Table 1.
Extraction table of the evaluated studies
| Study | Animal/human | Subject characteristics | Study design | Preventive/therapeutic | Stress protocol | Exercise protocol | Memory assessment | Main findings | Speculated mechanisms |
|---|---|---|---|---|---|---|---|---|---|
| Grace (2009) [56] | Animal | Sprague-Dawley rats | Experimental | Therapeutic | Deprived from their mothers for 3 h/day for 12 days | Voluntary access to running wheels for 20 days after the maternal separation | Morris water maze, object recognition | Maternal separation did not impair memory. Exercise, however, improved memory function | N/A |
| Mello (2009) [57] | Animal | Wistar rats (3–4 months) | Experimental | Therapeutic | Deprived from their mothers for 3 h/day during first 10 days of life | At day 45, engaged in forced treadmill exercise; 50 min/day, 5 days/week, 8 total weeks | Morris water maze, object recognition, inhibitory avoidance | Exercise reversed the deficit of inhibitory avoidance and reduced the deficit of spatial memory | Exercise may attenuate HPA-axis activity |
| Makena (2012) [58] | Animal | Sprague-Dawley rats | Experimental | Therapeutic | Deprived from their mothers for 3 h/day for 12 days | Voluntary access to running wheels for ~ 20 days after the maternal separation | Objective recognition task | Maternal separation enhanced memory function. Maternal separation also prevented exercise-induced MAPK/ERK signaling | N/A |
| Kim (2013) [59] | Animal | Sprague-Dawley rats | Experimental | Therapeutic | 95 dB supersonic machine sound (1 h/day) during pregnancy | After delivery, rat pups exercise on the treadmill for 30 min/day for 7 days, starting 4 weeks after birth | Radial 8-arm maze test | Stress protocol suppressed neurogenesis in the offspring and also impaired memory. Exercise attenuated these effects. Mild-intensity exercise was more effective than high-intensity exercise | Exercise-induced neurogenesis |
| Kim (2013) [60] | Animal | Sprague-Dawley rats | Experimental | Therapeutic | Foot shocks, 3 times/day, for 7 consecutive days | 4 weeks of treadmill exercise, 30 min/day | Radial 8-arm maze test | Stress protocol impaired memory, suppressed cell proliferation in the hippocampus, which was attenuated with exercise | Exercise-induced cell proliferation in the dentate gyrus |
| Radahmadi (2013) [25] | Animal | Wistar rats | Experimental | The exercise training and stress protocol occurred concurrently | Restrained in Plexiglass cylinder for 6 h/day for 21 days | Treadmill running, 1 h/day, for 21 days | Passive avoidance learning test | Although exercise was effective in enhancing memory, exercise was not effective in improving passive avoidance acquisition and retention when exposed to the stress protocol | N/A |
| Castilla-Ortega (2014) [61] | Animal | C57BL/6 J | Experimental | Preventive | Chronic intermittent restraint stress; restrained for 13 days for 3.5 h/day | 6 days of daily exercise | What-When-Where task | Stress impaired neurogenesis and the “when” memory task, while exercise promoted neurogenesis and improved the “where” memory | The stressed exercising animals showed a larger increase in cell survival, maturation of new neurons in the dentate gyrus |
| Patki (2014) [62] | Animal | Sprague-Dawley rats | Experimental | Therapeutic | Social defeat model; seven encounters for 7 consecutive days | After stress exposure, engaged in treadmill exercise for 2 weeks (30 min/day) | Radial arm water maze | Stress impaired long-term memory (not short term), which was attenuated with exercise | Suppression of oxidative stress and inflammation. Modulation of deacetylation processes. Regulation of BDNF |
| Patki (2014) [63] | Animal | Wistar rats | Experimental | Therapeutic | Single stress exposure (2 h restraint, 20 min forced swimming, 15 min rest, and 1–2 min diethyl ether exposure) | After stress exposure, exercised on treadmill for 2 weeks (30 min/day) | Radial arm water maze | Stress impaired memory, which was attenuated with exercise | Increase in BDNF and attenuation of HPA axis |
| Neves (2015) [64] | Animal | Wistar rats | Experimental | Preventive | Maternal deprivation, 3 h/day, 10 days | 5 days/week of exercise, 50 min/day, for 8 weeks | Object recognition test, inhibitory avoidance test | Exercise prevented stress-induced memory impairment, for both short- and long-term memory | Exercise may attenuate stress-induced oxidative damage. The stress protocol increased lipid peroxidation, which was attenuated with exercise. Dopamine is metabolized by monoamine oxidase, producing hydrogen peroxide. Thus, increased dopamine turnover may induce oxidative stress, which may lead to cell death |
| Dief (2015) [65] | Animal | Wistar rats | Experimental | Preventive | Chronic immobilization stress for 10 days | 6 weeks of swimming, 5 days/week | T-maze for spatial memory | Exercise attenuated stress-induced impairment in spatial memory | Stress protocol decreased BDNF levels; exercise increased BDNF levels, which may have prevented the stress-induced impairments. Exercise also increased Ach levels |
| Kang (2015) [66] | Animal | C57BL/6 mice | Experimental | Preventive and therapeutic | 6 h daily restraint for 3 weeks. Restraint occurred during weeks 5–8 | Treadmill exercise (60 min/day, 5 days/week) occurred from week 1 to 8 | Water maze task | Stress induced memory impairment, which was counter-regulated by exercise | Stress markedly reduced hippocampal CREB/BDNF signaling, which was reversed by 8 weeks of treadmill exercise |
| Ozbeyli (2015) [67] | Animal | Wistar rats | Experimental | Preventive | Exposure to cat odor | 6 weeks of swimming, 5 days/week, 1 h/day | Object recognition task | Exercise had a protective effect against stress-induced memory decline | Decreasing oxidative damage parameters, such as lipid peroxidation, neutrophil infiltration and lucigenin activity |
| Radahmadi (2015) [68] | Animal | Wistar rats | Experimental | Preventive and therapeutic | 21-day restraint stress, 6 h/day | Treadmill running 1 h/day for 21 days | Passive avoidance task | Exercise had both a preventive and therapeutic effect on stress-induced memory function, but a greater therapeutic effect was observed | Increased antioxidant enzymes, regulation of glucocorticoid receptors, increased neurotrophic factors, increased muscarinic receptor density, and increased acetylcholine release |
| Leem (2016) [69] | Animal | C57BL/6 mice | Experimental | Therapeutic | 21-day restraint stress, 6 h/day | 3 weeks of treadmill exercise, 1 h/day, 6 days/week | Y-maze and water maze task | Restraint stress produced learning and memory deficits, which were reversed with the 3-week exercise protocol | Exercise-induced expression of BDNF |
| Wearick-Silva (2016) [70] | Animal | Balb/c mice | Experimental | Therapeutic | Maternal separation during first 2 weeks of life | 3-week running protocol, 60 min/day, 5 days/week | Object recognition task | Maternal separation impaired memory, which was reversed with exercise | Exercise-induced expression of BDNF |
| Chen (2017) [71] | Animal | Thy1-H | Experimental | Therapeutic | Restraint stress; 1 h/day for 14 days | Treadmill exercise, 1 h/day, 14 days | Novel discrimination task | Stress protocol induced dendritic spine loss and memory impairment, which was rescued with exercise | Dendritic spine density and BDNF expression |
| dos Santos (2017) [72] | Animal | Wistar rats | Experimental | Preventive | Chronic variable stress; 24-h water deprivation, 1-3 h restraint, 24-h food deprivation, forced swimming, isolation, inclination of home cage, and damp bedding | 20 min/day, 3 times/week, for 2 months | Inhibitory avoidance task | Stress protocol induced oxidative stress and impaired memory. Exercise prevented memory impairment | Exercise prevented stress-induced oxidative damage |
| Kochi (2017) [73] | Animal | Long-Evans rats | Experimental | Preventive | Social defeat paradigm | 30 min of treadmill exercise for 14 days | Radial arm water maze | Exercise, prior to the trauma experience, mitigated memory impairment | Exercise prior to the stressor reduced anxiety levels from the stressor, which may have preserved memory function |
| Lapmanee (2017) [74] | Animal | Wistar rats | Experimental | Preventive | Restraint stress (varied, 1–8 weeks) | Voluntary wheel running for 4 weeks | Morris water maze and object recognition task | Exercise prevented impairments in memory | Exercise-induced BDNF expression |
| Leem (2017) [75] | Animal | C57BL/6 mice | Experimental | Concurrent; exercise and stress occurring together | Restraint stress; 6 h/day for 21 days | Treadmill running for 4 weeks | Morris water maze and object recognition task | Stress protocol impaired memory, which was attenuated with exercise | AMPA-receptor mediated mechanisms |
| da Silva (2018) [76] | Animal | Wistar rats | Experimental | Preventive | Restraint stress with cylindrical acrylic tube | 30 days of treadmill exercise, 30 min/day | Object recognition test | Exercise, coupled with virgin coconut oil, ameliorated the effects of stress on memory impairment | Preventive effects may occur from the antioxidant capabilities of exercise and coconut oil |
| Miller (2018) [77] | Animal | C57BL/6 mice | Experimental | Preventive and concurrent | 5-min cold water swim on day 1, 30-min elevated platform stress on day 2, and 60-min restraint on day 3 | 4 weeks of voluntary wheel access | Radial arm maze | Stress alone impaired LTP and exercise alone increased LTP. Exercise with stress increased LTP more than stress only group. Exercise group made fewer errors in the memory task | Modulation of BDNF, TrkB, glucocorticoid, mineralo-corticoid, and dopamine |