Volume 5, Issue 2 (5-2023)                   IJMCL 2023, 5(2): 21-28 | Back to browse issues page

XML Print

Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:

Abdollahzadeh M, Tahmasebi Boroujeni S, Arabameri E. (2023). Does Swimming Moderate the Negative Effects of Maternal Deprivation on Hippocampal BDNF Levels, Spatial Learning and Motor Function?. IJMCL. 5(2), 21-28. doi:10.61186/ijmcl.5.2.21
URL: http://ijmcl.com/article-1-139-en.html
Associate Professor, Department of Behavioral and Cognitive Sciences in Sport, Faculty of Sport Sciences and Health, University of Tehran, Tehran, Iran. , shahzadtahmaseb@ut.ac.ir
Abstract:   (688 Views)
Background: Previous research has emphasized the negative impact of early maternal deprivation on learning and memory. On the other hand, the role of training on cognition has been examined. However, whether neonates are given exercise at the same time as being deprived of their mothers is a novelty of this research. We also considered the study of underlying mechanisms, such as the study of changes in BDNF levels.  So, the purpose of this study was to examine the effect of swimming training on spatial learning, memory and motor function in male rats under early deprivation. Methods: Twenty-eight rats divided into four groups: Early maternal deprivation (EMD), Swimming Training (ST), EMD+ST group, and Control (CON) groups. The rats were exposed to deprivation for 10 days, three days a week for 30 minutes. The rats were at 33 postnatal days and their spatial learning and memory were assessed using the Morris Water Maze (MWM) test. Rats' motor function was assessed by the Open-Field (OF) test. Finally, after the extraction of the hippocampus, BDNF protein was measured by ELISA. Results: The results of this study revealed that male rats exposed to EMD had learning and spatial memory impairments, lower hippocampal BDNF protein levels. In addition, swimming alone has a positive impact on the BDNF protein level and motor function. Conclusions: Despite these findings, due to the high intensity of stress, swimming could not modify the irreparable effects of deprivation.

Full-Text [PDF 660 kb]   (159 Downloads)    
  • Rats exposed to Early maternal deprivation (EMD) + Swimming Training (ST) and individual ST groups.
  • The memory of the offspring measured by the level of the BDNF, MWM test, and OF test.
  • Early deprivation decreased hippocampal BDNF level significantly.
  • ST moderated the adverse effect of early deprivation.
  • ST as a non-pharmacological solution would moderate the effects of stress caused by EMD.

Type of Study: Original Article | Subject: 1. Motor learning
Received: 2023/02/6 | Accepted: 2023/05/13

1. Wiersma JE, Hovens JGFM, van Oppen P, et al. The Importance of Childhood Trauma and Childhood Life Events for Chronicity of Depression in Adults. J Clin Psychiatry. 2009;70(7). doi:10.4088/JCP.08m04521 [DOI:10.4088/JCP.08m04521]
2. Cooke L. The importance of exposure for healthy eating in childhood: A review. J Hum Nutr Diet. 2007;20(4):294-301. doi:10.1111/j.1365-277X.2007.00804.x [DOI:10.1111/j.1365-277X.2007.00804.x]
3. Braun K, Lange E, Metzger M, Poeggel G. Maternal separation followed by early social deprivation affects the development of monoaminergic fiber systems in the medial prefrontal cortex of Octodon degus. Neuroscience. 1999;95(1). doi:10.1016/S0306-4522(99)00420-0 [DOI:10.1016/S0306-4522(99)00420-0]
4. Fries ABW, Shirtcliff EA, Pollak SD. Neuroendocrine dysregulation following early social deprivation in children. Dev Psychobiol. 2008;50(6). doi:10.1002/dev.20319 [DOI:10.1002/dev.20319]
5. Lévy F, Melo AI, Galef BG, Madden M, Fleming AS. Complete maternal deprivation affects social, but not spatial, learning in adult rats. Dev Psychobiol. 2003;43(3). doi:10.1002/dev.10131 [DOI:10.1002/dev.10131]
6. Ahun MN, Côté SM. Maternal depressive symptoms and early childhood cognitive development: a review of putative environmental mediators. Arch Womens Ment Health. 2019;22(1):15-24. doi:10.1007/s00737-018-0870-x [DOI:10.1007/s00737-018-0870-x]
7. Kiernan KE, Huerta MC. Economic deprivation, maternal depression, parenting and children's cognitive and emotional development in early childhood1. Br J Sociol. 2008;59(4). doi:10.1111/j.1468-4446.2008.00219.x [DOI:10.1111/j.1468-4446.2008.00219.x]
8. Bessières B, Travaglia A, Mowery TM, Zhang X, Alberini CM. Early life experiences selectively mature learning and memory abilities. Nat Commun. 2020;11(1). doi:10.1038/s41467-020-14461-3 [DOI:10.1038/s41467-020-14461-3]
9. Loi M, Mossink JCL, Meerhoff GF, Den Blaauwen JL, Lucassen PJ, Joëls M. Effects of early-life stress on cognitive function and hippocampal structure in female rodents. Neuroscience. 2017;342. doi:10.1016/j.neuroscience.2015.08.024 [DOI:10.1016/j.neuroscience.2015.08.024]
10. Janetsian-Fritz SS, Timme NM, Timm MM, et al. Maternal deprivation induces alterations in cognitive and cortical function in adulthood. Transl Psychiatry. 2018;8(1). doi:10.1038/s41398-018-0119-5 [DOI:10.1038/s41398-018-0119-5]
11. Song MK, Kim EJ, Kim JK, Park HK, Lee SG. Effect of regular swimming exercise to duration-intensity on neurocognitive function in cerebral infarction rat model. Neurol Res. 2019;41(1):37-44. doi:10.1080/01616412.2018.1524087 [DOI:10.1080/01616412.2018.1524087]
12. e Silva-Gondim MB, de Souza TKM, Rodrigues MCA, Guedes RCA. Suckling in litters with different sizes, and early and late swimming exercise differentially modulates anxiety-like behavior, memory and electrocorticogram potentiation after spreading depression in rats. Nutr Neurosci. 2019;22(7). doi:10.1080/1028415X.2017.1407472 [DOI:10.1080/1028415X.2017.1407472]
13. Robinson AM, Bucci DJ. Physical exercise during pregnancy improves object recognition memory in adult offspring. Neuroscience. 2014;256. doi:10.1016/j.neuroscience.2013.10.012 [DOI:10.1016/j.neuroscience.2013.10.012]
14. Kim H, Lee SH, Kim SS, Yoo JH, Kim CJ. The influence of maternal treadmill running during pregnancy on short-term memory and hippocampal cell survival in rat pups. Int J Dev Neurosci. 2007;25(4):243-249. doi:10.1016/j.ijdevneu.2007.03.003 [DOI:10.1016/j.ijdevneu.2007.03.003]
15. Akhavan MM, Emami-Abarghoie M, Safari M, et al. Serotonergic and noradrenergic lesions suppress the enhancing effect of maternal exercise during pregnancy on learning and memory in rat pups. Neuroscience. 2008;151(4). doi:10.1016/j.neuroscience.2007.10.051 [DOI:10.1016/j.neuroscience.2007.10.051]
16. Zhang X, Li H, Sun H, et al. Effects of BDNF Signaling on Anxiety-Related Behavior and Spatial Memory of Adolescent Rats in Different Length of Maternal Separation. Front Psychiatry. 2020;11. doi:10.3389/fpsyt.2020.00709 [DOI:10.3389/fpsyt.2020.00709]
17. Roceri M, Hendriks W, Racagni G, Ellenbroek BA, Riva MA. Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol Psychiatry. 2002;7(6). doi:10.1038/sj.mp.4001036 [DOI:10.1038/sj.mp.4001036]
18. DastAmooz S, Tahmasebi Boroujeni S, Shahbazi M, Vali Y. Physical activity as an option to reduce adverse effect of EMF exposure during pregnancy. Int J Dev Neurosci. 2018;71. doi:10.1016/j.ijdevneu.2018.07.009 [DOI:10.1016/j.ijdevneu.2018.07.009]
19. Iñiguez SD, Parise LF, Lobo MK, et al. Upregulation of hippocampal extracellular signal-regulated kinase (ERK)-2 induces antidepressant-like behavior in the rat forced swim test. Behav Neurosci. 2019;133(2). doi:10.1037/bne0000303 [DOI:10.1037/bne0000303]
20. Venkataramaiah C, Swathi G, Rajendra W. Morris Water Maze - A Bench Mark Test For Learning And Memory Disorders In Animal Models: A Review. Asian J Pharm Clin Res. 2018;11(5). doi:10.22159/ajpcr.2018.v11i5.24292 [DOI:10.22159/ajpcr.2018.v11i5.24292]
21. DastAmooz S, Tahmasebi Boroujeni S, Shahbazi M, Vali Y. Physical activity as an option to reduce adverse effect of EMF exposure during pregnancy. Int J Dev Neurosci. Published online 2018. doi:10.1016/j.ijdevneu.2018.07.009 [DOI:10.1016/j.ijdevneu.2018.07.009]
22. Naghdi N, Majlessi N, Bozorgmehr T. The effect of intrahippocampal injection of testosterone enanthate (an androgen receptor agonist) and anisomycin (protein synthesis inhibitor) on spatial learning and memory in adult, male rats. Behav Brain Res. 2005;156(2). doi:10.1016/j.bbr.2004.05.032 [DOI:10.1016/j.bbr.2004.05.032]
23. Sherif F, Oreland L. Effect of the GABA-transaminase inhibitor vigabatrin on exploratory behaviour in socially isolated rats. Behav Brain Res. 1995;72(1-2). doi:10.1016/0166-4328(96)00047-2 [DOI:10.1016/0166-4328(96)00047-2]
24. Gomes da Silva S, de Almeida AA, Fernandes J, et al. Maternal Exercise during Pregnancy Increases BDNF Levels and Cell Numbers in the Hippocampal Formation but Not in the Cerebral Cortex of Adult Rat Offspring. PLoS One. 2016;11(1). doi:10.1371/journal.pone.0147200 [DOI:10.1371/journal.pone.0147200]
25. Lee HH, Kim H, Lee JW, et al. Maternal swimming during pregnancy enhances short-term memory and neurogenesis in the hippocampus of rat pups. Brain Dev. 2006;28(3):147-154. doi:10.1016/j.braindev.2005.05.007 [DOI:10.1016/j.braindev.2005.05.007]
26. Rees SL, Akbari E, Steiner M, Fleming AS. Effects of early deprivation and maternal separation on pup-directed behavior and HPA axis measures in the juvenile female rat. Dev Psychobiol. 2008;50(4). doi:10.1002/dev.20292 [DOI:10.1002/dev.20292]
27. Daniels WMU, Marais L, Stein DJ, Russell VA. Exercise normalizes altered expression of proteins in the ventral hippocampus of rats subjected to maternal separation. Exp Physiol. 2012;97(2). doi:10.1113/expphysiol.2011.061176 [DOI:10.1113/expphysiol.2011.061176]
28. Wang D, Li B, Wu Y, Li B. The Effects of Maternal Atrazine Exposure and Swimming Training on Spatial Learning Memory and Hippocampal Morphology in Offspring Male Rats via PSD95/NR2B Signaling Pathway. Cell Mol Neurobiol. 2019;39(7). doi:10.1007/s10571-019-00695-3 [DOI:10.1007/s10571-019-00695-3]
29. Tanapat P, Hastings NB, Rydel TA, Galea LAM, Gould E. Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J Comp Neurol. 2001;437(4). doi:10.1002/cne.1297 [DOI:10.1002/cne.1297]
30. Faure J, Uys JDK, Marais L, Stein DJ, Daniels WMU. Early maternal separation alters the response to traumatization: resulting in increased levels of hippocampal neurotrophic factors. Metab Brain Dis. 2007;22(2). doi:10.1007/s11011-007-9048-3 [DOI:10.1007/s11011-007-9048-3]
31. Czarnabay D, Dalmago J, Martins AS, et al. Repeated three-hour maternal deprivation as a model of early-life stress alters maternal behavior, olfactory learning and neural development. Neurobiol Learn Mem. 2019;163. doi:10.1016/j.nlm.2019.107040 [DOI:10.1016/j.nlm.2019.107040]
32. Conrad CD. A critical review of chronic stress effects on spatial learning and memory. Prog Neuro-Psychopharmacology Biol Psychiatry. 2010;34(5). doi:10.1016/j.pnpbp.2009.11.003 [DOI:10.1016/j.pnpbp.2009.11.003]
33. Zhang X, Wang B, Jin J, et al. Early deprivation reduced anxiety and enhanced memory in adult male rats. Brain Res Bull. 2014;108. doi:10.1016/j.brainresbull.2014.08.005 [DOI:10.1016/j.brainresbull.2014.08.005]
34. McLaughlin KJ, Baran SE, Wright RL, Conrad CD. Chronic stress enhances spatial memory in ovariectomized female rats despite CA3 dendritic retraction: Possible involvement of CA1 neurons. Neuroscience. 2005;135(4). doi:10.1016/j.neuroscience.2005.06.083 [DOI:10.1016/j.neuroscience.2005.06.083]
35. Irandoost K, Taheri M, Dev AS-JML, 2014 U. The effects swimming and running training protocol on motor function, learning, spatial memory of old rats. Mot Learn Growth. 2014;2(14):1-16.
36. Dimitrijević L, Aleksandrović M, Madić D, Okičić T, Radovanović D, Daly D. The Effect of Aquatic Intervention on the Gross Motor Function and Aquatic Skills in Children with Cerebral Palsy. J Hum Kinet. 2012;32(2012). doi:10.2478/v10078-012-0033-5 [DOI:10.2478/v10078-012-0033-5]
37. Swain R., Harris A., Wiener E., et al. Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience. 2003;117(4). doi:10.1016/S0306-4522(02)00664-4 [DOI:10.1016/S0306-4522(02)00664-4]
38. Pollock BS, Peacock CA, Ryan EJ, Spitznagel MB, Ridgel AL. A multifaceted exercise intervention did not alter cognitive function and cerebral perfusion in individuals with Parkinson's disease. Sci Sport. Published online 2019. doi:10.1016/j.scispo.2019.05.008 [DOI:10.1016/j.scispo.2019.05.008]
39. Antunes BM, Rossi FE, Teixeira AM, Lira FS. Short-time high-intensity exercise increases peripheral BDNF in a physical fitness-dependent way in healthy men. Eur J Sport Sci. 2020;20(1). doi:10.1080/17461391.2019.1611929 [DOI:10.1080/17461391.2019.1611929]
40. Yarrow JF, White LJ, McCoy SC, Borst SE. Training augments resistance exercise induced elevation of circulating brain derived neurotrophic factor (BDNF). Neurosci Lett. 2010;479(2). doi:10.1016/j.neulet.2010.05.058 [DOI:10.1016/j.neulet.2010.05.058]
41. Huang T, Larsen KT, Ried-Larsen M, Møller NC, Andersen LB. The effects of physical activity and exercise on brain-derived neurotrophic factor in healthy humans: A review. Scand J Med Sci Sports. 2014;24(1). doi:10.1111/sms.12069 [DOI:10.1111/sms.12069]
42. Shahroodi A, Mohammadi F, Vafaei AA, Miladi-Gorji H, Bandegi AR, Rashidy-Pour A. Impact of different intensities of forced exercise on deficits of spatial and aversive memory, anxiety-like behavior, and hippocampal BDNF during morphine abstinence period in male rats. Metab Brain Dis. 2020;35(1). doi:10.1007/s11011-019-00518-w [DOI:10.1007/s11011-019-00518-w]
43. Håkansson K, Ledreux A, Daffner K, et al. BDNF Responses in Healthy Older Persons to 35 Minutes of Physical Exercise, Cognitive Training, and Mindfulness: Associations with Working Memory Function. J Alzheimer's Dis. 2017;55(2):645-657. doi:10.3233/JAD-160593 [DOI:10.3233/JAD-160593]
44. Szuhany KL, Otto MW. Assessing BDNF as a mediator of the effects of exercise on depression. J Psychiatr Res. 2020;123. doi:10.1016/j.jpsychires.2020.02.003 [DOI:10.1016/j.jpsychires.2020.02.003]
45. Mir ahmad, azarbayjani mohammad ali, matin homai hasan, Fanaei H. Effect of Resistance and Aerobic Exercises with Different Intensities on BDNF & TrkB Receptor Gene Expression in Ovariectomized Mice. Complement Med J. 2018;8(2):2304-2316. Accessed June 10, 2021. https://cmja.arakmu.ac.ir/article-1-574-en.html
46. Sattarzadeh1 M H, Tahmasebi Boroujeni S, shahbazi M. Effect of Swimming Training on Spatial Memory of Maternal Deprived Infants: Inducing Stress by Six Hours Separation per Day. Journal title 2022; 30 (3) :88-100 [DOI:10.52547/sjimu.30.3.88]
47. URL: http://sjimu.medilam.ac.ir/article-1-7376-en.html
48. Jéssica, Fragoso., Allan, de, Oliveira, Lira., Guilherme, Souza, Chagas., Carolina, Cadete, Lucena, Cavalcanti., Renata, Beserra., Gisélia, de, Santana-Muniz., Adriano, Bento-Santos., Gerffeson, Willian, Martins., Luciano, Pirola., Raquel, da, Silva, Aragão., Carol, Góis, Leandro. (2017). Maternal voluntary physical activity attenuates delayed neurodevelopment in malnourished rats. Experimental Physiology, 102(11):1486-1499. doi: 10.1113/EP086400 [DOI:10.1113/EP086400]
49. Kholghi, G., Alipour, V., Rezaie, M., Zarrindast, M. R., & Vaseghi, S. (2023). The Interaction Effect of Sleep Deprivation and Treadmill Exercise in Various Durations on Spatial Memory with Respect to the Oxidative Status of Rats. Neurochemical Research, 1-16. [DOI:10.1007/s11064-023-03890-3]
50. Shekarchian, M., Peeri, M., & Azarbayjani, M. A. (2023). Physical activity in a swimming pool attenuates memory impairment by reducing glutamate and inflammatory cytokines and increasing BDNF in the brain of mice with type 2 diabetes. Brain Research Bulletin, 110725. [DOI:10.1016/j.brainresbull.2023.110725]
51. Eduardo, Farias, Sanches., Yohan, van, de, Looij., Yohan, van, de, Looij., Audrey, Toulotte., Analina, R., da, Silva., Jacqueline, Romero., Stéphane, Sizonenko. (2018). Brain Metabolism Alterations Induced by Pregnancy Swimming Decreases Neurological Impairments Following Neonatal Hypoxia-Ischemia in Very Immature Rats.. Frontiers in Neurology, 9:480-480. doi: 10.3389/FNEUR.2018.00480 [DOI:10.3389/fneur.2018.00480]
52. Somayeh, Niknazar., Somayeh, Niknazar., Arezo, Nahavandi., Ali, Asghar, Peyvandi., Hassan, Peyvandi., Fatemeh, Zare, Mehrjerdi., Mohsen, Karimi. (2017). Effect of Maternal Stress Prior to Conception on Hippocampal BDNF Signaling in Rat Offspring.. Molecular Neurobiology, 54(8):6436-6445. doi: 10.1007/S12035-016-0143-5 [DOI:10.1007/s12035-016-0143-5]
53. Gislaine, Z., Réus., Roberto, B., Stringari., Karine, F., Ribeiro., Andreza, L., Cipriano., Bruna, Panizzutti., Laura, Stertz., Camila, Lersch., Flávio, Kapczinski., João, Quevedo. (2011). Maternal Deprivation Induces Depressive-like Behaviour and Alters Neurotrophin Levels in the Rat Brain. Neurochemical Research, 36(3):460-466. doi: 10.1007/S11064-010-0364-3 [DOI:10.1007/s11064-010-0364-3]
54. Rose, Mary, Carvalho, Pinheiro., Maria, Noêmia, Martins, de, Lima., Bernardo, Chaves, D'avila, Portal., Stefano, Boemler, Busato., Lucio, Falavigna., Rafael, Dal, Ponte, Ferreira., André, Vinícius, Contri, Paz., Bianca, Wollenhaupt, de, Aguiar., Flávio, Kapczinski., Nadja, Schröder. (2015). Long-lasting recognition memory impairment and alterations in brain levels of cytokines and BDNF induced by maternal deprivation: effects of valproic acid and topiramate. Journal of Neural Transmission, 122(5):709-719. doi: 10.1007/S00702-014-1303-2 [DOI:10.1007/s00702-014-1303-2]
55. Gislaine, Z., Réus., Maria, Augusta, B, Dos, Santos., Helena, M., Abelaira., Karine, F., Ribeiro., Fabricia, Petronilho., Francieli, Vuolo., Gabriela, D., Colpo., Bianca, Pfaffenseller., Flávio, Kapczinski., Felipe, Dal-Pizzol., João, Quevedo. (2013). Imipramine reverses alterations in cytokines and BDNF levels induced by maternal deprivation in adult rats.. Behavioural Brain Research, 242(1):40-46. doi: 10.1016/J.BBR.2012.11.044 [DOI:10.1016/j.bbr.2012.11.044]
56. Min, Chen., Guoping, He., Qiang, Li. (2018). Maternal deprivation promotes hippocampal neuronal apoptosis via ERK1/2 signaling.. Frontiers in Bioscience, 23(10):1923-1932. doi: 10.2741/4681 [DOI:10.2741/4681]
57. Leena, N., Shoemaker., Luke, C., Wilson., Samuel, J., E., Lucas., Samuel, J., E., Lucas., Liana, Machado., Kate, N., Thomas., James, D., Cotter. (2019). Swimming-related effects on cerebrovascular and cognitive function. Physiological Reports, 7(20) doi: 10.14814/PHY2.14247 [DOI:10.14814/phy2.14247]
58. Jian-Ping, Zhou., Fan, Wang., Rui-lin, Li., Bao-li, Yuan., Ya-le, Guo. (2004). [Effects of febrile seizures on motor, behavior, spatial learning and memory in rats].. Chinese journal of pediatrics, 42(1):49-53.
59. Omar, F., Khabour., Karem, H., Alzoubi., Mahmoud, A., Alomari., Mohammad, A., Alzubi. (2013). Changes in spatial memory and BDNF expression to simultaneous dietary restriction and forced exercise.. Brain Research Bulletin, 90:19-24. doi: 10.1016/J.BRAINRESBULL.2012.08.005 [DOI:10.1016/j.brainresbull.2012.08.005]
60. Daniela, Delwing, de, Lima., Débora, Delwing, Dal, Magro., Júlia, Niehues, da, Cruz., José, Geraldo, Pereira, da, Cruz. (2012). The effects of swimming exercise on recognition memory for objects and conditioned fear in rats. Acta Scientiarum. Health Science, 34(2):163-169. doi: 10.4025/ACTASCIHEALTHSCI.V34I2.4378 [DOI:10.4025/actascihealthsci.v34i2.4378]
61. Yefeng, Yang., Yefeng, Yang., Malgorzata, Lagisz., Yong, Zhi, Foo., Daniel, W., A., Noble., Daniel, W., A., Noble., Hamza, Anwer., Shinichi, Nakagawa. (2021). Beneficial intergenerational effects of exercise on brain and cognition: a multilevel meta-analysis of mean and variance.. Biological Reviews, 96(4):1504-1527. doi: 10.1111/BRV.12712 [DOI:10.1111/brv.12712]

Add your comments about this article : Your username or Email:

Send email to the article author

Rights and Permissions
Creative Commons License This work is licensed under Attribution 4.0 International (CC BY 4.0).

© 2024 CC BY 4.0 | International Journal of Motor Control and Learning

Designed & Developed by : Yektaweb