Maternal voluntary physical exercise in the adult rat: evidence of exercise-associated differences in maternal food intake, and in brain effects on the progeny

References

• Kim P, Strathearn L, Swain JE. The maternal brain and its plasticity in humans. Horm Behav. 2016;77:113–23. doi:10.1016/j.yhbeh.2015.08.001.
   PubMed Web of Science ®Google Scholar
• Davenport MH, Meah VL, Ruchat SM, Davies GA, Skow RJ, Barrowman N, et al. Impact of prenatal exercise on neonatal and childhood outcomes: a systematic review and meta-analysis. Br J Sports Med. 2018;52(21):1386–96. doi:10.1136/bjsports-2018-099836.
   PubMed Web of Science ®Google Scholar
• Jones MA, Whitaker KM, Taverno Ross SE, Davis K, Libertus K, Barone Gibbs B. Maternal sedentary behavior and physical activity across pregnancy and early childhood motor development. Children (Basel). 2021;8(7):549, doi:10.3390/children8070549.
   PubMed Web of Science ®Google Scholar
• Jukic AM, Lawlor DA, Juhl M, Owe KM, Lewis B, Liu J, et al. Physical activity during pregnancy and language development in the offspring. Paediatr Perinat Epidemiol. 2013;27(3):283–93. doi:10.1111/ppe.12046.
   PubMed Web of Science ®Google Scholar
• Santana Muniz G, Beserra R, da Silva GDP, Fragoso J, de Oliveira Lira A, Nascimento E, et al. Active maternal phenotype is established before breeding and leads offspring to align growth trajectory outcomes and reflex ontogeny. Physiol Behav. 2014;129:1–10. doi:10.1016/j.physbeh.2014.02.027.
   PubMed Web of Science ®Google Scholar
• Fidalgo M, Falcao-Tebas F, Bento-Santos A, de Oliveira E, Nogueira-Neto JF, de Moura EG, et al. Programmed changes in the adult rat offspring caused by maternal protein restriction during gestation and lactation are attenuated by maternal moderate-low physical training. Br J Nutr. 2013;109(3):449–56. doi:10.1017/S0007114512001316.
   PubMed Web of Science ®Google Scholar
• Leandro CG, da Silva Ribeiro W, Dos Santos JA, Bento-Santos A, Lima-Coelho CH, Falcão-Tebas F, et al. Moderate physical training attenuates muscle-specific effects on fibre type composition in adult rats submitted to a perinatal maternal low-protein diet. Eur J Nutr. 2012;51(7):807–15. doi:10.1007/s00394-011-0259-3.
   PubMed Web of Science ®Google Scholar
• Senna SM, Torres MK, Lopes DA, Alheiros-Lira MC, de Moura DB, Pereira VR, et al. Moderate physical training attenuates perinatal low-protein-induced spleen lymphocyte apoptosis in endotoxemic adult offspring rats. Eur J Nutr. 2016;55(3):1113–22. doi:10.1007/s00394-015-0925-y.
   PubMed Web of Science ®Google Scholar
• Wells JCK. Life history trade-offs and the partitioning of maternal investment: implications for health of mothers and offspring. Evol Med Public Health. 2018;16(1):153–66. doi:10.1093/emph/eoy014.
   Google Scholar
• Fragoso J, Carvalho Jurema Santos G, Thomaz da Silva H, Oliveira Nogueira V, Loizon E, Vidal H, et al. Maternal physical activity-induced adaptive transcriptional response in brain and placenta of mothers and rat offspring. J Dev Orig Health Dis. 2019;11(2):108–17. doi:10.1017/S2040174419000333.
   PubMed Web of Science ®Google Scholar
• Fragoso J, Carvalho Jurema Santos G, da Silva HT, Loizon E, de Oliveira Nogueira Souza V, Vidal H, et al. Effects of maternal low-protein diet and spontaneous physical activity on the transcription of neurotrophic factors in the placenta and the brains of mothers and offspring rats. J Dev Orig Health Dis. 2021;12(3):505–12. doi:10.1017/S2040174420000756.
   PubMed Web of Science ®Google Scholar
• Fragoso J, Lira AO, Chagas GS, Lucena Cavalcanti CC, Beserra R, de Santana-Muniz G, et al. Maternal voluntary physical activity attenuates delayed neurodevelopment in malnourished rats. Exp Physiol. 2017;102(11):1486–99. doi:10.1113/EP086400.
   PubMed Web of Science ®Google Scholar
• 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):243–9. doi:10.1016/j.ijdevneu.2007.03.003.
   PubMed Web of Science ®Google Scholar
• Yau SY, Lee TH, Formolo DA, Lee WL, Li LC, Siu PM, Chan CCH. Effects of maternal voluntary wheel running during pregnancy on adult hippocampal neurogenesis, temporal order memory, and depression-like behavior in adult female and male offspring. Front Neurosci. 2019;13:470, doi:10.3389/fnins.2019.00470.
   PubMed Web of Science ®Google Scholar
• Jacotte-Simancas A, Costa-Miserachs D, Coll-Andreu M, Torras-Garcia M, Borlongan CV, Portell-Cortés I. Effects of voluntary physical exercise, citicoline, and combined treatment on object recognition memory, neurogenesis, and neuroprotection after traumatic brain injury in rats. J Neurotrauma. 2015;32:739–51. doi:10.1089/neu.2014.3502.
   PubMed Web of Science ®Google Scholar
• Lin Y, Dong J, Yan T, He X, Zheng X, Liang H, Sui M. Involuntary, forced and voluntary exercises are equally capable of inducing hippocampal plasticity and the recovery of cognitive function after stroke. Neurol Res. 2015;37(10):893–01. doi:10.1179/1743132815Y.0000000074.
   PubMed Web of Science ®Google Scholar
• Farmer J, Zhao X, Van Praag H, Wodtke K, Gage FH, Christie BR. Effects of voluntary exercise on synaptic plasticity and gene expression in the dentate gyrus of adult male Sprague-Dawley rats in vivo. Neuroscience. 2004;124(1):71–9. doi:10.1016/j.neuroscience.2003.09.029.
   PubMed Web of Science ®Google Scholar
• Leão AAP. Spreading depression of activity in the cerebral cortex. J Neurophysiol. 1944a;7:359–90.
   Google Scholar
• Leão AAP. Pial circulation and spreading depression of activity in the cerebral cortex. J Neurophisiol. 1944b;7:391–6.
   Google Scholar
• Leão AAP. Further observations on the spreading depression of activity in the cerebral cortex. J Neurophysiol. 1947;10:409–14.
   PubMed Web of Science ®Google Scholar
• Tamim I, Chung DY, de Morais AL, Loonen ICM, Qin T, Misra A, et al. Spreading depression as an innate antiseizure mechanism. Nat Commun. 2021;12(1):2206, doi:10.1038/s41467-021-22464-x.
   PubMed Web of Science ®Google Scholar
• Gollion C. Cortical excitability in migraine: contributions of magnetic resonance imaging. Rev Neurol. 2021;177(7):809–15. doi:10.1016/j.neurol.2021.07.008.
   PubMedGoogle Scholar
• Dreier JP, Major S, Pannek H-W, Woitzik J, Scheel M, Wiesenthal D, et al. Spreading convulsions, spreading depolarization and epileptogenesis in human cerebral cortex. Brain. 2012;135:259–75. doi:10.1093/brain/awr303.
   PubMed Web of Science ®Google Scholar
• Guedes RCA, Araújo MDGR, Verçosa TC, Bion FM, de Sá AL, Pereira A, Jr, Abadie-Guedes R. Evidence of an inverse correlation between serotonergic activity and spreading depression propagation in the rat cortex. Brain Res. 2017;1672:29–34. doi:10.1016/j.brainres.2017.07.011.
   PubMed Web of Science ®Google Scholar
• Guedes RCA, Abadie-Guedes R. Brain aging and electrophysiological signaling: revisiting the spreading depression model. Front Aging Neurosci. 2019;7(11):136, doi:10.3389/fnagi.2019.00136.
   Google Scholar
• Lima CB, Soares GDSF, Vitor SM, Andrade-da-Costa BL, Castellano B, Guedes RCA. Spreading depression features and Iba1 immunoreactivity in the cerebral cortex of developing rats submitted to treadmill exercise after treatment with monosodium glutamate. Int J Dev Neurosci. 2014;33:98–105. doi:10.1016/j.ijdevneu.2013.12.008.
   PubMed Web of Science ®Google Scholar
• Vitor-de-Lima SM, Medeiros LB, Benevides RDL, Dos Santos CN, Lima da Silva NO, Guedes RCA. Monosodium glutamate and treadmill exercise: anxiety-like behavior and spreading depression features in young adult rats. Nutr Neurosci. 2017;22(6):435–43. doi:10.1080/1028415X.2017.1398301.
   PubMed Web of Science ®Google Scholar
• 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. 2017;22:464–73. doi:10.1080/1028415X.2017.1407472.
   PubMed Web of Science ®Google Scholar
• Dere E, Huston JP, De Souza Silva MA. The pharmacology, neuroanatomy and neurogenetics of one-trial object recognition in rodents. Neurosci Biobehav Rev. 2007;31(5):673–704. doi:10.1016/j.neubiorev.2007.01.005.
   PubMed Web of Science ®Google Scholar
• Viana LC, Lima CM, Oliveira MA, Borges RP, Cardoso TT, Almeida IN, et al. Litter size, age-related memory impairments, and microglial changes in rat dentate gyrus: stereological analysis and three dimensional morphometry. Neuroscience. 2013;238:280–96. doi:10.1016/j.neuroscience.2013.02.019.
   PubMed Web of Science ®Google Scholar
• Antunes M, Biala G. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process. 2012;13(2):93–110. doi:10.1007/s10339-011-0430-z.
   PubMed Web of Science ®Google Scholar
• Francisco ES, Mendes-da-Silva RF, Lima-de-Castro CB, Soares GSF, Guedes RCA. Taurine/pilocarpine interaction in the malnourished rat brain: a behavioral, electrophysiological and immunohistochemical analysis. Front Neurosci. 2019;13(981):1–18. doi:10.3389/fnins.2019.00981.
   PubMedGoogle Scholar
• Nogueira VO, Andrade LDS, Rocha-Júnior RL, Melo PED, Helvécio E, Fontes DAF, et al. Maternal physical activity prevents the overexpression of hypoxia-inducible factor 1-α and cardiorespiratory dysfunction in protein malnourished rats. Sci Rep. 2019;9(1):14406, doi:10.1038/s41598-019-50967-7.
   PubMedGoogle Scholar
• Andersson-Hall U, de Maré H, Askeli F, Börjesson M, Holmäng A. Physical activity during pregnancy and association with changes in fat mass and adipokines in women of normal-weight or with obesity. Sci Rep. 2021;11(1):12549, doi:10.1038/s41598-021-91980-z.
   PubMed Web of Science ®Google Scholar
• Sakakima GM, Dos Santos ER, Bueno GC, Rempel MS, Furlan JP, da Costa C, et al. Treadmill walking differently affects body composition and metabolic parameters of female rats from normal or small litters. Physiol Int. 2016;103(2):169–82. doi:10.1556/036.103.2016.2.4.
   PubMed Web of Science ®Google Scholar
• Khambadkone SG, Cordner ZA, Tamashiro KLK. Maternal stressors and the developmental origins of neuropsychiatric risk. Front Neuroendocrinol. 2020;57:100834, doi:10.1016/j.yfrne.2020.100834.
   PubMed Web of Science ®Google Scholar
• Zhou X, Li L. Prenatal anxiety and its influence on delivery outcome. Zhong Nan Da Xue Bao Yi Xue Ban. 2011;36(8):803–8. doi:10.3969/j.issn.1672-7347.2011.08.020. Chinese.
   PubMedGoogle Scholar
• Yan W, Wang X, Kuang H, Chen Y, Baktash MB, Eskenazi B, et al. Physical activity and blood pressure during pregnancy: mediation by anxiety symptoms. J Affect Disord. 2020;264:376–82. doi:10.1016/j.jad.2019.11.056.
   PubMed Web of Science ®Google Scholar
• Torabi M, Pooriamehr A, Bigdeli I, Miladi-Gorji H. Maternal swimming exercise during pregnancy attenuates anxiety/depressive-like behaviors and voluntary morphine consumption in the pubertal male and female rat offspring born from morphine dependent mothers. Neurosci Lett. 2017;659:110–4. doi:10.1016/j.neulet.2017.08.074.
   PubMed Web of Science ®Google Scholar
• Farzad P, Rahimi R, Ebrahimi SA, Aghajani F, Mousavi Z, Najafizadeh P. The effect of voluntary exercise and prenatal exposure to sodium valproate on learning, memory, and anxiety of rats’ offspring. Iran J Med Sci. 2020;45(1):32–40. doi:10.30476/ijms.2019.45314.
   PubMed Web of Science ®Google Scholar
• Lima DS, Francisco ED, Lima CB, Guedes RCA. Neonatal L-glutamine modulates anxiety-like behavior, cortical spreading depression, and microglial immunoreactivity: analysis in developing rats suckled on normal size- and large size litters. Amino Acids. 2017;9(2):337–46. doi:10.1007/s00726-016-2365-2.
   Google Scholar
• Francisco EDS, Guedes RCA. Neonatal taurine and alanine modulate anxiety-like behavior and decelerate cortical spreading depression in rats previously suckled under different litter sizes. Amino Acids. 2015;47:2437–45. doi:10.1007/s00726-015-2036-8.
   PubMed Web of Science ®Google Scholar
• Benevides RDL, Vitor-de-Lima SM, Chagas CL, de Lima CF, Abadie-Guedes R, Guedes RCA. Lactation in large litters influences anxiety, memory, and spreading depression in adult male rats that were chronically subjected to a nonconvulsive pilocarpine dose. Nutr Neurosci. 2020;11:1–11. doi:10.1080/1028415X.2020.1819103.
   Google Scholar
• Francisco EDS, Mendes-da-Silva RF, de Castro CBL, Soares GSF, Guedes RCA. Taurine/Pilocarpine interaction in the malnourished rat brain: a behavioral, electrophysiological, and immunohistochemical analysis. Front Neurosci. 2019;13:981, doi:10.3389/fnins.2019.00981.
   PubMed Web of Science ®Google Scholar
• Arida RM. Physical exercise and seizure activity. BBA Mol Basis Dis. 2021;1867:165979.
   PubMed Web of Science ®Google Scholar
• Labonte-Lemoyne E, Curnier D, Ellemberg D. Exercise during pregnancy enhances cerebral maturation in the newborn: a randomized controlled trial. J Clin Exp Neuropsychol. 2017;39(4):347–54. doi:10.1080/13803395.2016.1227427.
   PubMed Web of Science ®Google Scholar
• Gomes da Silva S, de Almeida AA, Fernandes J, Lopim GM, Cabral FR, Scerni DA, 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):e0147200, doi:10.1371/journal.pone.0147200.
   PubMed Web of Science ®Google Scholar
• Robinson AM, Bucci DJ. Physical exercise during pregnancy improves object recognition memory in adult offspring. Neuroscience. 2014;256:53–60. doi:10.1016/j.neuroscience.2013.10.012.
   PubMed Web of Science ®Google Scholar