Cited by 394Neurogenesis and neuroplasticity mechanismsMemory and Neural MechanismsNerve injury and regeneration

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Spatial memory is improved by aerobic and resistance exercise through divergent molecular mechanisms

Cassilhas, R.C., Lee, K.S., Fernandes, J., Oliveira, M.G.M., Tufik, S., Meeusen, R., de Mello, M.T.·2012·Neuroscience

DOI 10.1016/j.neuroscience.2011.11.029

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Abstract

A growing body of scientific evidence indicates that exercise has a positive impact on human health, including neurological health. Aerobic exercise, which is supposed to enhance cardiovascular functions and metabolism, also induces neurotrophic factors that affect hippocampal neurons, thereby improving spatial learning and memory. Alternatively, little is known about the effect of resistance exercise on hippocampus-dependent memory, although this type of exercise is increasingly recommended to improve muscle strength and bone density and to prevent age-related disabilities. Therefore, we evaluated the effects of resistance training on spatial memory and the signaling pathways of brain-derived neurotrophic factor (BDNF) and insulin-like growth factor 1 (IGF-1), comparing these effects with those of aerobic exercise. Adult male Wistar rats underwent 8 weeks of aerobic training on a treadmill (AERO group) or resistance training on a vertical ladder (RES group). Control and sham groups were also included. After the training period, both AERO and RES groups showed improved learning and spatial memory in a similar manner. However, both groups presented distinct signaling pathways. Although the AERO group showed increased level of IGF-1, BDNF, TrkB, and β-CaMKII (calcium/calmodulin-dependent kinase II) in the hippocampus, the RES group showed an induction of peripheral and hippocampal IGF-1 with concomitant activation of receptor for IGF-1 (IGF-1R) and AKT in the hippocampus. These distinct pathways culminated in an increase of synapsin 1 and synaptophysin expression in both groups. These findings demonstrated that both aerobic and resistance exercise can employ divergent molecular mechanisms but achieve similar results on learning and spatial memory.

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Stein, A. M., Coelho, F. G. D. M., Vital-Silva, T. M., Rueda, A. V., Pereira, J. R., Deslandes, A. C., Camarini, R., & Galduróz, R. F. (2022) · Experimental Aging Research · doi:10.1080/0361073x.2022.2048586 · Cited by 24
Time-restricted feeding combined with resistance exercise prevents obesity and improves lipid metabolism in the liver of mice fed a high-fat diet
de Lima, R. D., Vieira, R. F. L., Muñoz, V. R., Chaix, A., Macêdo, A. P. A., Antunes, G. C., Felonato, M., Braga, R. R., Nakandakari, S. C. B. R., Gaspar, R. C., et al. (2023) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00129.2023 · Cited by 28
Active body, healthy brain: Exercise for healthy cognitive aging
Liu-Ambrose, T. Y. L., Barha, C. K., & Falck, R. S. (2019) · International review of neurobiology · doi:10.1016/bs.irn.2019.07.004 · Cited by 27
Optimal dose and type of exercise to improve cognitive function in patients with mild cognitive impairment: a systematic review and network meta-analysis of RCTs
Yu, Y., Wang, J., & Xu, J. (2024) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2024.1436499 · Cited by 26
RETRACTED: Adult hippocampal neurogenesis (AHN) controls central nervous system and promotes peripheral nervous system regeneration via physical exercise
Zalouli, V., Rajavand, H., Bayat, M., Khaleghnia, J., Sharifianjazi, F., Jafarinazhad, F., & Beheshtizadeh, N. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.115078 · Cited by 27
Retracted
Aerobic exercise training effects on hippocampal volume in healthy older individuals: a meta-analysis of randomized controlled trials
Balbim, G. M., Silva, N. C. B. S., ten Brinke, L., Falck, R. S., Hortobágyi, T., Granacher, U., Erickson, K. I., Hernández‐Gamboa, R., & Liu-Ambrose, T. Y. L. (2023) · GeroScience · doi:10.1007/s11357-023-00971-7 · Cited by 28
“The neuroplastic adaptations following AET were theorized to result from the upregulating effect on neurotrophins, most notably the brain-derived neurotrophic factor (BDNF) [21, 22].”
Influential
Cortical and hippocampal expression of inflammatory and intracellular signaling proteins in aged rats submitted to aerobic and resistance physical training
Henrique, J. S., França, E. F., Cardoso, F. D. S., Serra, F. T., de Almeida, A. A., Fernandes, J., Arida, R. M., & da Silva, S. G. (2018) · Experimental Gerontology · doi:10.1016/j.exger.2018.06.025 · Cited by 24
Self-citation
Moderate treadmill exercise improves spatial learning and memory deficits possibly via changing PDE-5, IL-1 β and pCREB expression
Sabouri, M., Kordi, M. R., Shabkhiz, F., Taghibeikzadehbadr, P., & Geramian, Z. S. (2020) · Experimental Gerontology · doi:10.1016/j.exger.2020.111056 · Cited by 22
Indoor aerobic exercise reduces exposure to pollution, improves cognitive function, and enhances BDNF levels in the elderly
Cassilhas, R. C., Sousa, R. A. L. D., Caxa, L., Viana, V. A. R., MEEUSEN, R. R., Gonçalves, F. L. T., Magalhães, C. O. D. E., Tufik, S. B., Dias‐Peixoto, M. F., Monteiro-Júnior, R. S., et al. (2021) · Air Quality Atmosphere & Health · doi:10.1007/s11869-021-01083-x · Cited by 23
Self-citation
The impact of the frequency of moderate exercise on memory and brain-derived neurotrophic factor signaling in young adult and middle-aged rats
da Costa, M. S., Ardais, A. P., Fioreze, G. T., Mioranzza, S., Botton, P. H. S., Souza, D. O., da Rocha, J. B. T., & Porciúncula, L. O. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.06.068 · Cited by 21
“The frequencies did not change the performance of young adult rats in the inhibitory avoidance and object recognition task, in agreement with a similar training protocol (8 weeks, 50 min/day, 5 days/week and 60–75% VO2max) (Mello et al., 2008).”
Influential
The effect of aerobic training and vitamin D supplements on the neurocognitive functions of elderly women with sleep disorders
Eshaghi, S., Taheri, M., Irandoust, K., Knechtle, B., Nikolaidis, P. Τ., & Chtourou, H. (2019) · Biological Rhythm Research · doi:10.1080/09291016.2019.1579884 · Cited by 22
“Recently, it has been hypothesized that vitamin D plays an important role in controlling sleep in the brain stem, and it has been argued that vitamin D deficiency is the epidemic reason of sleep disorder (Cassilhas et al. 2012; Gominak and Stumpf 2012).”
Short-term environmental enrichment, and not physical exercise, alleviate cognitive decline and anxiety from middle age onwards without affecting hippocampal gene expression
Singhal, G., Morgan, J., Jawahar, M. C., Corrigan, F., Jaehne, E. J., Toben, C. G., Breen, J., Pederson, S., Hannan, A. J., & Baune, B. T. (2019) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-019-00743-x · Cited by 21
“…as a modulator of brain functions and shown to improve spatial memory in young, middle age and old age male rodents (Albeck et al., 2006; Anderson et al., 2000; Radák et al., 2001; Nichol et al., 2009; Singhal et al., 2014; Van Praag et al., 1999; Cassilhas et al., 2012; Uysal et al., 2005).”
Background
Rationale and Design of the PAIRED Trial: Partnered Dance Aerobic Exercise as a Neuroprotective, Motor, and Cognitive Intervention in Parkinson's Disease
Hackney, M. E., Bay, A. A., Jackson, J. M., Nocera, J. R., Krishnamurthy, V., Crosson, B., Evatt, M. L., Langley, J. A., Cui, X., McKay, J. L., et al. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00943 · Cited by 22
“Spatial memory has been shown to improve with aerobic and resistance training exercises (96).”
Background
Gross Motor Skills Training Leads to Increased Brain-Derived Neurotrophic Factor Levels in Healthy Older Adults: A Pilot Study
Grégoire, C., Berryman, N., St-Onge, F., Vu, T. T. M., Bosquet, L., Arbour, N., & Bherer, L. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00410 · Cited by 20
“Nevertheless, the absence of a significant increase in BDNF following an aerobic training program in the present study is equivocal (Cassilhas et al., 2012).”
Background
Long-term exercise training down-regulates m6A RNA demethylase FTO expression in the hippocampus and hypothalamus: an effective intervention for epigenetic modification
Liu, S.-J., Cai, T.-H., Fang, C., Lin, S., Yang, W.-Q., Wei, Y., Zhou, F., Liu, L., Luo, Y., Guo, Z., et al. (2022) · BMC Neuroscience · doi:10.1186/s12868-022-00742-8 · Cited by 23
“Studies on humans and animals suggested that physical exercise improves spatial learning and memory [4, 5].”
Background
An integrated model of acute exercise on memory function
Loprinzi, P. D. (2019) · Medical Hypotheses · doi:10.1016/j.mehy.2019.03.010 · Cited by 23
“For example, aerobic training has been shown to increase hippocampal levels of IGF-1, BDNF, TrkB, and β-CaMKII, whereas resistance training has been shown to increase peripheral and hippocampal levels of IGF-1, with concomitant activation of IGF-1 receptor and AKT in the hippocampus [60].”
Background
Future InBodied: A Framework for Inbodied Interaction Design
Andrés, J., schraefel, M. C., Patibanda, R., & Mueller, F. (2020) · International Conference on Tangible, Embedded, and Embodied Interaction (TEI) · doi:10.1145/3374920.3374969 · Cited by 20
“Aerobic exercise improves spatial learning and memory [4].”
Background
Effects of exercise modalities on BDNF and IL-1β content in circulating total extracellular vesicles and particles obtained from aged rats
Barcellos, N., Cechinel, L. R., de Meireles, L. C. F., Lovatel, G. A., Bruch, G. E., Carregal, V. M., Massensini, A. R., Costa, T. D., Pereira, L. O., & Siqueira, I. R. (2020) · Experimental Gerontology · doi:10.1016/j.exger.2020.111124 · Cited by 20
Strength training or green tea prevent memory deficits in a β-amyloid peptide-mediated Alzheimer's disease model
Schimidt, H. L., Carrazoni, G. S., Garcia, A., Izquierdo, I., Mello‐Carpes, P. B., & Carpes, F. P. (2020) · Experimental Gerontology · doi:10.1016/j.exger.2020.111186 · Cited by 20
Resistance-exercise training attenuates LPS-induced astrocyte remodeling and neuroinflammatory cytokine expression in female Wistar rats
Kelty, T. J., Mao, X., Kerr, N. R., Childs, T. E., Ruegsegger, G. N., & Booth, F. W. (2021) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00571.2021 · Cited by 19
Effects of different exercise modes and intensities on cognitive performance, adult hippocampal neurogenesis, and synaptic plasticity in mice
Jiang, H., Kimura, Y., Inoue, S., Li, C., Hatakeyama, J., Wakayama, M., Takamura, D., & Moriyama, H. (2024) · Experimental Brain Research · doi:10.1007/s00221-024-06854-3 · Cited by 19
“This includes releasing insulin-like growth factor 1 (IGF-1), potentially influencing neurogenesis (Cassilhas et al. 2012 ).”
Comparative overview of the effects of aerobic and resistance exercise on anxiety-like behavior, cognitive flexibility, and hippocampal synaptic plasticity parameters in healthy rats
Segabinazi, E., Gasperini, N. F., Faustino, A. M., Centeno, R. S., dos Santos, A. S., de Almeida, W., Bronauth, L., Marcuzzo, S., & Pereira, L. O. (2020) · Brazilian Journal of Medical and Biological Research · doi:10.1590/1414-431x20209816 · Cited by 19
Effects of human concurrent aerobic and resistance training on cognitive health: A systematic review with meta-analysis
Zhang, M., Fang, W., & Wang, J. (2025) · International Journal of Clinical and Health Psychology · doi:10.1016/j.ijchp.2025.100559 · Cited by 25
“…both AET and SRT improve global cognition (Han et al., 2023), attention (Dunsky et al., 2017; Hacker et al., 2020), memory (Babaei et al., 2013; Cassilhas et al., 2012; Erickson et al., 2011; Makino et al., 2021), information processing speed (Eckardt et al., 2020; Sandroff et al., 2015),…”
Exercise, Cognition, and Health
Erickson, K. I., & Liu-Ambrose, T. Y. L. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-411469-2.00010-8 · Cited by 18
Long-term consequences of COVID-19 on mental health and the impact of a physically active lifestyle: a narrative review
Roever, L., Cavalcante, B. R. R., & Caria, A. C. I. (2023) · Annals of General Psychiatry · doi:10.1186/s12991-023-00448-z · Cited by 23
Developing a Non-Pharmacological Intervention for Individuals With Mild Cognitive Impairment
Rodakowski, J. L., Reynolds, C. F., López, O. L., Butters, M. A., Dew, M. A., & Skidmore, E. R. (2016) · Journal of Applied Gerontology · doi:10.1177/0733464816645808 · Cited by 18
“…as at UNIV OF TENNESSEE on June 4, 2016jag.sagepub.comDownloaded from several mechanisms, in addition to neurocognitive and emotional health, link engagement in daily activities to biological factors (Butters et al., 2008; Cassilhas et al., 2012; Kivipelto et al., 2001; Radák et al., 2001).”
Background
Resistance exercise reduces memory impairment induced by monosodium glutamate in male and female rats
Araújo, P. C. O., Quines, C. B., Jardim, N. S., Leite, M. R., & Nogueira, C. W. (2017) · Experimental Physiology · doi:10.1113/ep086198 · Cited by 18
Electrically evoked local muscle contractions cause an increase in hippocampal BDNF
Maekawa, T., Ogasawara, R., Tsutaki, A., Lee, K., Nakada, S., Nakazato, K., & Ishii, N. (2018) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2017-0536 · Cited by 22
Self-citation
Significant Acute Response of Brain-Derived Neurotrophic Factor Following a Session of Extreme Conditioning Program Is Correlated With Volume of Specific Exercise Training in Trained Men
Pereira, E. S., Neto, W. K., Calefi, A. S., Georgetti, M., Guerreiro, L., Zocoler, C. A. S., & Gama, E. F. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.00823 · Cited by 19
Epigenetic modifications induced by exercise: Drug-free intervention to improve cognitive deficits associated with obesity
Barros, L., Eichwald, T., Solano, A. F., Scheffer, D. D. L., da Silva, R. A., Gaspar, J. M., & Latini, A. (2019) · Physiology & Behavior · doi:10.1016/j.physbeh.2019.03.009 · Cited by 18
TNF signalling via the TNF receptors mediates the effects of exercise on cognition-like behaviours.
Morgan, J., Singhal, G., Corrigan, F., Jaehne, E. J., Jawahar, M. C., & Baune, B. T. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.06.036 · Cited by 18
Acute bouts of aerobic and resistance exercise similarly alter inhibitory control and response time while inversely modifying plasma BDNF concentrations in middle-aged and older adults with type 2 diabetes
Silveira-Rodrigues, J. G., Campos, B. T., de Lima, A. T., Ogando, P. H. M., Gomes, C. B., Gomes, P. F., Aleixo, I. M. S., & Soares, D. D. (2023) · Experimental Brain Research · doi:10.1007/s00221-023-06588-8 · Cited by 18
Aerobic exercise training improves memory function through modulation of brain-derived neurotrophic factor and synaptic proteins in the hippocampus and prefrontal cortex of type 2 diabetic rats
Sadri, I., Nikookheslat, S. D., Karimi, P., Khani, M., & Nadimi, S. (2023) · Journal of Diabetes & Metabolic Disorders · doi:10.1007/s40200-023-01360-9 · Cited by 17
“On the contrary, some studies have reported the increased hippocampal expression of synaptophysin after different exercise regimens [44].”
Exercise effects on cognitive functioning in young adults with first-episode psychosis: FitForLife
Hallgren, M. Å., Skott, M., Ekblom, Ö. B., Firth, J., Schembri, A. J., & Forsell, Y. (2018) · Psychological Medicine · doi:10.1017/s0033291718001022 · Cited by 19
Experimental Effects of Acute High-Intensity Resistance Exercise on Episodic Memory Function: Consideration for Post-Exercise Recovery Period
Loprinzi, P. D., Green, D., Wages, S., Cheke, L. G., & Jones, T. W. (2020) · Journal of Lifestyle Medicine · doi:10.15280/jlm.2020.10.1.7 · Cited by 17
“Further, emerging work in animal models suggest that the mechanisms through which resistance exercise improves memory function may differ from mechanisms modulated by aerobic exercise, with different intracellular pathways being activated [28-32].”
Background
Aerobic Training Increases Hippocampal Volume and Protects Cognitive Function for Type 2 Diabetes Patients with Normal Cognition
Wang, Y., Wang, L., Yan, J., Yuan, X., & Lou, Q. (2023) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/a-2105-0799 · Cited by 16
“Exercise training can increase the number of new neurons in the hippocampus through the increase of IGF-1, which mediates the proliferation of hippocampal neurons and improve cognitive function [35].”
Background
One physical exercise session promotes recognition learning in rats with cognitive deficits related to amyloid beta neurotoxicity
Daré, L. R., Garcia, A., das Neves, B.-H. S., & Mello‐Carpes, P. B. (2020) · Brain Research · doi:10.1016/j.brainres.2020.146918 · Cited by 18
Implications of Physical Exercise on Episodic Memory and Anxiety: The Role of the Serotonergic System
Illesca-Matus, R., Ardiles, N. M., Muñoz, F., & Moya, P. R. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241411372 · Cited by 19
“Despite the different signaling pathways activated depending on the type of exercise, both aerobic and resistance training improve spatial learning and memory [109].”
Background
SMART: physical activity and cerebral metabolism in older people: study protocol for a randomised controlled trial
Fleckenstein, J., Matura, S., Engeroff, T., Füzéki, E., Tesky, V. A., Pilatus, U., Hattingen, E., Deichmann, R., Vogt, L., Banzer, W. E., et al. (2015) · Trials · doi:10.1186/s13063-015-0662-9 · Cited by 16
“Abbreviations ADP: adenosine diphosphate; ATP: adenosine triphosphate; AV: atrioventricular; BDNF: brain-derived neurotrophic factor; CERAD: Consortium to Establish a Registry of Alzheimer’s Disease; COP: centre of pressure; CPET: cardiopulmonary exercise test; ECG: electrocardiogram; ELISA: enzyme-linked immunosorben…”
Background
Burrowing as a novel voluntary strength training method for mice: A comparison of various voluntary strength or resistance exercise methods
Roemers, P., Mazzola, P. N., Deyn, P. P. D., Bossers, W. J. R., van Heuvelen, M. J. G., & van der Zee, E. A. (2017) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2017.05.027 · Cited by 16
Hippocampal Adaptations to Continuous Aerobic Training: A Functional and Ultrastructural Evaluation in a Young Murine Model
Cariati, I., Bonanni, R., Pallone, G., Scimeca, M., Frank, C., Tancredi, V., & D’Arcangelo, G. (2021) · Journal of Functional Morphology and Kinesiology · doi:10.3390/jfmk6040101 · Cited by 18
“such as synaptophysin and postsynaptic density protein 95 (PSD-95) in the hippocampus [43].”
Background
Cognitive Improvement After Aerobic and Resistance Exercise Is Not Associated With Peripheral Biomarkers
Ando, S., Komiyama, T., Tanoue, Y., Sudo, M., Costello, J. T., Uehara, Y., & Higaki, Y. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.853150 · Cited by 16

Authors: Cassilhas, R. C., Lee, K. S., Fernandes, J., Oliveira, M. G. M., Tufik, S., Meeusen, R., & de Mello, M. T.
Affiliations: Universidade Federal de São Paulo (BR)
Vrije Universiteit Brussel (BE)
ORCID: Cassilhas, R.C.
Fernandes, J.
Tufik, S.
Meeusen, R.
Venue: Neuroscience
Publisher: Elsevier BV
Published: 2012-01
Volume: 202
Pages: 309-317
ISSN: 0306-4522 (ISSN-L)
DOI: 10.1016/j.neuroscience.2011.11.029
OpenAlex: W2146864294
Cited by: 394
References: 74
Citations by year: 2026: 21 · 2025: 30 · 2024: 26 · 2023: 34 · 2022: 26 · 2021: 36 · 2020: 34 · 2019: 35 · 2018: 34 · 2017: 23 · 2016: 28 · 2015: 23 · 2014: 21 · 2013: 15 · 2012: 8
FWCI: 4.60
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience (publishedVersion)
PubMed (publishedVersion)
UNIFESP Institutional Repository (Universidade Federal de São Paulo) (submittedVersion)
VUBIR (Vrije Universiteit Brussel) (submittedVersion)
Funders: São Paulo Research Foundation (2008/03083-6)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
Keywords: spatial memory, aerobic exercise, resistance training, hippocampus, brain-derived neurotrophic factor, insulin-like growth factor I, IGF-1 receptor, Akt signaling, TrkB, CaMKII, synapsin-1, synaptophysin, neurotrophic factors, exercise and cognition
MeSH terms: Animals, Corticosterone, Enzyme-Linked Immunosorbent Assay, Hippocampus, Insulin-Like Growth Factor I, Male, Memory, Physical Conditioning, Animal, Radioimmunoassay, Space Perception, Blotting, Western, Signal Transduction, Synapsins, Rats, Wistar, Receptor, IGF Type 1, Maze Learning, Brain-Derived Neurotrophic Factor, Receptor, trkB, Oncogene Protein v-akt, Rats, Calcium-Calmodulin-Dependent Protein Kinase Type 2, Resistance Training

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Spatial memory is improved by aerobic and resistance exercise through divergent molecular mechanisms

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