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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“The protocol was adapted and subdivided into training and test phases accordingly with our previous publication (Cassilhas et al. 2012).”
Self-citation
Experimental Periodontitis Increases Anxious Behavior and Worsens Cognitive Aspects and Systemic Oxidative Stress in Wistar Rats
Castro, G., Pereira, R. R. D. S., Magalhães, C. O. D. E., Costa, K. B., Rocha‐Vieira, E., Cassilhas, R. C., Sampaio, K. H., Machado, A. R. T., Carvalho, J. D. C. L., Murata, R. M., et al. (2024) · Clinical and Experimental Dental Research · doi:10.1002/cre2.70017 · Cited by 7
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Differential Regulation of miRNA and Protein Profiles in Human Plasma-Derived Extracellular Vesicles via Continuous Aerobic and High-Intensity Interval Training
Wang, Z., Ou, Y., Zhu, X., Zhou, Y. H., Zheng, X., Zhang, M., Li, S., Yang, S.-N., Juntti‐Berggren, L., Berggren, P., et al. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26031383 · Cited by 7
“Actually, both aerobic and resistance exercise have been shown to improve spatial learning and memory in both humans [30] and rodents [31].”
Exercise induced irisin mitigates hepatitis in anabolic-androgenic steroids treated rats via modulation of PGC-1-α/PPARγ/Nrf2 and NRF2/NF-κB/TLR4 signaling
Salem, G. A., Aref, M., El-Malkey, N. F., Alqahtani, H. A., Abd-Almotaleb, N. A., NASSAN, M. A., & Elsherbiny, H. (2025) · Tissue and Cell · doi:10.1016/j.tice.2025.102829 · Cited by 6
The Muscle–Brain Axis in Aging: Mechanistic and Clinical Perspectives on Resistance Training and Cognitive Function
Yu, S., Fan, Y., You, B., Zhang, H., Cai, Z., Zhang, S., & Tian, H. (2026) · Biology · doi:10.3390/biology15020154 · Cited by 9
“In rodent models, resistance training—but not aerobic exercise—has been shown to enhance hippocampal synaptic plasticity through the upregulation of the IGF-1/Akt pathway [91].”
Effects of Different Continuous Aerobic Training Protocols in a Heterozygous Mouse Model of Niemann-Pick Type C Disease
Cariati, I., Scimeca, M., Tancredi, V., D’Amico, A. G., Pallone, G., Palmieri, M., Frank, C., & D’Arcangelo, G. (2020) · Journal of Functional Morphology and Kinesiology · doi:10.3390/jfmk5030053 · Cited by 6
“Nevertheless, it is well reported in the literature that physical exercise exerts several beneficial effects on cognitive and brain plasticity [26,27] by promoting hippocampal neurogenesis and enhancement in neuroplasticity, improving spatial memory and learning [28].”
Background
Targeting Insulin-Like Growth Factor-I in Management of Neurological Disorders
Makkar, R., Behl, T., Sehgal, A., Singh, S., Sharma, N., Makeen, H. A., Albratty, M., Alhazmi, H. A., & Meraya, A. M. (2022) · Neurotoxicity Research · doi:10.1007/s12640-022-00513-7 · Cited by 6
“an increase in oxidative stress-mediated damage, neuroinflammation, apoptosis, and edema in brain and also impaired the memory and learning capabilities of the individual and weakened the integrity of blood brain barrier (Cassilhas et al. 2012).”
Background
Exercise as therapy for neurodevelopmental and cognitive dysfunction in people with a Fontan circulation: A narrative review
Verrall, C. E., Tran, D., Yang, J. Y., Lubans, D. R., Winlaw, D. S., Ayer, J. G., Celermajer, D. S., & Cordina, R. (2023) · Frontiers in Pediatrics · doi:10.3389/fped.2023.1111785 · Cited by 7
Effects of Physical Activity on Brain Energy Biomarkers in Alzheimer’s Diseases
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“Similar results have also been observed in a rodent model (90-day-old rats) undertaking eight weeks of aerobic training on a treadmill and resistance exercise on a vertical ladder, showing an improvement in learning and spatial memory in a similar manner, using either the Morris water maze test or a passive avoidance…”
Result
Distinct effects of long-term resistance exercise on cognitive deficits, neurotrophins, and amyloid pathology in male and female APP/PS1 mice
Azevedo, C. V., Otaviano, S. F. S. D., Campos, H. C., Figueiredo, E. V., Pereira, A. R., Alves, L., Braga, M., Gimenes, C., Boldarine, V. T., Oyama, L. M., et al. (2025) · Journal of Alzheimer s Disease · doi:10.1177/13872877251389824 · Cited by 6
“37,62 By measuring VEGF and IGF-1, we explored the potential mechanisms by which RE exerts neuroprotective effects in APP/ PS1 mice, particularly regarding vascular and neurotrophic modulation in males and females.”
Resistance training boosts lactate transporters and synaptic proteins in insulin-resistance mice
Bian, X., Li, M., & Lou, S. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e34425 · Cited by 5
“While resistance training has been demonstrated to activate the PI3K/Akt signaling pathway in the hippocampus of normal Wistar rats [18], research on the effects of resistance exercise on the hippocampal PI3K/Akt signaling pathway and lactate transport mechanisms in models of insulin resistance…”
Can acute resistance exercise facilitate episodic memory encoding?
Amico, G., Braun, T., & Schaefer, S. (2021) · Current Psychology · doi:10.1007/s12144-021-02352-9 · Cited by 6
The Post-conditioning Acute Strength Exercise Facilitates Contextual Fear Memory Consolidation Via Hippocampal N-methyl-D-aspartate-receptors
Leite, A. K. O., Farias, C. P., Schmidt, B. E., Teixeira, L., Rieder, A. S., Furini, C. R. G., & Wyse, Â. T. D. S. (2023) · Neuroscience · doi:10.1016/j.neuroscience.2023.10.016 · Cited by 6
Effects of Aerobic Exercise and Resistance Training on Cognitive Function: Comparative Study Based on FNDC5/Irisin/BDNF Pathway
Izawa, S., Nishii, K., Aizu, N., Kito, T., Iwata, D., Chihara, T., Sawada, H., Yao, R., & Yamada, K. (2024) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000541093 · Cited by 5
“Another mechanism with RT involves an increase in the insulin-like growth factor 1 (IGF-1) and IGF-1 receptor expression levels in the hippocampus, and their binding to the receptors promotes Akt activation [33].”
Animal Models of Exercise–Brain Interactions
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Aptitud física y habilidades cognitivas
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Concurrent exercise training and Murf-l and Atrogin-1 gene expression in the vastus lateralis muscle of male Wistar rats
Moradi, Y., Zehsaz, F., & Nourazar, M. A. (2020) · Apunts Sports Medicine · doi:10.1016/j.apunsm.2020.02.001 · Cited by 5
Nandrolone decanoate and resistance exercise affect body composition and energy metabolism
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Moving beyond the weight-loss paradigm of exercise interventions for mental illness
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Exercise as a multitarget therapy: modulating myokines, neurotrophins, and inflammation in Parkinson’s disease
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“It has been established through research that aerobic exercises are eective in enhancing BDNF levels (Cassilhas et al., 2012).”
The preconditioning effect of different exercise training modes on middle cerebral artery occlusion induced-behavioral deficit in senescent rats
Zarrinkalam‎, E., Arabi, S. M., Komaki‬, A., & Ranjbar, K. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e17992 · Cited by 4
The Effects of Essential Amino Acid Supplementation on Hippocampal Neurotrophin, Dopaminergic and Serotonergic Changes in an Overtraining Mouse Model
Binman, L., Ben‐Zeev, T., Harris, A., Levi, C., Weissman, I., Church, D. D., Ferrando, A. A., & Hoffman, J. R. (2025) · Nutrients · doi:10.3390/nu17182957 · Cited by 4
“Interestingly, TrkB expression in the RT group was not significantly different from CTL, consistent with previous studies indicating limited hippocampal TrkB responsiveness to resistance training in rodents [51,52].”
Nandrolone decanoate reduces the positive effects of resistance training on cognition, anxious behavior, and hippocampal morphology in rats
Magalhães, C. O. D. E., de Oliveira, L. R. S., Santos, S. T., Mendes, B. F., Dias, I. R., Cruz, P. P., Sampaio, K. H., Dias‐Peixoto, M. F., Sousa, R. A. L. D., & Cassilhas, R. C. (2022) · Research Society and Development · doi:10.33448/rsd-v11i8.30600 · Cited by 4
“However, resistance training is the main modality practiced by recreational AAs users (Camiletti-Moirón et al., 2015; Novaes Gomes et al., 2014; Pope et al., 2014), and it is unclear if this exercise modality protects the brain from the administration of supraphysiologic doses of AAs.”
BackgroundSelf-citation
Higher Protein Intake does not Modulate Resistance Training–Induced Changes in Myokines and Cognitive Function in Middle-Aged Adults
Kim, J., McKenna, C. F., Askow, A. T., Salvador, A. F., Scaroni, S. E., Cerna, J., Cannavale, C. N., Paluska, S. A., Lisio, M. D., Petruzzello, S. J., et al. (2024) · Journal of Cognitive Enhancement · doi:10.1007/s41465-024-00285-2 · Cited by 4
“As aerobic and resistance exercise have been suggested to affect cognitive outcomes through divergent pathways (Cassilhas et al., 2012), the aerobic component of this intervention may have driven the neuroelectric changes.”
An acute bout of resistance exercise increases BDNF in hippocampus and restores the long-term memory of insulin-resistant rats
Gomes, C. B., Ramos, J. S., Silveira-Rodrigues, J. G., Leite, D. M. D. M., Melo, B. P., & Soares, D. D. (2024) · Experimental Brain Research · doi:10.1007/s00221-024-06795-x · Cited by 4
“Between each trial, the animals remained in the housing chamber for 60 s (Pereira et al. 2010; Cassilhas et al. 2012a).”
Various modalities of resistance exercise promote similar acute cognitive improvements and hemodynamic increases in young, healthy adults
Batman, G. B., Cooper, C. B., Traylor, M. K., Ransom, K. V., Hill, E. C., Hill, B. D., & Keller, J. L. (2024) · Cerebral Circulation - Cognition and Behavior · doi:10.1016/j.cccb.2024.100363 · Cited by 4
“Further, it is possible that factors other than BDNF, such as insulin-like growth factor 1, contributed to these responses as well [69].”
Background
Research Progress on the Effects of Different Exercise Modes on the Secretion of Exerkines After Spinal Cord Injury
Li, Q., Li, C., & Zhang, X. (2024) · Cellular and molecular neurobiology · doi:10.1007/s10571-024-01497-y · Cited by 5
“Based on current evidence, RE appears to be mostly ineffective for BDNF (Huang et al. 2014; Knaepen et al. 2010), while AE has been shown to successfully increase circulating BDNF levels (Cassilhas et al. 2012).”
Background
Association between serum insulin-like growth factor 1 and locomotive syndrome in community-dwelling older people
Nakamura, M., Imaoka, M., Nakao, H., Hida, M., Tazaki, F., Imai, R., & Hashizume, H. (2022) · BMC Musculoskeletal Disorders · doi:10.1186/s12891-022-05738-3 · Cited by 4
Guidelines for animal models of endurance and resistance exercise
Rezaee, Z. (2025) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2025.110362 · Cited by 3
The Role of Physical Activity on Spatial and Temporal Cognitive Processing in Young Women
Castillo, J., Salvador-Viñas, M. D. M., & Cimadevilla, J. M. (2025) · Brain Sciences · doi:10.3390/brainsci15050431 · Cited by 4
“Therefore, physically active individuals are able to outperform sedentary participants in spatial navigation tasks in both animals [11,12] and humans [13–15].”
Movement and brain health in perimenopausal and early postmenopausal females: A scoping review
Faridi, W., Daun, J. T., Dhruva, T., McLaughlin, E., Bhullar, I., Bolianatz, G., Gentleman, E., Hayden, A., Culos-Reed, S. N., McDonough, M. H., et al. (2025) · Maturitas · doi:10.1016/j.maturitas.2025.108747 · Cited by 4
Synergistic Effects of Exercise and Dietary Polyphenols on Cognitive Function and Neuroprotection in Aging: A Focus on Spatial Learning and Memory
Cheng, R., Yang, X., Su, H., Wei, X., Ji, H., & Song, D. (2026) · Phytotherapy Research · doi:10.1002/ptr.70341 · Cited by 3
“A combined exercise routine that incorporates both aerobic activities and resistance training, including weightlifting, has been found to enhance hippocampal function, a key factor in spatial memory (Cassilhas et al. 2012; Lee et al. 2022; Tsai et al. 2018).”
Differences in risk of generalized anxiety disorder according to physical activity type in Korea adolescents: The Korea youth risk behavior web-based survey, 2020–2021
Shin, J., & Lee, K. (2024) · Digital Health · doi:10.1177/20552076231225572 · Cited by 3
“30,31 However, increased secretion of these substances through PA helps reduce anxiety disorders, including stress.”
BackgroundSelf-citation
The relationship between neurotransmission-related amino acid blood concentrations and neuropsychological performance following acute exercise
Parthimos, T. P., Schulpis, K. H., Karousi, A. D., Loukas, Y. L., & Dotsikas, Y. (2022) · Applied Neuropsychology Adult · doi:10.1080/23279095.2022.2043327 · Cited by 3
“Moreover, Cassilhas et al., observed that acute exercise can improve spatial memory through increased synapsin 1 and synaptophysin expression, which are essential proteins for neurotransmitter release and vesicle fusion (Cassilhas et al., 2012).”
Endurance Exercise Training Attenuates the Waterpipe Smoke Inhaling-Induced Learning and Memory Impairment in Rats: Role of Neurotrophic Factors and Apoptotic System
Taghipour, M., Joukar, S., Alavi, S. S., Mohammadi, F., Asadi‐Shekaari, M., & Alibolandi, Z. (2023) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntad101 · Cited by 3
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Practical Application of Resistance Exercise for Prevention of Sarcopenia
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The Link Between Exercise and Mediation of Alzheimer's Disease and Neurodegenerative Diseases
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“…reuptake inhibitors (SSRIs) and serotonin– norepinephrine reuptake inhibitors (SNRIs), as well as other antidepressant classes such as tricyclic antidepressants (TCAs), with commonly prescribed medications including sertraline, paroxetine, venlafaxine, duloxetine, and amitriptyline [5, 6] [58].”

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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