is dynamically exchanged at postsynaptic sites. J Neurosci. 2010;30(38):12733-44. https://doi.org/10.1523/JNEUROSCI.0896-10.2010

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

Cassilhas RC, Lee KS, Fernandes J, Oliveira MG, Tufik S, Meeusen R, et al. Spatial memory is improved by aerobic and resistance exercise through divergent molecular mechanisms. Neuroscience. 2012;202:309-17. https://doi.org/10.1016/j.neuroscience.2011.11.029

Fares RP, Kouchi H, Bezin L. Standardized environmental enrichment for rodents in Marlau cage. 2012 [cited 2016]. Available from: http://dx.doi.org/10.1038/protex.2012.036. https://doi.org/10.1038/protex.2012.036

Seyed Jafari SM, Hunger RE. IHC optical density score: a new practical method for quantitative immunohistochemistry image analysis. Appl Immunohistochem Mol Morphol. 2017;25(1):e12-e3. https://doi.org/10.1097/PAI.0000000000000370

Makinodan M, Rosen KM, Ito S, Corfas G. A critical period for social experience-dependent oligodendrocyte maturation and myelination. Science. 2012;337(6100):1357-60. https://doi.org/10.1126/science.1220845

Pereda-Pérez I, Popovi? N, Otalora BB, Popovi? M, Madrid JA, Rol MA, et al. Long-term social isolation in the adulthood results in CA1 shrinkage and cognitive impairment. Neurobiology Learn Mem. 2013;106:31-9. https://doi.org/10.1016/j.nlm.2013.07.004

Fischer A. Environmental enrichment as a method to improve cognitive function. What can we learn from animal models? Neuroimage. 2016;131:42-7. https://doi.org/10.1016/j.neuroimage.2015.11.039

Nithianantharajah J, Levis H, Murphy M. Environmental enrichment results in cortical and subcortical changes in levels of synaptophysin and PSD-95 proteins. Neurobiol Learn Mem. 2004;81(3):200-10. https://doi.org/10.1016/j.nlm.2004.02.002

Brito-Moreira J, Lourenco MV, Oliveira MM, Ribeiro FC, Ledo JH, Diniz LP, et al. Interaction of amyloid-v (Av) oligomers with neurexin 2a and neuroligin 1 mediates synapse damage and memory loss in mice. Journal Biol Chem. 2017;292(18):7327-37. https://doi.org/10.1074/jbc.M116.761189

Heine M, Thoumine O, Mondin M, Tessier B, Giannone G, Choquet D. Activity-independent and subunit-specific recruitment of functional AMPA receptors at neurexin/neuroligin contacts. Proc Natl Acad Sci U S A. 2008;105(52):20947-52. https://doi.org/10.1073/pnas.0804007106

El-Husseini AE, Schnell E, Chetkovich DM, Nicoll RA, Bredt DS. PSD-95 involvement in maturation of excitatory synapses. Science. 2000;290(5495):1364-8. https://doi.org/10.1126/science.290.5495.1364

Hu X, Luo JH, Xu J. The interplay between synaptic activity and neuroligin function in the CNS. BioMed Res Int. 2015;2015:498957. https://doi.org/10.1155/2015/498957

Südhof TC. Neuroligins and neurexins link synaptic function to cognitive disease. Nature. 2008;455(7215):903-11. https://doi.org/10.1038/nature07456

Jiang M, Polepalli J, Chen LY, Zhang B, Südhof TC, Malenka RC. Conditional ablation of neuroligin-1 in CA1 pyramidal neurons blocks LTP by a cell-autonomous NMDA receptor-independent mechanism. Mol Psychiatry. 2017;22(3):375-83. https://doi.org/10.1038/mp.2016.80

Kotloski RJ, Sutula TP. Environmental enrichment: evidence for an unexpected therapeutic influence. Exp Neurol. 2015;264:121-6. https://doi.org/10.1016/j.expneurol.2014.11.012

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(3):250-60. https://doi.org/10.1002/hipo.20157

Published

2019-10-04

How to Cite

1.
Djawas FA, Redjeki S, Kodariah R, Kartinah NT. Aerobic exercise combined with environmental enrichment improves spatial memory and enhances neuroligin 1 expression: an animal study. Med J Indones [Internet]. 2019Oct.4 [cited 2024Nov.22];28(3):228-33. Available from: https://mji.ui.ac.id/journal/index.php/mji/article/view/2109

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Section

Basic Medical Research
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