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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Molecular mechanisms of physical exercise on depression in the elderly: a systematic review
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Differential impact of stress and environmental enrichment on corticolimbic circuits
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Voluntary resistance running with short distance enhances spatial memory related to hippocampal BDNF signaling
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“For example, circulating insulin-like growth factor-1 (IGF-1) levels increased following resistance exercise (6) and caused increased BDNF mRNA levels in the hippocampus (5).”
Background
Physical activity for brain health in older adults
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The beneficial effects of strength exercise on hippocampal cell proliferation and apoptotic signaling is impaired by anabolic androgenic steroids
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“In fact, we have recently demonstrated that 8 weeks of both aerobic and strength exercise improve learning and spatial memory through divergent molecular mechanisms (Cassilhas et al., 2012a).”
BackgroundMethodResultInfluentialSelf-citation
Protective effects of different exercise modalities in an Alzheimer’s disease-like model
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Physical Activity, Cognitive Function, and Brain Health: What Is the Role of Exercise Training in the Prevention of Dementia?
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The effect of physical exercise on circulating brain‐derived neurotrophic factor in healthy subjects: A meta‐analysis of randomized controlled trials
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“Based on current evidences, aerobic exercise has been proved to be successful in improving circulating BDNF (Cassilhas et al., 2012; Dinoff et al., 2016), while strength training seems to be mostly ineffective (Huang et al., 2014; Knaepen et al., 2010).”
Background
Resistance exercise improves hippocampus-dependent memory
Cassilhas, R. C., Lee, K. S., Venâncio, D. P., Oliveira, M. G. M., Tufik, S., & de Mello, M. T. (2012) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2012007500138 · Cited by 64
“This crosstalk between peripheral and central compartments makes the IGF-1/IGF-1R signaling pathway an interesting therapeutic target for neurological disorders (35).”
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A strength exercise program in rats with epilepsy is protective against seizures
Peixinho-Pena, L. F., Fernandes, J., de Almeida, A. A., Gomes, F. G. N., Cassilhas, R. C., Venâncio, D. P., de Mello, M. T., Scorza, F. A., Cavalheiro, É. A., & Arida, R. M. (2012) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2012.08.011 · Cited by 68
“Because it is important to indicate the effectiveness of the strength exercise protocol and to demonstrate the positive impact of strength exercise in the present investigation, we confirmed by histological analysis of the FDL muscle that the strength exercise protocol was efficient in causing muscle hypertrophy [23,2…”
Self-citation
Effects of Resistance Exercise on Cerebral Redox Regulation and Cognition: An Interplay Between Muscle and Brain
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The Effect of Different Intensities of Treadmill Exercise on Cognitive Function Deficit Following a Severe Controlled Cortical Impact in Rats
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“An animal study found that endurance training increased BDNF in the brain as well as tyrosine kinase B receptor, while resistance training did not but increased insulin growth factor 1 and its receptor (Cassilhas et al., 2012), triggering the hypothesis that both aerobic and resistance training can employ divergent mo…”
BackgroundResult
Resistance Exercise May Improve Spatial Awareness and Visual Reaction in Older Adults
Fragala, M. S., Beyer, K. S., Jajtner, A. R., Townsend, J. R., Pruna, G. J., Boone, C. H., Bohner, J. D., Fukuda, D. H., Stout, J. R., & Hoffman, J. R. (2014) · The Journal of Strength and Conditioning Research · doi:10.1519/jsc.0000000000000520 · Cited by 61
“judgment of proprioception and evaluation of loads, which activate different regions of the brain (6,8).”
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Sports can protect dynamic visual acuity from aging: A study with young and older judo and karate martial arts athletes
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Result
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BackgroundMethod
Resistance Exercise Decreases Amyloid Load and Modulates Inflammatory Responses in the APP/PS1 Mouse Model for Alzheimer’s Disease
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“In fact, RE has been suggested to increase IGF-1 in both humans and animals, which in turn crosses the blood-brain barrier and seems to be related to neurogenic processes [14, 22, 40].”
Influential
Resistance Exercise Reduces Seizure Occurrence, Attenuates Memory Deficits and Restores BDNF Signaling in Rats with Chronic Epilepsy
de Almeida, A. A., da Silva, S. G., Lopim, G. M., Campos, D. V., Fernandes, J., Cabral, F. R., & Arida, R. M. (2017) · Neurochemical Research · doi:10.1007/s11064-016-2165-9 · Cited by 55
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Does physical exercise improve perceptual skills and visuospatial attention in older adults? A review
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Executive function after exhaustive exercise
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Neurotrophic growth factor responses to lower body resistance training in older adults
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“In addition, cerebral blood flow decreases in ischemic region (Cupini et al., 2001; Zhang et al., 2013a) while the reduced vessel density in aging brain leads to an overall reduced blood flow and oxygenation into the brain (Petcu et al., 2010).”
BackgroundInfluential
The Effect of Different Exercise Modes on Domain-Specific Cognitive Function in Patients Suffering from Parkinson’s Disease: A Systematic Review of Randomized Controlled Trials
Stuckenschneider, T., Askew, C. D., Menêses, A. L., Baake, R., Weber, J., & Schneider, S. (2019) · Journal of Parkinson s Disease · doi:10.3233/jpd-181484 · Cited by 48
“…exercise improves hippocampal volume, modulated by a higher expression of brain-derived neurotrophic factor (BDNF) [49, 51, 113, 114], whereas resistance exercise more likely produces higher concentrations of insulin-like growth factor 1 (IGF-1), with a smaller, or no, increase in BDNF [114, 115].”
Effects of Exercise on Type 2 Diabetes Mellitus-Related Cognitive Impairment and Dementia
Callisaya, M. L., & Nosaka, K. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-161154 · Cited by 48
“The mechanisms at play may be through improvement in cardio-metabolic profiles in addition to increased cerebral blood flow, BDNF, angiogensesis, synaptogenesis, and neurogenesis [11, 70].”
Background
High-intensity interval training improves cerebellar antioxidant capacity without affecting cognitive functions in rats
Freitas, D. A., Rocha‐Vieira, E., Sousa, R. A. L. D., Soares, B. A., Rocha‐Gomes, A., Garcia, B. C. C., Cassilhas, R. C., Mendonça, V. A., Camargos, A. C. R., Gregorio, J. A. M. D., et al. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112181 · Cited by 47
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Effects of physical activity on cognitive function among patients with diabetes in China: a nationally longitudinal study
Bai, A., Tao, L., Huang, J., Tao, J., & Liu, J. (2021) · BMC Public Health · doi:10.1186/s12889-021-10537-x · Cited by 44
Moderate-intensity continuous training and high-intensity interval training improve cognition, and BDNF levels of middle-aged overweight men
de Lima, N. S., Sousa, R. A. L. D., Amorim, F. T., Gripp, F., Magalhães, C. O. D. E., Pinto, S. H., Dias‐Peixoto, M. F., Monteiro-Júnior, R. S., Bourbeau, K., & Cassilhas, R. C. (2021) · Metabolic Brain Disease · doi:10.1007/s11011-021-00859-5 · Cited by 44
Self-citation
Comparison of the Effect of Exercise on Late-Phase LTP of the Dentate Gyrus and CA1 of Alzheimer’s Disease Model
Dao, A. T., Zagaar, M. A., Levine, A. T., & Alkadhi, K. A. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9612-5 · Cited by 43
“Our previous findings showed that the basal levels of hippocampal BDNF were markedly upregulated with exercise [6, 19], confirming similar findings reported by other investigators [43, 44].”
Result

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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