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Cardiovascular exercise and motor learning in non-disabled individuals: A systematic review with a behavioral emphasis

Abstract

Aim:

This systematic review aimed to investigate the acute effects of cardiovascular exercise on motor learning of non-disabled individuals.

Methods:

Forty studies were identified through database searching (PsycINFO, CENTRAL, Google Scholar, Scielo, and PUBMED). The studies demonstrated heterogeneity and were classified into two categories to guide the analyses: (1) – studies that investigated the effects of exercise-induced fatigue during practice on the performance in the retention test; (2) – studies that verified the acute impact of the cardiovascular exercise in close temporal proximity to the task practice on motor learning.

Results:

The studies demonstrated that (1) - the practice under fatigue conditions did not impair motor learning and that (2) – the cardiovascular exercise bout performed in close temporal proximity to task practice enhances the motor learning processes.

Conclusion:

Cardiovascular exercise enhances motor learning processes; however, these priming effects are dependents on the timing between practice and exercise, type of exercise, and task characteristics.

Keywords
aerobic exercise; motor learning; cardiovascular exercise; priming

Introduction

The development of neuromodulatory strategies to enhance motor skill acquisition can benefit the intervention of several movement professionals (e.g., physical education professionals, personal trainers, yoga and pilates instructors, sports coaches, physiotherapists, physicians). Among other alternatives, cardiovascular exercise is a cost-effective approach to enhance the capacity of the neuromotor system to be more receptive to practice and optimize motor learning and recovery11. Stoykov ME, Corcos DM, Madhavan S. Movement-Based Priming: Clinical Applications and Neural Mechanisms. J Mot Behav. 2017;49(1):88-97. doi:10.1080/00222895.2016.1250716
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2. Moriarty TA, Mermier C, Kravitz L, Gibson A, Beltz N, Zuhl M. Acute Aerobic Exercise Based Cognitive and Motor Priming: Practical Applications and Mechanisms. Front Psychol. 2019;10. doi:10.3389/fpsyg.2019.02790
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-33. Taubert M, Villringer A, Lehmann N. Endurance Exercise as an “Endogenous” Neuro-enhancement Strategy to Facilitate Motor Learning. Front Hum Neurosci. 2015;9. doi:10.3389/fnhum.2015.00692
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.

Cardiovascular exercise stimulates neuropsychological mechanisms associated with better motor learning outcomes, such as better blood flow and oxygenation44. Tsubaki A, Morishita S, Tokunaga Y, Sato D, Tamaki H, Yamazaki Y et al. Changes in Cerebral Oxyhaemoglobin Levels During and After a Single 20-Minute Bout of Moderate-Intensity Cycling. In: Oxygen Transport to Tissue XL. Berlin: Springer; 2018:127-131. doi:10.1007/978-3-319-91287-5_20
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, an increase of cerebral volume5,5. Kleim JA, Cooper NR, VandenBerg PM. Exercise induces angiogenesis but does not alter movement representations within rat motor cortex. Brain Res. 2002;934(1):1-6. doi:10.1016/S0006-8993(02)02239-4
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66. Smith PJ, Blumenthal JA, Hoffman BM, et al. Aerobic exercise and neurocognitive performance: a meta-analytic review of randomized controlled trials. Psychosom Med. 2010;72(3):239-252. doi:10.1097/PSY.0b013e3181d14633
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and secretion of neurotransmitters and catecholamines77. McMorris T, Collard K, Corbett J, Dicks M, Swain JP. A test of the catecholamines hypothesis for an acute exercise–cognition interaction. Pharmacol Biochem Behav. 2008;89(1):106-15. doi:10.1016/j.pbb.2007.11.007
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, and enhancement of neuroplasticity and neurogenesis through a hyperregulation of Brain-Derived Neurotrophic Factor (BDNF) and Neurotrophin-388. Cotman CW, Berchtold NC. Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 2002;25(6):295-301. doi:Exercise: a behavioral intervention to enhance brain health and plasticity.9. Knaepen K, Goekint M, Heyman EM, Meeusen R. Neuroplasticity ? Exercise-Induced Response of Peripheral Brain-Derived Neurotrophic Factor. Sport Med. 2010;40(9):765-801. doi:10.2165/11534530-000000000-00000
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10. Marlatt MW, Lucassen PJ, van Praag H. Comparison of neurogenic effects of fluoxetine, duloxetine, and running in mice. Brain Res. 2010;1341:93-9. doi:10.1016/j.brainres.2010.03.086
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-1111. Rasmussen P, Brassard P, Adser H, et al. Evidence for a release of brain-derived neurotrophic factor from the brain during exercise. Exp Physiol. 2009;94(10):1062-9. doi:10.1113/expphysiol.2009.048512
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.

These positive effects on the Central Nervous System (CNS) have been associated with enhancements on the motor memory creation process and, consequently, on motor learning3,3. Taubert M, Villringer A, Lehmann N. Endurance Exercise as an “Endogenous” Neuro-enhancement Strategy to Facilitate Motor Learning. Front Hum Neurosci. 2015;9. doi:10.3389/fnhum.2015.00692
https://doi.org/10.3389/fnhum.2015.00692...
1212. Mang CS, Campbell KL, Ross CJD, Boyd LA. Promoting Neuroplasticity for Motor Rehabilitation After Stroke: Considering the Effects of Aerobic Exercise and Genetic Variation on Brain-Derived Neurotrophic Factor. Phys Ther. 2013;93(12):1707-16. doi:10.2522/ptj.20130053
https://doi.org/10.2522/ptj.20130053...
. Cardiovascular exercise may induce better motor performance during the acquisition phase and retention test, when performed in temporal proximity to the motor practice (immediately before or after). These results suggest that cardiovascular exercise improves the encoding and consolidation processes of motor memory creation1313. Roig M, Thomas R, Mang CS, et al. Time-Dependent Effects of Cardiovascular Exercise on Memory. Exerc Sport Sci Rev. 2016;44(2):81-8. doi:10.1249/JES.0000000000000078
https://doi.org/10.1249/JES.000000000000...
14. Labban JD, Etnier JL. Effects of acute exercise on long-term memory. Res Q Exerc Sport. 2011. doi:10.1080/02701367.2011.10599808
https://doi.org/10.1080/02701367.2011.10...
-1515. Hasan SMM, Rancourt SN, Austin MW, Ploughman M. Defining Optimal Aerobic Exercise Parameters to Affect Complex Motor and Cognitive Outcomes after Stroke: A Systematic Review and Synthesis. Neural Plast. 2016;2016:1-12. doi:10.1155/2016/2961573
https://doi.org/10.1155/2016/2961573...
.

Nevertheless, the impact of cardiovascular exercise on the motor learning process is mediated by multiple factors, such as the nature of the motor task and exercise characteristics (i.e., intensity and type). This systematic review aimed to investigate the acute effects of cardiovascular exercise on motor learning of non-disabled individuals. We presented the impacts of each potential factor that influence the relationship between cardiovascular exercise and motor learning (i.e., motor task characteristics, the timing between cardiovascular exercise and practice, exercise intensity, and exercise features).

Material and methods

Identification and selection of studies

PsycINFO, Pubmed, CENTRAL, Google Scholar, and Scielo databases were searched from 1968 to April 2020. The selection of studies was run from January 2020 to June 2020. The search strategy comprised the following keywords and Boolean Operators: (“motor learning” OR “motor memory”) AND (“aerobic exercise” OR “high-intensity interval training” OR HIIT OR “cardiovascular exercise”), without the addition of filters to the search. Additionally, the reference list of the studies included was reviewed to identify other relevant studies.

Eligibility criteria

The eligibility criteria for include the studies were: 1) Experimental studies investigating the acute effects of cardiovascular exercise (before, during, or after practice) on motor learning. 2) Studies with non-disabled individuals, 3) Studies with an acquisition phase (motor practice), and a retention test or a transfer test in the experimental design. 4) Dependent variable based on the motor performance (either acquisition or retention and transfer test). 5) Studies in English.

The exclusion criteria were: 1 - Experimental studies that exclusively investigated mechanisms (without motor performance analysis) related to the effects of cardiovascular exercise on the motor learning process (i.e., neurophysiological, genetic, or neuroimages studies), 2 - Studies with disabling or clinical participants (i.e., stroke survivors and people with Parkinson's disease) or non-human sample. 3 - Studies with no retention (at least 1 h after practice) or transfer tests in the experimental design. 4 - Intervention-based studies that investigated resistance or strength exercises. 5 - Studies investigating the chronic impact of the cardiovascular exercise or fitness level on motor learning and executive function. 6 - Studies including tasks without motor demand (i.e., perceptual tasks). 7 - Pilot and review studies. 8 - Not published and preprint studies (e.g., thesis and dissertations), 9 - Methodological inconsistency or discrepancy in data analysis (e.g., to promote practice immediately before retention test).

Data extraction and analysis

Data extraction followed the items: sample characteristics, motor task characteristics, methodology (research design), exercise parameters, and results related to behavior outcome (motor performance).

The selected studies showed heterogeneity concerning method and procedures. Some studies investigated exercise as a neuromodulatory strategy to enhance motor performance and learning without exhausting exercise protocols and choosing motor tasks unrelated to exercise (i.e., stationary bike and upper limb motor tasks). In contrast, other studies investigated the effects of exercise-induced fatigue during task practice on motor learning, with exhaustion exercise protocols and/or choosing motor tasks related to exercise (i.e., running on treadmill and Bachman Ladder Climb). Thus, we separated these studies into two subcategories: fatigue studies and non-fatigued studies to better guide the studies analysis.

There is no specific instrument to assess methodological rigor in motor learning studies. This review used the methodological quality assessment employed in the motor learning systematic review developed by Subramanian et al.1616. Subramanian SK, Massie CL, Malcolm MP, Levin MF. Does Provision of Extrinsic Feedback Result in Improved Motor Learning in the Upper Limb Poststroke? A Systematic Review of the Evidence. Neurorehabil Neural Repair. 2010;24(2):113-24. doi:10.1177/1545968309349941
https://doi.org/10.1177/1545968309349941...
.

Firstly, the studies were evaluated using the PEDro Scale1717. Moseley AM, Herbert RD, Sherrington C, Maher CG. Evidence for physiotherapy practice: A survey of the Physiotherapy Evidence Database (PEDro). Aust J Physiother. 2002;48(1):43-9. doi:10.1016/S0004-9514(14)60281-6
https://doi.org/10.1016/S0004-9514(14)60...
, with some items adapted to the motor learning background. PEDro Scale has been proposed to assess the quality of controlled trials; however, its acceptance as a strength criterion for experimental research quality allows its application in other contexts, including motor learning reviews1616. Subramanian SK, Massie CL, Malcolm MP, Levin MF. Does Provision of Extrinsic Feedback Result in Improved Motor Learning in the Upper Limb Poststroke? A Systematic Review of the Evidence. Neurorehabil Neural Repair. 2010;24(2):113-24. doi:10.1177/1545968309349941
https://doi.org/10.1177/1545968309349941...
. In PEDro Scale, 11-items allow evaluating the generalizability of the findings (criteria 1), blinding methods, randomization and internal validity details (criteria 2-9), and data analysis and statistical reporting (criteria 10-11). The PEDro items adaptations and the assessment of each item of the scale for each study included in this review can be found in the Supplementary Material.

The assessment of the quality of the studies was performed based on the methodology described previoulsy1616. Subramanian SK, Massie CL, Malcolm MP, Levin MF. Does Provision of Extrinsic Feedback Result in Improved Motor Learning in the Upper Limb Poststroke? A Systematic Review of the Evidence. Neurorehabil Neural Repair. 2010;24(2):113-24. doi:10.1177/1545968309349941
https://doi.org/10.1177/1545968309349941...
. Then, the score derived from the PEDro Scale was classified by following conditions proposed by Foley et al.,1818. Foley NC, Teasell RW, Bhogal SK, Doherty T, Speechley MR. The Efficacy of Stroke Rehabilitation: A Qualitative Review. Top Stroke Rehabil. 2003;10(2):1-18. doi:10.1310/AQE1-PCW1-FW9K-M01G
https://doi.org/10.1310/AQE1-PCW1-FW9K-M...
: 9 to 10, excellent; 6 to 8, good; 4 to 5, fair; and < 4, poor. Following, Sackett's evidence levels were used to determine the strength of the conclusions for each analysis of this review1919. Sackett DL, Richardson WS, Rosenberg W, Haynes RB. Evidence-Based Medicine: How to Practice and Teach EBM. 2nd ed. New York, NY: Churchill Livingstone; 2002.. The evidence was classified in 1A (≥ 2 good or excellent studies supported it), 1B (1 good or excellent study supported it), 2A (≥ 1 fair study supported it), 2B (PEDro score ≤ 3 studies or nonrandomized studies supported it), 3 (several pre-post design studies showed similar results), 4 (indicated contradictory results of ≥ 2 studies with similar design and quality) or 5 (absence of experimental studies).

Both authors evaluated the methodological quality of the studies included, including a third person who was consulted in case of incoherence in the PEDro scores (physiotherapist, Master Degree, and Ph.D. student in Motor Behavior area).

Results

It was found a total of 6542 records. Removing duplicates and screening for title and abstract resulted in 54 articles considered for full-text assessment. In the eligibility criteria assessment, 14 studies were excluded (7 with no retention test, 1 duplicated, 1 showed methodological inconsistency in the data extraction and analyses, 2 studies investigated genetic and neurophysiological mechanisms exclusively, 1 study did not demonstrate motor performance analyses, 1 study used a perceptual task with no motor demand, and 1 study investigated the effect of the strength exercise). Figure 1 demonstrates the flow of study selection.

Figure 1
Flowchart of the study.

From 40 studies included, none were classified as excellent, 27 studies were considered good (6 to 8 points in the PEDro scale), 20 studies were classified as fair (4 to 5 points in the PEDro scale), and one study was classified as poor (< 4 points in PEDro scale). Ten studies did not perform the allocation process by a random process (or they did not relate it in the manuscript), which compromises their evidence level. Two studies were composed of 2 experiments20,20. Statton MA, Encarnacion M, Celnik P, Bastian AJ. A Single Bout of Moderate Aerobic Exercise Improves Motor Skill Acquisition. Gribble PL, ed. PLoS One. 2015;10(10):e0141393. doi:10.1371/journal.pone.0141393
https://doi.org/10.1371/journal.pone.014...
2121. Tomporowski PD, Pendleton DM. Effects of the Timing of Acute Exercise and Movement Complexity on Young Adults’ Psychomotor Learning. J Sport Exerc Psychol. 2018;40(5):240-8. doi:10.1123/jsep.2017-0289
https://doi.org/10.1123/jsep.2017-0289...
; each experiment was analyzed separately. Table 1 demonstrates the main characteristics and results of all studies included in this review.22. Cochran BJ. Effect of Physical Fatigue on Learning to Perform a Novel Motor Task. Res Q Exerc Sport. 1975;46(2):243-9. doi:10.1080/10671315.1975.10615329
https://doi.org/10.1080/10671315.1975.10...
24. Carron A V. Physical Fatigue and Motor Learning. Res Q Am Assoc Heal Phys Educ Recreat. 1969;40(4):682-6. doi:10.1080/10671188.1969.10614902
https://doi.org/10.1080/10671188.1969.10...
25. Schmidt RA. Performance and Learning a Gross Motor Skill under Conditions of Artificially-Induced Fatigue. Res Q Am Assoc Heal Phys Educ Recreat. 1969;40(1):185-90. doi:10.1080/10671188.1969.10616658
https://doi.org/10.1080/10671188.1969.10...
26. Godwin MA, Schmidt RA. Muscular Fatigue and Learning a Discrete Motor Skill. Res Q Am Assoc Heal Phys Educ Recreat. 1971;42(4):374-82. doi:10.1080/10671188.1971.10615084
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27. Michael Pack D, Cotten DJ, Biasiotto J. Effect of Four Fatigue Levels on Performance and Learning of a Novel Dynamic Balance Skill. J Mot Behav. 1974;6(3):191-7. doi:10.1080/00222895.1974.10734995
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28. Williams J, Singer RN. Muscular Fatigue and the Learning and Performance of a Motor Control Task. J Mot Behav. 1975;7(4):265-9. doi:10.1080/00222895.1975.10735044
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Table 1
Characteristics and results from the included studies.

Discussion

General findings

The main findings of this review show us the acute benefits effects of cardiovascular exercise on motor performance and learning. Previous studies showed that exercise-induced fatigue does not impair motor learning, mainly when exercise does not involve the same motor effector related to motor task performance. Also, the effects of cardiovascular exercise on motor learning are more evident when the exercise is carried out in temporal proximity to the practice; moreover, depending on the order between exercise and practice, the priming effects may have a different impact on the motor learning process.

Two fatigue studies demonstrated the adverse effects of fatigue on motor learning. Benson2323. Benson DW. Influence of Imposed Fatigue on Learning a Jumping Task and a Juggling Task. Res Q Am Assoc Heal Phys Educ Recreat. 1968;39(2):251-7. doi:10.1080/10671188.1968.10618045
https://doi.org/10.1080/10671188.1968.10...
demonstrated that the fatigue induced by stationary bike impaired the jumping task learning, and Carron & Ferchuk3131. Carron A V., Ferchuk AD. The Effect of Fatigue on Learning and Performance of a Gross Motor Task. J Mot Behav. 1971;3(1):62-8. doi:10.1080/00222895.1971.10734893
https://doi.org/10.1080/00222895.1971.10...
reported that the fatigue induced by stationary bike mitigated the balance stabilometer task learning. In sum, the excessive fatigue induced by cardiovascular exercise only impacts motor performance. Fatigue conditions may not be related to motor learning. The level of this evidence is 2A.

Besides, cardiovascular exercise seems to be a possible strategy to prime the CNS and induce better motor practice. From the 30 non-fatigue studies investigating the cardiovascular effects on motor learning, 19 demonstrated some positive effects from cardiovascular exercise on motor performance20,20. Statton MA, Encarnacion M, Celnik P, Bastian AJ. A Single Bout of Moderate Aerobic Exercise Improves Motor Skill Acquisition. Gribble PL, ed. PLoS One. 2015;10(10):e0141393. doi:10.1371/journal.pone.0141393
https://doi.org/10.1371/journal.pone.014...
32,32. Snow NJ, Mang CS, Roig M, McDonnell MN, Campbell KL, Boyd LA. The effect of an acute bout of moderate-intensity aerobic exercise on motor learning of a continuous tracking task. PLoS One. 2016;11(2):1-16. doi:10.1371/journal.pone.0150039
https://doi.org/10.1371/journal.pone.015...
3333. Neva JL, Ma JA, Orsholits D, Boisgontier MP, Boyd LA. The effects of acute exercise on visuomotor adaptation, learning, and inter-limb transfer. Exp Brain Res. 2019;237:1109-27. doi:10.1007/s00221-019-05491-5
https://doi.org/10.1007/s00221-019-05491...
or learning21,21. Tomporowski PD, Pendleton DM. Effects of the Timing of Acute Exercise and Movement Complexity on Young Adults’ Psychomotor Learning. J Sport Exerc Psychol. 2018;40(5):240-8. doi:10.1123/jsep.2017-0289
https://doi.org/10.1123/jsep.2017-0289...
3333. Neva JL, Ma JA, Orsholits D, Boisgontier MP, Boyd LA. The effects of acute exercise on visuomotor adaptation, learning, and inter-limb transfer. Exp Brain Res. 2019;237:1109-27. doi:10.1007/s00221-019-05491-5
https://doi.org/10.1007/s00221-019-05491...
34. Thomas R, Flindtgaard M, Skriver K, et al. Acute exercise and motor memory consolidation: Does exercise type play a role? Scand J Med Sci Sports. 2017;27(11):1523-32. doi:10.1111/sms.12791
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35. Lundbye-Jensen J, Skriver K, Nielsen JB, Roig M. Acute Exercise Improves Motor Memory Consolidation in Preadolescent Children. Front Hum Neurosci. 2017;11(April):1-10. doi:10.3389/fnhum.2017.00182
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36. Stavrinos EL, Coxon JP. High-intensity interval exercise promotes motor cortex disinhibition and early motor skill consolidation. J Cogn Neurosci. 2017;29(4):593-604. doi:10.1162/jocn_a_01078
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37. Dal Maso F, Desormeau B, Boudrias M-H, Roig M. Acute cardiovascular exercise promotes functional changes in cortico-motor networks during the early stages of motor memory consolidation. Neuroimage. 2018;174:380-92. doi:10.1016/j.neuroimage.2018.03.029
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38. Ferrer-Uris B, Busquets A, Angulo-Barroso R. Adaptation and Retention of a Perceptual-Motor Task in Children: Effects of a Single Bout of Intense Endurance Exercise. J Sport Exerc Psychol. 2018;40(1):1-9. doi:10.1123/jsep.2017-0044
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39. Angulo-Barroso R, Ferrer-Uris B, Busquets A. Enhancing Children's Motor Memory Retention Through Acute Intense Exercise: Effects of Different Exercise Durations. Front Psychol. 2019;10:1-9. doi:10.3389/fpsyg.2019.02000
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44. Mang CS, Snow NJ, Campbell KL, Ross CJD, Boyd LA. A single bout of high-intensity aerobic exercise facilitates response to paired associative stimulation and promotes sequence-specific implicit motor learning. J Appl Physiol. 2014;117(11):1325-36. doi:10.1152/japplphysiol.00498.2014
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. In the 30 studies investigating the effects of cardiovascular exercise (without excessive fatigue) on motor learning (retention test), some of them reported null effects20,20. Statton MA, Encarnacion M, Celnik P, Bastian AJ. A Single Bout of Moderate Aerobic Exercise Improves Motor Skill Acquisition. Gribble PL, ed. PLoS One. 2015;10(10):e0141393. doi:10.1371/journal.pone.0141393
https://doi.org/10.1371/journal.pone.014...
32,32. Snow NJ, Mang CS, Roig M, McDonnell MN, Campbell KL, Boyd LA. The effect of an acute bout of moderate-intensity aerobic exercise on motor learning of a continuous tracking task. PLoS One. 2016;11(2):1-16. doi:10.1371/journal.pone.0150039
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53. Helm EE, Matt KS, Kirschner KF, Pohlig RT, Kohl D, Reisman DS. The influence of high-intensity exercise and the Val66Met polymorphism on circulating BDNF and locomotor learning. Neurobiol Learn Mem. 2017;144:77-85. doi:10.1016/j.nlm.2017.06.003
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54. Stranda H, Haga M, Sigmundsson H, Lorås H. The Effect of Aerobic Exercise on Speed and Accuracy Task Components in Motor Learning. Sports. 2019;7(3):54. doi:10.3390/sports7030054
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57. Ferrer-Uris B, Busquets A, Lopez-Alonso V, Fernandez-del-Olmo M, Angulo-Barroso R. Enhancing consolidation of a rotational visuomotor adaptation task through acute exercise. PLoS One. 2017;12(4):e0175296. doi:10.1371/journal.pone.0175296
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, but anyone demonstrated adverse effects.

Therefore, it can be supposed that the evidence that cardiovascular exercise enhances motor learning has a level of 4 (conflicting results). In this case, the positive effect of cardiovascular exercise on motor learning is multifactorial, and it depends mainly on the task and exercise characteristics and the timing of exposure of the exercise in relation to the practice.

Specifically, regarding the motor performance during practice, the findings demonstrated that a cardiovascular exercise bout before motor practice improves the subsequent motor performance concerning the error rate2020. Statton MA, Encarnacion M, Celnik P, Bastian AJ. A Single Bout of Moderate Aerobic Exercise Improves Motor Skill Acquisition. Gribble PL, ed. PLoS One. 2015;10(10):e0141393. doi:10.1371/journal.pone.0141393
https://doi.org/10.1371/journal.pone.014...
, temporal synchronization3232. Snow NJ, Mang CS, Roig M, McDonnell MN, Campbell KL, Boyd LA. The effect of an acute bout of moderate-intensity aerobic exercise on motor learning of a continuous tracking task. PLoS One. 2016;11(2):1-16. doi:10.1371/journal.pone.0150039
https://doi.org/10.1371/journal.pone.015...
, kinematics reaching accuracy measures, time duration, and reaction time3333. Neva JL, Ma JA, Orsholits D, Boisgontier MP, Boyd LA. The effects of acute exercise on visuomotor adaptation, learning, and inter-limb transfer. Exp Brain Res. 2019;237:1109-27. doi:10.1007/s00221-019-05491-5
https://doi.org/10.1007/s00221-019-05491...
.

The cardiovascular exercise benefits on motor memory consolidation were reported in the retention tests from 5 h3636. Stavrinos EL, Coxon JP. High-intensity interval exercise promotes motor cortex disinhibition and early motor skill consolidation. J Cogn Neurosci. 2017;29(4):593-604. doi:10.1162/jocn_a_01078
https://doi.org/10.1162/jocn_a_01078...
to 7 days21,21. Tomporowski PD, Pendleton DM. Effects of the Timing of Acute Exercise and Movement Complexity on Young Adults’ Psychomotor Learning. J Sport Exerc Psychol. 2018;40(5):240-8. doi:10.1123/jsep.2017-0289
https://doi.org/10.1123/jsep.2017-0289...
35,35. Lundbye-Jensen J, Skriver K, Nielsen JB, Roig M. Acute Exercise Improves Motor Memory Consolidation in Preadolescent Children. Front Hum Neurosci. 2017;11(April):1-10. doi:10.3389/fnhum.2017.00182
https://doi.org/10.3389/fnhum.2017.00182...
38,38. Ferrer-Uris B, Busquets A, Angulo-Barroso R. Adaptation and Retention of a Perceptual-Motor Task in Children: Effects of a Single Bout of Intense Endurance Exercise. J Sport Exerc Psychol. 2018;40(1):1-9. doi:10.1123/jsep.2017-0044
https://doi.org/10.1123/jsep.2017-0044...
43,43. Roig M, Skriver K, Lundbye-Jensen J, Kiens B, Nielsen JB. A Single Bout of Exercise Improves Motor Memory. Sinigaglia C, ed. PLoS One. 2012;7(9):e44594. doi:10.1371/journal.pone.0044594
https://doi.org/10.1371/journal.pone.004...
45,45. Skriver K, Roig M, Lundbye-Jensen J, Pingel J, Helge JW, Kiens B, et al. Acute exercise improves motor memory: Exploring potential biomarkers. Neurobiol Learn Mem. 2014;116:46-58. doi:10.1016/j.nlm.2014.08.004
https://doi.org/10.1016/j.nlm.2014.08.00...
4848. Thomas R, Johnsen LK, Geertsen SS, Christiansen L, Ritz C, Roig M et al. Acute Exercise and Motor Memory Consolidation: The Role of Exercise Intensity. Philp A, ed. PLoS One. 2016;11(7):e0159589. doi:10.1371/journal.pone.0159589
https://doi.org/10.1371/journal.pone.015...
. Nevertheless, it seems that cardiovascular exercise effects on motor memory consolidation are more robust in the long-term retention tests. For instance, some studies did not find the effect of the cardiovascular exercise in the short-term retention test (1-h or 1-day retention test); however, the exercise group demonstrated a better long-term retention test (7-days retention test) if compared to the control group34,34. Thomas R, Flindtgaard M, Skriver K, et al. Acute exercise and motor memory consolidation: Does exercise type play a role? Scand J Med Sci Sports. 2017;27(11):1523-32. doi:10.1111/sms.12791
https://doi.org/10.1111/sms.12791...
43,43. Roig M, Skriver K, Lundbye-Jensen J, Kiens B, Nielsen JB. A Single Bout of Exercise Improves Motor Memory. Sinigaglia C, ed. PLoS One. 2012;7(9):e44594. doi:10.1371/journal.pone.0044594
https://doi.org/10.1371/journal.pone.004...
5151. Jo JS, Chen J, Riechman S, Roig M, Wright DL. The protective effects of acute cardiovascular exercise on the interference of procedural memory. Psychol Res. 2019;83(7):1543-55. doi:10.1007/s00426-018-1005-8
https://doi.org/10.1007/s00426-018-1005-...
.

Concerning the consolidation of motor memory, Mang and colleagues6060. Mang CS, Snow NJ, Wadden KP, Campbell KL, Boyd LA. High-Intensity Aerobic Exercise Enhances Motor Memory Retrieval. Med Sci Sport Exerc. 2016;48(12):2477-2486. doi:10.1249/MSS.0000000000001040
https://doi.org/10.1249/MSS.000000000000...
, and Opie and Semmler4040. Opie GM, Semmler JG. Acute Exercise at Different Intensities Influences Corticomotor Excitability and Performance of a Ballistic Thumb Training Task. Neuroscience. 2019;412:29-39. doi:10.1016/j.neuroscience.2019.05.049
https://doi.org/10.1016/j.neuroscience.2...
demonstrated that a cardiovascular exercise bout impacts the relearning of a serial motor sequence task and a thumb abduction task, respectively. Thus, cardiovascular exercise may influence the following motor practice sessions, providing a faster relearning rate than original learning.

Finally, cardiovascular exercise effects on motor learning seem to be multifactorial, including motor tasks and exercise characteristics. In the following sections, each potential factor was analyzed separately.

Timing

The effects of cardiovascular exercise on the motor learning process may depend on exposure to the exercise concerning the practice. The exposure timing can be conjectured based on two aspects: 1 - The temporal proximity between cardiovascular exercise and practice. 2 - the order between cardiovascular exercise and practice.

Regarding the temporal proximity between cardiovascular exercise and practice, the findings have demonstrated that cardiovascular exercise must be performed in close temporal proximity to the practice to engage enhancements on motor performance and learning. Hence, Statton et al.2020. Statton MA, Encarnacion M, Celnik P, Bastian AJ. A Single Bout of Moderate Aerobic Exercise Improves Motor Skill Acquisition. Gribble PL, ed. PLoS One. 2015;10(10):e0141393. doi:10.1371/journal.pone.0141393
https://doi.org/10.1371/journal.pone.014...
demonstrated that cardiovascular exercise performed immediately before the practice improves motor performance more than when cardiovascular exercise is performed 1 h before the practice. Thomas, Beck, et al.4747. Thomas R, Beck MM, Lind RR, Korsgaard Johnsen L, Geertsen SS, Christiansen L et al. Acute Exercise and Motor Memory Consolidation: The Role of Exercise Timing. Neural Plast. 2016;2016:1-11. doi:10.1155/2016/6205452
https://doi.org/10.1155/2016/6205452...
demonstrated that performing cardiovascular exercise 20 min immediately after the practice induced better motor performance in the 1-day and 7-days retention tests than rest, or to perform cardiovascular exercise after 1 h or 2 h the practice. Therefore, the level of evidence for the temporal proximity between cardiovascular exercise and practice to enhance motor learning is 1B.

About the effects of the order between cardiovascular exercise and practice, it has been suggested that maybe the priming effects from the cardiovascular exercise on the motor memory creation processes are order-dependents12,12. Mang CS, Campbell KL, Ross CJD, Boyd LA. Promoting Neuroplasticity for Motor Rehabilitation After Stroke: Considering the Effects of Aerobic Exercise and Genetic Variation on Brain-Derived Neurotrophic Factor. Phys Ther. 2013;93(12):1707-16. doi:10.2522/ptj.20130053
https://doi.org/10.2522/ptj.20130053...
1313. Roig M, Thomas R, Mang CS, et al. Time-Dependent Effects of Cardiovascular Exercise on Memory. Exerc Sport Sci Rev. 2016;44(2):81-8. doi:10.1249/JES.0000000000000078
https://doi.org/10.1249/JES.000000000000...
. Therefore, whether the practitioner performs exercise before or during the practice, better motor performance is expected. On the other hand, whether the cardiovascular exercise is performed after the motor practice, an improvement in the consolidation process is expected, and therefore, a better retention test12,12. Mang CS, Campbell KL, Ross CJD, Boyd LA. Promoting Neuroplasticity for Motor Rehabilitation After Stroke: Considering the Effects of Aerobic Exercise and Genetic Variation on Brain-Derived Neurotrophic Factor. Phys Ther. 2013;93(12):1707-16. doi:10.2522/ptj.20130053
https://doi.org/10.2522/ptj.20130053...
1313. Roig M, Thomas R, Mang CS, et al. Time-Dependent Effects of Cardiovascular Exercise on Memory. Exerc Sport Sci Rev. 2016;44(2):81-8. doi:10.1249/JES.0000000000000078
https://doi.org/10.1249/JES.000000000000...
.

However, the order-dependent hypothesis was not fully confirmed in the studies that investigated it. Roig et al.4343. Roig M, Skriver K, Lundbye-Jensen J, Kiens B, Nielsen JB. A Single Bout of Exercise Improves Motor Memory. Sinigaglia C, ed. PLoS One. 2012;7(9):e44594. doi:10.1371/journal.pone.0044594
https://doi.org/10.1371/journal.pone.004...
and Tomporowski and Pendleton2121. Tomporowski PD, Pendleton DM. Effects of the Timing of Acute Exercise and Movement Complexity on Young Adults’ Psychomotor Learning. J Sport Exerc Psychol. 2018;40(5):240-8. doi:10.1123/jsep.2017-0289
https://doi.org/10.1123/jsep.2017-0289...
demonstrated that performing cardiovascular exercise after the practice induced better retention than performing a cardiovascular exercise before the practice. In a contrary way, Ferrer-Uris et al.5757. Ferrer-Uris B, Busquets A, Lopez-Alonso V, Fernandez-del-Olmo M, Angulo-Barroso R. Enhancing consolidation of a rotational visuomotor adaptation task through acute exercise. PLoS One. 2017;12(4):e0175296. doi:10.1371/journal.pone.0175296
https://doi.org/10.1371/journal.pone.017...
did not demonstrate a significant difference in motor learning of adults who perform a cardiovascular exercise before or after the practice; and Ferrer-Uris et al.3838. Ferrer-Uris B, Busquets A, Angulo-Barroso R. Adaptation and Retention of a Perceptual-Motor Task in Children: Effects of a Single Bout of Intense Endurance Exercise. J Sport Exerc Psychol. 2018;40(1):1-9. doi:10.1123/jsep.2017-0044
https://doi.org/10.1123/jsep.2017-0044...
demonstrated that the children who perform cardiovascular exercise before the practice demonstrated better retention if compared to children who perform cardiovascular exercise after the practice.

Therefore, the order-dependent hypothesis must be more investigated for further conclusions; 2 good studies (both 7 points in PEDro scale) supported it, but 2 other good studies (both 7 points on PEDro scale) did not corroborate with that.

Exercise characteristics

Type

Most studies that were incorporated in this review used running or stationary bikes in their exercise protocol. Concerning the running studies, 4 of the 8 studies reported positive cardiovascular exercise effects on motor learning35,35. Lundbye-Jensen J, Skriver K, Nielsen JB, Roig M. Acute Exercise Improves Motor Memory Consolidation in Preadolescent Children. Front Hum Neurosci. 2017;11(April):1-10. doi:10.3389/fnhum.2017.00182
https://doi.org/10.3389/fnhum.2017.00182...
3838. Ferrer-Uris B, Busquets A, Angulo-Barroso R. Adaptation and Retention of a Perceptual-Motor Task in Children: Effects of a Single Bout of Intense Endurance Exercise. J Sport Exerc Psychol. 2018;40(1):1-9. doi:10.1123/jsep.2017-0044
https://doi.org/10.1123/jsep.2017-0044...
39. Angulo-Barroso R, Ferrer-Uris B, Busquets A. Enhancing Children's Motor Memory Retention Through Acute Intense Exercise: Effects of Different Exercise Durations. Front Psychol. 2019;10:1-9. doi:10.3389/fpsyg.2019.02000
https://doi.org/10.3389/fpsyg.2019.02000...
-4040. Opie GM, Semmler JG. Acute Exercise at Different Intensities Influences Corticomotor Excitability and Performance of a Ballistic Thumb Training Task. Neuroscience. 2019;412:29-39. doi:10.1016/j.neuroscience.2019.05.049
https://doi.org/10.1016/j.neuroscience.2...
. While of the 20 studies that used the stationary bike, 6 studies demonstrated the null effect of cardiovascular exercise on motor performance and learning32,32. Snow NJ, Mang CS, Roig M, McDonnell MN, Campbell KL, Boyd LA. The effect of an acute bout of moderate-intensity aerobic exercise on motor learning of a continuous tracking task. PLoS One. 2016;11(2):1-16. doi:10.1371/journal.pone.0150039
https://doi.org/10.1371/journal.pone.015...
51,51. Jo JS, Chen J, Riechman S, Roig M, Wright DL. The protective effects of acute cardiovascular exercise on the interference of procedural memory. Psychol Res. 2019;83(7):1543-55. doi:10.1007/s00426-018-1005-8
https://doi.org/10.1007/s00426-018-1005-...
52,52. Ostadan F, Centeno C, Daloze J-F, Frenn M, Lundbye-Jensen J, Roig M. Changes in corticospinal excitability during consolidation predict acute exercise-induced off-line gains in procedural memory. Neurobiol Learn Mem. 2016;136:196-203. doi:10.1016/j.nlm.2016.10.009
https://doi.org/10.1016/j.nlm.2016.10.00...
54,54. Stranda H, Haga M, Sigmundsson H, Lorås H. The Effect of Aerobic Exercise on Speed and Accuracy Task Components in Motor Learning. Sports. 2019;7(3):54. doi:10.3390/sports7030054
https://doi.org/10.3390/sports7030054...
55,55. Wanner P, Müller T, Cristini J, Pfeifer K, Steib S. Exercise Intensity Does not Modulate the Effect of Acute Exercise on Learning a Complex Whole-Body Task. Neuroscience. 2020;426:115-28. doi:10.1016/j.neuroscience.2019.11.027
https://doi.org/10.1016/j.neuroscience.2...
5858. Baird JF, Gaughan ME, Saffer HM, et al. The effect of energy-matched exercise intensity on brain-derived neurotrophic factor and motor learning. Neurobiol Learn Mem. 2018;156:33-44. doi:10.1016/j.nlm.2018.10.008
https://doi.org/10.1016/j.nlm.2018.10.00...
. Only 1 study used an upper body ergometer for cardiovascular exercise prescription, and it did not report the positive effect of cardiovascular exercise on the learning of a locomotor skill5353. Helm EE, Matt KS, Kirschner KF, Pohlig RT, Kohl D, Reisman DS. The influence of high-intensity exercise and the Val66Met polymorphism on circulating BDNF and locomotor learning. Neurobiol Learn Mem. 2017;144:77-85. doi:10.1016/j.nlm.2017.06.003
https://doi.org/10.1016/j.nlm.2017.06.00...
. Besides, 1 study used a whole-body exercise involving upper and lower limbs in the exercise, and it did not demonstrate the positive effects of the exercise on locomotor learning5959. Charalambous CC, French MA, Morton SM, Reisman DS. A single high-intensity exercise bout during early consolidation does not influence retention or relearning of sensorimotor locomotor long-term memories. Exp Brain Res. 2019;237(11):2799-810. doi:10.1007/s00221-019-05635-7
https://doi.org/10.1007/s00221-019-05635...
.

From these findings, it can be considered that maybe the effects of cardiovascular exercise on motor learning are more evident for exercises that use exclusively the motor effector that is not involved in the performance of the motor task. More investigations about this topic should be run because the level of this evidence is 4.

Additionally, 3 studies investigated different types of exercises on motor learning. Thomas et al.3434. Thomas R, Flindtgaard M, Skriver K, et al. Acute exercise and motor memory consolidation: Does exercise type play a role? Scand J Med Sci Sports. 2017;27(11):1523-32. doi:10.1111/sms.12791
https://doi.org/10.1111/sms.12791...
identified that a rest group demonstrated better motor performance of a visuomotor tracking task in the 1-h retention test than the 3 groups with different exercise types after practice; strength training, circuit training, and hockey. However, in the 1-day retention test, the exercise groups demonstrated offline gains (without difference among them) that were not found in the rest group. These findings revealed that the fatigue might harm the short-term retention test; however, in a 24 h retention test (without fatigue effects), it is possible to verify that the exercise improved the consolidation processes. In agreement with these findings, Lundbye-Jensen et al.3535. Lundbye-Jensen J, Skriver K, Nielsen JB, Roig M. Acute Exercise Improves Motor Memory Consolidation in Preadolescent Children. Front Hum Neurosci. 2017;11(April):1-10. doi:10.3389/fnhum.2017.00182
https://doi.org/10.3389/fnhum.2017.00182...
also showed that a non-traditional exercise (floorball) could enhance motor learning compared to running; besides, both groups were superior in the retention test than rest condition.

In a complementary perspective, Tomporowski & Pendleton2121. Tomporowski PD, Pendleton DM. Effects of the Timing of Acute Exercise and Movement Complexity on Young Adults’ Psychomotor Learning. J Sport Exerc Psychol. 2018;40(5):240-8. doi:10.1123/jsep.2017-0289
https://doi.org/10.1123/jsep.2017-0289...
demonstrated that performing an exercise after the practice based on a dance routine with a high complexity level (high complexity steps involved in the dance routine) improved more the consolidation processes than a simple dance routine. Though, when exercises (simple and complex) were performed before the practice, there was no enhancement effect on the retention of the pursuit-rotor task.

These studies demonstrated that the exercise priming effects might also be provided using non-traditional exercise types, with a level of evidence of 1A. It seems that mental engagement during the cardiovascular exercise session can be a factor that may influence the priming effect derived from cardiovascular exercise, with a level of evidence of 1B.

Intensity

Thomas, Johnsen, et al.4848. Thomas R, Johnsen LK, Geertsen SS, Christiansen L, Ritz C, Roig M et al. Acute Exercise and Motor Memory Consolidation: The Role of Exercise Intensity. Philp A, ed. PLoS One. 2016;11(7):e0159589. doi:10.1371/journal.pone.0159589
https://doi.org/10.1371/journal.pone.015...
showed that the group that performed High-Intensity Interval Training (HIIT) demonstrated better retention if compared to the group that performed the interval training with the intensity of 45% Wmax; yet, both groups were better in the retention test than the group that just had practice. Contrary, Opie & Semmler4040. Opie GM, Semmler JG. Acute Exercise at Different Intensities Influences Corticomotor Excitability and Performance of a Ballistic Thumb Training Task. Neuroscience. 2019;412:29-39. doi:10.1016/j.neuroscience.2019.05.049
https://doi.org/10.1016/j.neuroscience.2...
related that a low-intense running protocol induced better 24-h retention of a ballistic thumb abduction task than a high-intense condition; also, they reported that both exercise conditions (low and intense) induced better retention than just practice condition.

On the other hand, Baird et al.5858. Baird JF, Gaughan ME, Saffer HM, et al. The effect of energy-matched exercise intensity on brain-derived neurotrophic factor and motor learning. Neurobiol Learn Mem. 2018;156:33-44. doi:10.1016/j.nlm.2018.10.008
https://doi.org/10.1016/j.nlm.2018.10.00...
did not demonstrate a significant difference in motor performance and learning in the groups with interval training of high intensity 80% Wmax and low intensity 40 Wmax with the energy expenditure matched between them. In this case, this finding allows us to suppose that the effect on motor performance and learning is not derived from the intensity, but it is energy-expenditure dependent, in other words, total work dependent.

Another two studies did not demonstrate significant differences between high and low intensities on motor performance and learning. Wanner et al.5555. Wanner P, Müller T, Cristini J, Pfeifer K, Steib S. Exercise Intensity Does not Modulate the Effect of Acute Exercise on Learning a Complex Whole-Body Task. Neuroscience. 2020;426:115-28. doi:10.1016/j.neuroscience.2019.11.027
https://doi.org/10.1016/j.neuroscience.2...
did not find a significant difference in the motor performance and learning of a balance task among the groups that had low-intensity (25% Wmax), moderate-intensity (45% Wmax), and high-intensity (90% Wmax) exercises before practice. Lorås et al.4242. Lorås H, Haga M, Sigmundsson H. Effect of a Single Bout of Acute Aerobic Exercise at Moderate-to-Vigorous Intensities on Motor Learning, Retention and Transfer. Sports. 2020;8(2):15. doi:10.3390/sports8020015
https://doi.org/10.3390/sports8020015...
did not demonstrate a significant difference in the learning of golf putting task between the groups with a cardiovascular exercise at either 50% to 75% of the age-predicted maximal heart rate.

These results did not support the idea that exercise priming is dependent on high-intensity cardiovascular exercise. Contrary, perhaps the critical aspect can be the total volume instead of intensity per se.

Volume

As demonstrated by Baird et al.5858. Baird JF, Gaughan ME, Saffer HM, et al. The effect of energy-matched exercise intensity on brain-derived neurotrophic factor and motor learning. Neurobiol Learn Mem. 2018;156:33-44. doi:10.1016/j.nlm.2018.10.008
https://doi.org/10.1016/j.nlm.2018.10.00...
, the volume or total work may be more important than intensity concerning cardiovascular exercise effects on motor learning. However, Angulo-Barroso et al.3939. Angulo-Barroso R, Ferrer-Uris B, Busquets A. Enhancing Children's Motor Memory Retention Through Acute Intense Exercise: Effects of Different Exercise Durations. Front Psychol. 2019;10:1-9. doi:10.3389/fpsyg.2019.02000
https://doi.org/10.3389/fpsyg.2019.02000...
demonstrated that a long-High Intense Interval Training (HIIT) (total 13 min) was not significantly different from a short-HIIT (total 5 min); moreover, both exercise groups were better than the rest group in the retention test. In this case, there is no consensus about the volume or total work effect of cardiovascular exercise on motor learning.

Given the heterogeneity of the exercise protocols used in the studies incorporated in this review and the lack of information about the exercise, it was impossible to assess the volume exercise effects on motor learning compared to the other studies.

Task characteristics

Continuous, serial, and discrete skills

Most studies that identified positive effects of the cardiovascular exercise on consolidation processes used continuous and temporal synchronization tasks21,21. Tomporowski PD, Pendleton DM. Effects of the Timing of Acute Exercise and Movement Complexity on Young Adults’ Psychomotor Learning. J Sport Exerc Psychol. 2018;40(5):240-8. doi:10.1123/jsep.2017-0289
https://doi.org/10.1123/jsep.2017-0289...
34,34. Thomas R, Flindtgaard M, Skriver K, et al. Acute exercise and motor memory consolidation: Does exercise type play a role? Scand J Med Sci Sports. 2017;27(11):1523-32. doi:10.1111/sms.12791
https://doi.org/10.1111/sms.12791...
35,35. Lundbye-Jensen J, Skriver K, Nielsen JB, Roig M. Acute Exercise Improves Motor Memory Consolidation in Preadolescent Children. Front Hum Neurosci. 2017;11(April):1-10. doi:10.3389/fnhum.2017.00182
https://doi.org/10.3389/fnhum.2017.00182...
37,37. Dal Maso F, Desormeau B, Boudrias M-H, Roig M. Acute cardiovascular exercise promotes functional changes in cortico-motor networks during the early stages of motor memory consolidation. Neuroimage. 2018;174:380-92. doi:10.1016/j.neuroimage.2018.03.029
https://doi.org/10.1016/j.neuroimage.201...
40,40. Opie GM, Semmler JG. Acute Exercise at Different Intensities Influences Corticomotor Excitability and Performance of a Ballistic Thumb Training Task. Neuroscience. 2019;412:29-39. doi:10.1016/j.neuroscience.2019.05.049
https://doi.org/10.1016/j.neuroscience.2...
41,41. Beck MM, Grandjean MU, Hartmand S, Spedden ME, Christiansen L, Roig, M et al. Acute Exercise Protects Newly Formed MOTOR Memories Against rTMS-induced Interference Targeting Primary Motor Cortex. Neuroscience. 2020; 436: 110-21. doi:10.1016/j.neuroscience.2020.04.016
https://doi.org/10.1016/j.neuroscience.2...
4343. Roig M, Skriver K, Lundbye-Jensen J, Kiens B, Nielsen JB. A Single Bout of Exercise Improves Motor Memory. Sinigaglia C, ed. PLoS One. 2012;7(9):e44594. doi:10.1371/journal.pone.0044594
https://doi.org/10.1371/journal.pone.004...
44. Mang CS, Snow NJ, Campbell KL, Ross CJD, Boyd LA. A single bout of high-intensity aerobic exercise facilitates response to paired associative stimulation and promotes sequence-specific implicit motor learning. J Appl Physiol. 2014;117(11):1325-36. doi:10.1152/japplphysiol.00498.2014
https://doi.org/10.1152/japplphysiol.004...
-45,45. Skriver K, Roig M, Lundbye-Jensen J, Pingel J, Helge JW, Kiens B, et al. Acute exercise improves motor memory: Exploring potential biomarkers. Neurobiol Learn Mem. 2014;116:46-58. doi:10.1016/j.nlm.2014.08.004
https://doi.org/10.1016/j.nlm.2014.08.00...
47,47. Thomas R, Beck MM, Lind RR, Korsgaard Johnsen L, Geertsen SS, Christiansen L et al. Acute Exercise and Motor Memory Consolidation: The Role of Exercise Timing. Neural Plast. 2016;2016:1-11. doi:10.1155/2016/6205452
https://doi.org/10.1155/2016/6205452...
48,48. Thomas R, Johnsen LK, Geertsen SS, Christiansen L, Ritz C, Roig M et al. Acute Exercise and Motor Memory Consolidation: The Role of Exercise Intensity. Philp A, ed. PLoS One. 2016;11(7):e0159589. doi:10.1371/journal.pone.0159589
https://doi.org/10.1371/journal.pone.015...
5050. Lauber B, Franke S, Taube W, Gollhofer A. The effects of a single bout of exercise on motor memory interference in the trained and untrained hemisphere. Neuroscience. 2017;347:57-64. doi:10.1016/j.neuroscience.2017.01.048
https://doi.org/10.1016/j.neuroscience.2...
. Nevertheless, most studies that used serial tasks did not demonstrate effects from cardiovascular exercise on the motor memory consolidation20,20. Statton MA, Encarnacion M, Celnik P, Bastian AJ. A Single Bout of Moderate Aerobic Exercise Improves Motor Skill Acquisition. Gribble PL, ed. PLoS One. 2015;10(10):e0141393. doi:10.1371/journal.pone.0141393
https://doi.org/10.1371/journal.pone.014...
51,51. Jo JS, Chen J, Riechman S, Roig M, Wright DL. The protective effects of acute cardiovascular exercise on the interference of procedural memory. Psychol Res. 2019;83(7):1543-55. doi:10.1007/s00426-018-1005-8
https://doi.org/10.1007/s00426-018-1005-...
52,52. Ostadan F, Centeno C, Daloze J-F, Frenn M, Lundbye-Jensen J, Roig M. Changes in corticospinal excitability during consolidation predict acute exercise-induced off-line gains in procedural memory. Neurobiol Learn Mem. 2016;136:196-203. doi:10.1016/j.nlm.2016.10.009
https://doi.org/10.1016/j.nlm.2016.10.00...
54,54. Stranda H, Haga M, Sigmundsson H, Lorås H. The Effect of Aerobic Exercise on Speed and Accuracy Task Components in Motor Learning. Sports. 2019;7(3):54. doi:10.3390/sports7030054
https://doi.org/10.3390/sports7030054...
5656. Chartrand G, Kaneva P, Kolozsvari N, Li C, Petrucci AM, Mutter AF et al. The effects of acute aerobic exercise on the acquisition and retention of laparoscopic skills. Surg Endosc. 2015;29(2):474-80. doi:10.1007/s00464-014-3691-7
https://doi.org/10.1007/s00464-014-3691-...
57. Ferrer-Uris B, Busquets A, Lopez-Alonso V, Fernandez-del-Olmo M, Angulo-Barroso R. Enhancing consolidation of a rotational visuomotor adaptation task through acute exercise. PLoS One. 2017;12(4):e0175296. doi:10.1371/journal.pone.0175296
https://doi.org/10.1371/journal.pone.017...
-5858. Baird JF, Gaughan ME, Saffer HM, et al. The effect of energy-matched exercise intensity on brain-derived neurotrophic factor and motor learning. Neurobiol Learn Mem. 2018;156:33-44. doi:10.1016/j.nlm.2018.10.008
https://doi.org/10.1016/j.nlm.2018.10.00...
, or just demonstrated effect on relearning6060. Mang CS, Snow NJ, Wadden KP, Campbell KL, Boyd LA. High-Intensity Aerobic Exercise Enhances Motor Memory Retrieval. Med Sci Sport Exerc. 2016;48(12):2477-2486. doi:10.1249/MSS.0000000000001040
https://doi.org/10.1249/MSS.000000000000...
.

In this case, these findings revealed that cardiovascular exercise priming effects on motor learning are superior in continuous and temporal synchronization tasks than serial tasks. This evidence has a level of 1A.

Regarding discrete skills, only Lorås et al.4242. Lorås H, Haga M, Sigmundsson H. Effect of a Single Bout of Acute Aerobic Exercise at Moderate-to-Vigorous Intensities on Motor Learning, Retention and Transfer. Sports. 2020;8(2):15. doi:10.3390/sports8020015
https://doi.org/10.3390/sports8020015...
investigated the effect of different cardiovascular exercise intensities in golf putting task learning. However, this study can not infer the cardiovascular exercise effect; there was no control group (rest condition). It is necessary to investigate more discrete skills to create reliable conclusions for this motor skill type.

Simple and complex tasks

Most studies that were incorporated in this review used simple perceptual-motor laboratory skills. Among them were used visuomotor accuracy-tracking task32,32. Snow NJ, Mang CS, Roig M, McDonnell MN, Campbell KL, Boyd LA. The effect of an acute bout of moderate-intensity aerobic exercise on motor learning of a continuous tracking task. PLoS One. 2016;11(2):1-16. doi:10.1371/journal.pone.0150039
https://doi.org/10.1371/journal.pone.015...
34,34. Thomas R, Flindtgaard M, Skriver K, et al. Acute exercise and motor memory consolidation: Does exercise type play a role? Scand J Med Sci Sports. 2017;27(11):1523-32. doi:10.1111/sms.12791
https://doi.org/10.1111/sms.12791...
35,35. Lundbye-Jensen J, Skriver K, Nielsen JB, Roig M. Acute Exercise Improves Motor Memory Consolidation in Preadolescent Children. Front Hum Neurosci. 2017;11(April):1-10. doi:10.3389/fnhum.2017.00182
https://doi.org/10.3389/fnhum.2017.00182...
37,37. Dal Maso F, Desormeau B, Boudrias M-H, Roig M. Acute cardiovascular exercise promotes functional changes in cortico-motor networks during the early stages of motor memory consolidation. Neuroimage. 2018;174:380-92. doi:10.1016/j.neuroimage.2018.03.029
https://doi.org/10.1016/j.neuroimage.201...
41,41. Beck MM, Grandjean MU, Hartmand S, Spedden ME, Christiansen L, Roig, M et al. Acute Exercise Protects Newly Formed MOTOR Memories Against rTMS-induced Interference Targeting Primary Motor Cortex. Neuroscience. 2020; 436: 110-21. doi:10.1016/j.neuroscience.2020.04.016
https://doi.org/10.1016/j.neuroscience.2...
4343. Roig M, Skriver K, Lundbye-Jensen J, Kiens B, Nielsen JB. A Single Bout of Exercise Improves Motor Memory. Sinigaglia C, ed. PLoS One. 2012;7(9):e44594. doi:10.1371/journal.pone.0044594
https://doi.org/10.1371/journal.pone.004...
44. Mang CS, Snow NJ, Campbell KL, Ross CJD, Boyd LA. A single bout of high-intensity aerobic exercise facilitates response to paired associative stimulation and promotes sequence-specific implicit motor learning. J Appl Physiol. 2014;117(11):1325-36. doi:10.1152/japplphysiol.00498.2014
https://doi.org/10.1152/japplphysiol.004...
-45,45. Skriver K, Roig M, Lundbye-Jensen J, Pingel J, Helge JW, Kiens B, et al. Acute exercise improves motor memory: Exploring potential biomarkers. Neurobiol Learn Mem. 2014;116:46-58. doi:10.1016/j.nlm.2014.08.004
https://doi.org/10.1016/j.nlm.2014.08.00...
47,47. Thomas R, Beck MM, Lind RR, Korsgaard Johnsen L, Geertsen SS, Christiansen L et al. Acute Exercise and Motor Memory Consolidation: The Role of Exercise Timing. Neural Plast. 2016;2016:1-11. doi:10.1155/2016/6205452
https://doi.org/10.1155/2016/6205452...
48,48. Thomas R, Johnsen LK, Geertsen SS, Christiansen L, Ritz C, Roig M et al. Acute Exercise and Motor Memory Consolidation: The Role of Exercise Intensity. Philp A, ed. PLoS One. 2016;11(7):e0159589. doi:10.1371/journal.pone.0159589
https://doi.org/10.1371/journal.pone.015...
5050. Lauber B, Franke S, Taube W, Gollhofer A. The effects of a single bout of exercise on motor memory interference in the trained and untrained hemisphere. Neuroscience. 2017;347:57-64. doi:10.1016/j.neuroscience.2017.01.048
https://doi.org/10.1016/j.neuroscience.2...
, sequential visual isometric pinch task20,20. Statton MA, Encarnacion M, Celnik P, Bastian AJ. A Single Bout of Moderate Aerobic Exercise Improves Motor Skill Acquisition. Gribble PL, ed. PLoS One. 2015;10(10):e0141393. doi:10.1371/journal.pone.0141393
https://doi.org/10.1371/journal.pone.014...
3636. Stavrinos EL, Coxon JP. High-intensity interval exercise promotes motor cortex disinhibition and early motor skill consolidation. J Cogn Neurosci. 2017;29(4):593-604. doi:10.1162/jocn_a_01078
https://doi.org/10.1162/jocn_a_01078...
, motor sequence task4646. Rhee J, Chen J, Riechman SM, Handa A, Bhatia S, Wright DL. An acute bout of aerobic exercise can protect immediate offline motor sequence gains. Psychol Res. 2016;80(4):518-31. doi:10.1007/s00426-015-0682-9
https://doi.org/10.1007/s00426-015-0682-...
, serial targeting task6060. Mang CS, Snow NJ, Wadden KP, Campbell KL, Boyd LA. High-Intensity Aerobic Exercise Enhances Motor Memory Retrieval. Med Sci Sport Exerc. 2016;48(12):2477-2486. doi:10.1249/MSS.0000000000001040
https://doi.org/10.1249/MSS.000000000000...
, rotational visuomotor adaptation task33,33. Neva JL, Ma JA, Orsholits D, Boisgontier MP, Boyd LA. The effects of acute exercise on visuomotor adaptation, learning, and inter-limb transfer. Exp Brain Res. 2019;237:1109-27. doi:10.1007/s00221-019-05491-5
https://doi.org/10.1007/s00221-019-05491...
38,38. Ferrer-Uris B, Busquets A, Angulo-Barroso R. Adaptation and Retention of a Perceptual-Motor Task in Children: Effects of a Single Bout of Intense Endurance Exercise. J Sport Exerc Psychol. 2018;40(1):1-9. doi:10.1123/jsep.2017-0044
https://doi.org/10.1123/jsep.2017-0044...
5757. Ferrer-Uris B, Busquets A, Lopez-Alonso V, Fernandez-del-Olmo M, Angulo-Barroso R. Enhancing consolidation of a rotational visuomotor adaptation task through acute exercise. PLoS One. 2017;12(4):e0175296. doi:10.1371/journal.pone.0175296
https://doi.org/10.1371/journal.pone.017...
, serial reaction time task5252. Ostadan F, Centeno C, Daloze J-F, Frenn M, Lundbye-Jensen J, Roig M. Changes in corticospinal excitability during consolidation predict acute exercise-induced off-line gains in procedural memory. Neurobiol Learn Mem. 2016;136:196-203. doi:10.1016/j.nlm.2016.10.009
https://doi.org/10.1016/j.nlm.2016.10.00...
and keyboard typing task5454. Stranda H, Haga M, Sigmundsson H, Lorås H. The Effect of Aerobic Exercise on Speed and Accuracy Task Components in Motor Learning. Sports. 2019;7(3):54. doi:10.3390/sports7030054
https://doi.org/10.3390/sports7030054...
.

Only 5 studies incorporated complex motor skills in their experimental design, demonstrating the necessity of the subsequent studies in this area to incorporate it. As mentioned before, Wanner et al.5555. Wanner P, Müller T, Cristini J, Pfeifer K, Steib S. Exercise Intensity Does not Modulate the Effect of Acute Exercise on Learning a Complex Whole-Body Task. Neuroscience. 2020;426:115-28. doi:10.1016/j.neuroscience.2019.11.027
https://doi.org/10.1016/j.neuroscience.2...
and Lorås et al.4242. Lorås H, Haga M, Sigmundsson H. Effect of a Single Bout of Acute Aerobic Exercise at Moderate-to-Vigorous Intensities on Motor Learning, Retention and Transfer. Sports. 2020;8(2):15. doi:10.3390/sports8020015
https://doi.org/10.3390/sports8020015...
investigated the intensity effects of cardiovascular exercise on motor learning. Both studies demonstrated that the intensity did not impact the learning of balance and golf putting tasks, respectively.

Helm et al.5353. Helm EE, Matt KS, Kirschner KF, Pohlig RT, Kohl D, Reisman DS. The influence of high-intensity exercise and the Val66Met polymorphism on circulating BDNF and locomotor learning. Neurobiol Learn Mem. 2017;144:77-85. doi:10.1016/j.nlm.2017.06.003
https://doi.org/10.1016/j.nlm.2017.06.00...
and Charalambous et al.5959. Charalambous CC, French MA, Morton SM, Reisman DS. A single high-intensity exercise bout during early consolidation does not influence retention or relearning of sensorimotor locomotor long-term memories. Exp Brain Res. 2019;237(11):2799-810. doi:10.1007/s00221-019-05635-7
https://doi.org/10.1007/s00221-019-05635...
investigated cardiovascular exercise effects on locomotor skill learning. Both studies demonstrated that cardiovascular exercise did not benefit the learning of a locomotor skill; this evidence has level 1B. These studies used protocols of exercise mutually different. Helm et al.5353. Helm EE, Matt KS, Kirschner KF, Pohlig RT, Kohl D, Reisman DS. The influence of high-intensity exercise and the Val66Met polymorphism on circulating BDNF and locomotor learning. Neurobiol Learn Mem. 2017;144:77-85. doi:10.1016/j.nlm.2017.06.003
https://doi.org/10.1016/j.nlm.2017.06.00...
proposed exercise using HIIT protocol in an upper-body ergometer before the practice (to avoid fatigue effect on motor effector related to the motor performance). Whereas Charalambous et al.5959. Charalambous CC, French MA, Morton SM, Reisman DS. A single high-intensity exercise bout during early consolidation does not influence retention or relearning of sensorimotor locomotor long-term memories. Exp Brain Res. 2019;237(11):2799-810. doi:10.1007/s00221-019-05635-7
https://doi.org/10.1007/s00221-019-05635...
promoted exercise after motor practice using a continuous protocol in a total body exerciser ergometer. Both studies corroborated with the no effect of cardiovascular exercise on motor learning even with different exercise protocols, reinforcing the non-susceptibility of locomotor skill to exercise priming.

Finally, Chartrand et al.5656. Chartrand G, Kaneva P, Kolozsvari N, Li C, Petrucci AM, Mutter AF et al. The effects of acute aerobic exercise on the acquisition and retention of laparoscopic skills. Surg Endosc. 2015;29(2):474-80. doi:10.1007/s00464-014-3691-7
https://doi.org/10.1007/s00464-014-3691-...
identified that a moderate-intense continuous running session performed after the practice did not influence the learning of laparoscopic surgery simulator tasks. However, in this study, the participants practiced 3 tasks simultaneously, promoting an interfering effect.

Retroactive interference

The studies demonstrated that a cardiovascular exercise bout exerts a protective effect on retroactive interference41,41. Beck MM, Grandjean MU, Hartmand S, Spedden ME, Christiansen L, Roig, M et al. Acute Exercise Protects Newly Formed MOTOR Memories Against rTMS-induced Interference Targeting Primary Motor Cortex. Neuroscience. 2020; 436: 110-21. doi:10.1016/j.neuroscience.2020.04.016
https://doi.org/10.1016/j.neuroscience.2...
46,46. Rhee J, Chen J, Riechman SM, Handa A, Bhatia S, Wright DL. An acute bout of aerobic exercise can protect immediate offline motor sequence gains. Psychol Res. 2016;80(4):518-31. doi:10.1007/s00426-015-0682-9
https://doi.org/10.1007/s00426-015-0682-...
5050. Lauber B, Franke S, Taube W, Gollhofer A. The effects of a single bout of exercise on motor memory interference in the trained and untrained hemisphere. Neuroscience. 2017;347:57-64. doi:10.1016/j.neuroscience.2017.01.048
https://doi.org/10.1016/j.neuroscience.2...
. However, when the retention test was performed on the same day of the practice, there was no protective effect against retroactive interference, suggesting that the cardiovascular exercise effects are sleep-dependent in this case5151. Jo JS, Chen J, Riechman S, Roig M, Wright DL. The protective effects of acute cardiovascular exercise on the interference of procedural memory. Psychol Res. 2019;83(7):1543-55. doi:10.1007/s00426-018-1005-8
https://doi.org/10.1007/s00426-018-1005-...
. It was also demonstrated that the protective effect of cardiovascular exercise is more evident when the cardiovascular exercise is performed in a temporal close to the task to be prioritized4646. Rhee J, Chen J, Riechman SM, Handa A, Bhatia S, Wright DL. An acute bout of aerobic exercise can protect immediate offline motor sequence gains. Psychol Res. 2016;80(4):518-31. doi:10.1007/s00426-015-0682-9
https://doi.org/10.1007/s00426-015-0682-...
. The evidence that cardiovascular exercise induces a protective effect against retroactive interference has a level 1A.

Adaptation

There was no effect of the cardiovascular exercise on motor adaptation across the practice in all of them. It was verified in young adults39,39. Angulo-Barroso R, Ferrer-Uris B, Busquets A. Enhancing Children's Motor Memory Retention Through Acute Intense Exercise: Effects of Different Exercise Durations. Front Psychol. 2019;10:1-9. doi:10.3389/fpsyg.2019.02000
https://doi.org/10.3389/fpsyg.2019.02000...
5757. Ferrer-Uris B, Busquets A, Lopez-Alonso V, Fernandez-del-Olmo M, Angulo-Barroso R. Enhancing consolidation of a rotational visuomotor adaptation task through acute exercise. PLoS One. 2017;12(4):e0175296. doi:10.1371/journal.pone.0175296
https://doi.org/10.1371/journal.pone.017...
and children3838. Ferrer-Uris B, Busquets A, Angulo-Barroso R. Adaptation and Retention of a Perceptual-Motor Task in Children: Effects of a Single Bout of Intense Endurance Exercise. J Sport Exerc Psychol. 2018;40(1):1-9. doi:10.1123/jsep.2017-0044
https://doi.org/10.1123/jsep.2017-0044...
. Also, Angulo-Barroso et al.3939. Angulo-Barroso R, Ferrer-Uris B, Busquets A. Enhancing Children's Motor Memory Retention Through Acute Intense Exercise: Effects of Different Exercise Durations. Front Psychol. 2019;10:1-9. doi:10.3389/fpsyg.2019.02000
https://doi.org/10.3389/fpsyg.2019.02000...
verified that increasing the exercise duration (volume) did not impact the adaptation during motor performance. There is evidence of 1A that cardiovascular exercise did not influence the adaptation during motor performance.

Implicit x explicit

Some insights maybe support the hypothesis that cardiovascular exercise would be an attractive strategy to improve implicit motor learning. Mang et al.5757. Ferrer-Uris B, Busquets A, Lopez-Alonso V, Fernandez-del-Olmo M, Angulo-Barroso R. Enhancing consolidation of a rotational visuomotor adaptation task through acute exercise. PLoS One. 2017;12(4):e0175296. doi:10.1371/journal.pone.0175296
https://doi.org/10.1371/journal.pone.017...
demonstrated in a serial motor sequence task that the cardiovascular exercise improved motor performance related to the implicit representation, which did not occur in the pseudorandom sequences.

Besides, Poolton et al.2929. Poolton JM, Masters RSW, Maxwell JP. Passing thoughts on the evolutionary stability of implicit motor behaviour: Performance retention under physiological fatigue. Conscious Cogn. 2007;16(2):456-68. doi:10.1016/j.concog.2006.06.008
https://doi.org/10.1016/j.concog.2006.06...
and Masters et al.3030. Masters RSW, Poolton JM, Maxwell JP. Stable implicit motor processes despite aerobic locomotor fatigue. Conscious Cogn. 2008;17(1):335-8. doi:10.1016/j.concog.2007.03.009
https://doi.org/10.1016/j.concog.2007.03...
demonstrated that a high fatigue level impacts the motor learning process based on explicit mechanisms. Both studies demonstrated that implicit learning is resistant to the high level of effort and fatigue provided by cardiovascular (VO2 max fatigue test) and anaerobic (Wingate anaerobic test peak power).

Then, the priming effects from the cardiovascular exercise are related to the type of motor learning process that was engaged during the skill acquisition. The implicit motor learning is more resilient and stable under stress and fatigue effects, suggesting that the exercise can induce better motor consolidation of implicit motor memories than explicit motor memories29,29. Poolton JM, Masters RSW, Maxwell JP. Passing thoughts on the evolutionary stability of implicit motor behaviour: Performance retention under physiological fatigue. Conscious Cogn. 2007;16(2):456-68. doi:10.1016/j.concog.2006.06.008
https://doi.org/10.1016/j.concog.2006.06...
3030. Masters RSW, Poolton JM, Maxwell JP. Stable implicit motor processes despite aerobic locomotor fatigue. Conscious Cogn. 2008;17(1):335-8. doi:10.1016/j.concog.2007.03.009
https://doi.org/10.1016/j.concog.2007.03...
.

Methodological considerations

Some studies used cross-over designs in their experimental setup32,32. Snow NJ, Mang CS, Roig M, McDonnell MN, Campbell KL, Boyd LA. The effect of an acute bout of moderate-intensity aerobic exercise on motor learning of a continuous tracking task. PLoS One. 2016;11(2):1-16. doi:10.1371/journal.pone.0150039
https://doi.org/10.1371/journal.pone.015...
33,33. Neva JL, Ma JA, Orsholits D, Boisgontier MP, Boyd LA. The effects of acute exercise on visuomotor adaptation, learning, and inter-limb transfer. Exp Brain Res. 2019;237:1109-27. doi:10.1007/s00221-019-05491-5
https://doi.org/10.1007/s00221-019-05491...
40,40. Opie GM, Semmler JG. Acute Exercise at Different Intensities Influences Corticomotor Excitability and Performance of a Ballistic Thumb Training Task. Neuroscience. 2019;412:29-39. doi:10.1016/j.neuroscience.2019.05.049
https://doi.org/10.1016/j.neuroscience.2...
44,44. Mang CS, Snow NJ, Campbell KL, Ross CJD, Boyd LA. A single bout of high-intensity aerobic exercise facilitates response to paired associative stimulation and promotes sequence-specific implicit motor learning. J Appl Physiol. 2014;117(11):1325-36. doi:10.1152/japplphysiol.00498.2014
https://doi.org/10.1152/japplphysiol.004...
6060. Mang CS, Snow NJ, Wadden KP, Campbell KL, Boyd LA. High-Intensity Aerobic Exercise Enhances Motor Memory Retrieval. Med Sci Sport Exerc. 2016;48(12):2477-2486. doi:10.1249/MSS.0000000000001040
https://doi.org/10.1249/MSS.000000000000...
. Cross-over designs induce significant limitations in the inference about motor learning. The participants may transfer the learning from the first phase to the second phase of the experiment, promoting fewer motor improvements in the second phase, which may induce misconceptions. The cross-over studies adopted some strategies to avoid problems with that, such as 1 - to allocate the participants by a random process such that half of the participants completed the rest condition first and the other half the cardiovascular exercise condition. 2 - to promote washout of at least two weeks between the phases of the study. 3 - to provide some modification in the task between the first and second study phases. However, even with all these methodological details, this experimental design must be avoided in further studies to ensure a reliable interpretation of the motor learning phenomenon.

Study limitations

Motor learning literature has not had any methodological quality assessment tool to evaluate motor learning studies. In this way, this review used health research science tools in an adapted approach that can be verified in the Supplementary Material. This methodological assessment was based on a previous systematic review of the motor learning area. The development of instruments for assessing the methodological quality of motor learning studies may have particular implications for further systematic reviews in this area. It may be useful to guide the subsequent studies in the motor learning field.

Conclusion

This systematic review of 40 studies provides a synopsis of evidence that indicates the benefit of the acute effects of cardiovascular exercise on motor performance and learning. Until now, the evidence suggests that exercise-induced fatigue does not impair motor learning, mainly when the exercise does not engage the same motor effector involved in the performance of the motor task.

The studies also demonstrated that the effects of cardiovascular exercise on motor learning are more evident when the exercise is performed in temporal proximity of the practice; besides, depending on the order between exercise and practice, the priming effects perhaps can impact the motor learning process differently.

There is evidence that different types of exercise may induce positive effects on motor learning. However, the exercise that involves a higher amount of muscle mass may stimulate priming effects with more regularity. Given that cardiovascular exercise that does not engage larger muscle groups during the performance (e.g., upper body ergometer) may be limited by local/neural fatigue, consequently, it does not stimulate in a high magnitude the metabolic/ cardiovascular systems, which may decrease the priming effects.

The exercise intensity was not more determinant than the total work for motor performance and learning enhancements. So, the importance attributed to high-intensity protocols needs to be revisited. In this case, the moderate-intensity protocols are equally effective as high-intensity protocols if the total work is pared between them.

Regarding task characteristics, the exercise priming on motor learning is more evident for continuous tasks than serial tasks. The cardiovascular exercise has an interesting effect on avoiding retroactive interference when allocated between the practice of 2 different motor skills; probably, this effect is sleep-dependent and occurs when the cardiovascular exercise is performed immediately after the practice of the first motor skill. Finally, the current evidence suggests that cardiovascular exercise does not influence adaptation. It was identified with different exercise protocols and the timing (before or after practice).

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Associate Editor: Angelina Zanesco, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Instituto de Biociências, Departamento de Educação Física, Rio Claro, SP, Brasil.

Publication Dates

  • Publication in this collection
    18 Mar 2022
  • Date of issue
    2022

History

  • Received
    15 Mar 2021
  • Accepted
    11 May 2021
Universidade Estadual Paulista Universidade Estadual Paulista, Av. 24-A, 1515, 13506-900 Rio Claro, SP/Brasil, Tel.: (55 19) 3526-4330 - Rio Claro - SP - Brazil
E-mail: motriz.rc@unesp.br