Studying brain activity in sports performance: Contributions and issues.

Understanding the interactions between brain activity and behavior comprehensively in achieving optimal exercise performance in sports is still lacking. The existent research in this area has been limited by the constraints of sports environments and the robustness of the most suitable non-invasive functional neuroimaging methods (electroencephalography, EEG and functional near-infrared spectroscopy, fNIRS) to motion artifacts and noise. However, recent advances in brain mapping technology should improve the capabilities of the future brain imaging devices to assess and monitor the level of adaptive cognitive-motor performance during exercise in sports environments. The purpose of this position manuscript is to discuss the contributions and issues in behavioral neuroscience related to brain activity measured during exercise and in various sports. A first part aims to give an overview of EEG and fNIRS neuroimaging methods assessing electrophysiological activity and hemodynamic responses of the acute and chronic relation of physical exercise on the human brain. Then, methodological issues, such as the reliability of brain data during physical exertion, key limitations and possible prospects of fNIRS and EEG methods are provided. While the use of such methods in sports environments remains scarce and limited to controlled cycling task, new generation of wearable, whole-scalp EEG and fNIRS technologies could open up a range of new applications in sports sciences for providing neuroimaging-based biomarkers (hemodynamic and/or neural electrical signals) to various types of exercise and innovative training.

[1]  Li Min Li,et al.  Brain stimulation modulates the autonomic nervous system, rating of perceived exertion and performance during maximal exercise , 2013, British Journal of Sports Medicine.

[2]  David I. Donaldson,et al.  Neuroscience and Biobehavioral Reviews Making the Case for Mobile Cognition: Eeg and Sports Performance , 2022 .

[3]  A. Neubauer,et al.  Intelligence and neural efficiency , 2009, Neuroscience & Biobehavioral Reviews.

[4]  V. Brümmer,et al.  Changes in brain cortical activity measured by EEG are related to individual exercise preferences , 2009, Physiology & Behavior.

[5]  Wolfgang Taube,et al.  Effects of age on the soccer-specific cognitive-motor performance of elite young soccer players: Comparison between objective measurements and coaches’ evaluation , 2017, PloS one.

[6]  Ichiro Miyai,et al.  Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: an optical imaging study , 2004, NeuroImage.

[7]  V. Brümmer,et al.  Primary motor cortex activity is elevated with incremental exercise intensity , 2011, Neuroscience.

[8]  Lan-Ya Chuang,et al.  The differences in frontal midline theta power between successful and unsuccessful basketball free throws of elite basketball players. , 2013, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[9]  João Ricardo Sato,et al.  fNIRS Optodes’ Location Decider (fOLD): a toolbox for probe arrangement guided by brain regions-of-interest , 2018, Scientific Reports.

[10]  Lucas R. Trambaiolli,et al.  Imaging Brain Function with Functional Near-Infrared Spectroscopy in Unconstrained Environments , 2017, Front. Hum. Neurosci..

[11]  L. Engels,et al.  Factors influencing the spatial precision of electromagnetic tracking systems used for MEG/EEG source imaging , 2010, Neurophysiologie Clinique/Clinical Neurophysiology.

[12]  Kevin K. McCully,et al.  Effects of incremental exercise on cerebral oxygenation measured by near-infrared spectroscopy: A systematic review , 2010, Progress in Neurobiology.

[13]  Franck Multon,et al.  Using Virtual Reality to Analyze Sports Performance , 2010, IEEE Computer Graphics and Applications.

[14]  Jeffrey W. Barker,et al.  Correction of motion artifacts and serial correlations for real-time functional near-infrared spectroscopy , 2016, Neurophotonics.

[15]  R. Meeusen,et al.  The Effects of Mental Fatigue on Physical Performance: A Systematic Review , 2017, Sports Medicine.

[16]  T. Alvarez,et al.  Altered cortical activation and connectivity patterns for visual attention processing in young adults post‐traumatic brain injury: A functional near infrared spectroscopy study , 2018, CNS neuroscience & therapeutics.

[17]  Anna Wexler Recurrent themes in the history of the home use of electrical stimulation: Transcranial direct current stimulation (tDCS) and the medical battery (1870–1920) , 2017, Brain Stimulation.

[18]  P. Ekkekakis Pleasure and displeasure from the body: Perspectives from exercise , 2003, Cognition & emotion.

[19]  K. R. Ridderinkhof,et al.  Impaired cognitive control and reduced cingulate activity during mental fatigue. , 2005, Brain research. Cognitive brain research.

[20]  Marc Jubeau,et al.  Mental fatigue alters the speed and the accuracy of the ball in table tennis , 2018, Journal of sports sciences.

[21]  H. Jasper,et al.  The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[22]  Bradley D. Hatfield,et al.  Neuro-cognitive activity during a self-paced visuospatial task: comparative EEG profiles in marksmen and novice shooters , 2000, Biological Psychology.

[23]  Usman Naeem,et al.  Neural Correlates of Single- and Dual-Task Walking in the Real World , 2017, Front. Hum. Neurosci..

[24]  L. Wichert-Ana,et al.  Neurovascular coupling and functional neuroimaging in epilepsy , 2009 .

[25]  R. Eston,et al.  Prefrontal Cortex Haemodynamics and Affective Responses during Exercise: A Multi-Channel Near Infrared Spectroscopy Study , 2014, PloS one.

[26]  A. R. Anwar,et al.  Multimodal integration of fNIRS, fMRI and EEG neuroimaging , 2013, Clinical Neurophysiology.

[27]  Raja Parasuraman,et al.  Wearable functional near infrared spectroscopy (fNIRS) and transcranial direct current stimulation (tDCS): expanding vistas for neurocognitive augmentation , 2015, Front. Syst. Neurosci..

[28]  Arne Dietrich,et al.  Transient hypofrontality as a mechanism for the psychological effects of exercise , 2006, Psychiatry Research.

[29]  Kelvin S. Oie,et al.  Cognition in action: imaging brain/body dynamics in mobile humans , 2011, Reviews in the neurosciences.

[30]  A. Darzi,et al.  Quality control and assurance in functional near infrared spectroscopy (fNIRS) experimentation , 2010, Physics in medicine and biology.

[31]  A. R. Anwar,et al.  Effective Connectivity of Cortical Sensorimotor Networks During Finger Movement Tasks: A Simultaneous fNIRS, fMRI, EEG Study , 2016, Brain Topography.

[32]  Thomas Gronwald,et al.  Effects of high vs. low cadence training on cyclists' brain cortical activity during exercise. , 2016, Journal of science and medicine in sport.

[33]  Sotaro Shimada,et al.  Simultaneous measurement of electroencephalography and near-infrared spectroscopy during voluntary motor preparation , 2015, Scientific Reports.

[34]  Silvia Comani,et al.  Neural Markers of Performance States in an Olympic Athlete: An EEG Case Study in Air-Pistol Shooting. , 2016, Journal of sports science & medicine.

[35]  Heinz Liesen,et al.  Cortical activity of skilled performance in a complex sports related motor task , 2008, European Journal of Applied Physiology.

[36]  Anna L. Gert,et al.  Kinesthetic and vestibular information modulate alpha activity during spatial navigation: a mobile EEG study , 2014, Front. Hum. Neurosci..

[37]  D. Rouffet,et al.  Cortical current density oscillations in the motor cortex are correlated with muscular activity during pedaling exercise , 2013, Neuroscience.

[38]  Toru Yamada,et al.  Removal of motion artifacts originating from optode fluctuations during functional near-infrared spectroscopy measurements. , 2015, Biomedical optics express.

[39]  M. Iacoboni,et al.  Golf putt outcomes are predicted by sensorimotor cerebral EEG rhythms , 2008, The Journal of physiology.

[40]  David A. Boas,et al.  Validating atlas-guided DOT: A comparison of diffuse optical tomography informed by atlas and subject-specific anatomies , 2012, NeuroImage.

[41]  Niall Holmes,et al.  Moving magnetoencephalography towards real-world applications with a wearable system , 2018, Nature.

[42]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[43]  Tzyy-Ping Jung,et al.  Assessing the quality of steady-state visual-evoked potentials for moving humans using a mobile electroencephalogram headset , 2014, Front. Hum. Neurosci..

[44]  Arne Dietrich,et al.  The reticular-activating hypofrontality (RAH) model of acute exercise , 2011, Neuroscience & Biobehavioral Reviews.

[45]  Daniel P. Ferris,et al.  Removal of movement artifact from high-density EEG recorded during walking and running. , 2010, Journal of neurophysiology.

[46]  Mohamad Sawan,et al.  Multichannel wearable fNIRS‐EEG system for long‐term clinical monitoring , 2018, Human brain mapping.

[47]  Thomas Gronwald,et al.  The Athlete's Brain: Cross-Sectional Evidence for Neural Efficiency during Cycling Exercise , 2015, Neural plasticity.

[48]  T. Noakes,et al.  Fatigue is a Brain-Derived Emotion that Regulates the Exercise Behavior to Ensure the Protection of Whole Body Homeostasis , 2012, Front. Physio..

[49]  R. Parasuraman,et al.  Continuous monitoring of brain dynamics with functional near infrared spectroscopy as a tool for neuroergonomic research: empirical examples and a technological development , 2013, Front. Hum. Neurosci..

[50]  L. Sherlin,et al.  Developing a Performance Brain Training™ Approach for Baseball: A Process Analysis with Descriptive Data , 2013, Applied psychophysiology and biofeedback.

[51]  Stéphane Perrey,et al.  Non-invasive NIR spectroscopy of human brain function during exercise. , 2008, Methods.

[52]  L. Prichep,et al.  The Use of an Electrophysiological Brain Function Index in the Evaluation of Concussed Athletes , 2017, The Journal of head trauma rehabilitation.

[53]  Anthony D Bateson,et al.  Categorisation of Mobile EEG: A Researcher's Perspective , 2017, BioMed research international.

[54]  S. Ludyga,et al.  Four weeks of high cadence training alter brain cortical activity in cyclists , 2017, Journal of sports sciences.

[55]  Dirk Koester,et al.  Sensorimotor Rhythm Neurofeedback Enhances Golf Putting Performance. , 2015, Journal of sport & exercise psychology.

[56]  Jeanick Brisswalter,et al.  Saving mental effort to maintain physical effort: a shift of activity within the prefrontal cortex in anticipation of prolonged exercise , 2017, Cognitive, affective & behavioral neuroscience.

[57]  Roger M Enoka,et al.  The neurobiology of muscle fatigue: 15 years later. , 2007, Integrative and comparative biology.

[58]  Yumie Ono,et al.  fMRI Validation of fNIRS Measurements During a Naturalistic Task , 2015, Journal of visualized experiments : JoVE.

[59]  John J. Foxe,et al.  Oscillatory beta activity predicts response speed during a multisensory audiovisual reaction time task: a high-density electrical mapping study. , 2005, Cerebral cortex.

[60]  R. Pascual-Marqui,et al.  Fatigue‐induced increase in intracortical communication between mid/anterior insular and motor cortex during cycling exercise , 2011, The European journal of neuroscience.

[61]  Abraham Z. Snyder,et al.  A quantitative spatial comparison of high-density diffuse optical tomography and fMRI cortical mapping , 2012, NeuroImage.

[62]  Reiko Kawagoe,et al.  Influence of skin blood flow on near-infrared spectroscopy signals measured on the forehead during a verbal fluency task , 2011, NeuroImage.

[63]  Mingqiang Xiang,et al.  The effect of neurofeedback training for sport performance in athletes: A meta‐analysis , 2018 .

[64]  Swapan Mookerjee,et al.  Cerebral oxygenation declines at exercise intensities above the respiratory compensation threshold , 2007, Respiratory Physiology & Neurobiology.

[65]  M. Mintun,et al.  Brain work and brain imaging. , 2006, Annual review of neuroscience.

[66]  F. Marino,et al.  A role for the prefrontal cortex in exercise tolerance and termination. , 2016, Journal of applied physiology.

[67]  Martin Wolf,et al.  A review on continuous wave functional near-infrared spectroscopy and imaging instrumentation and methodology , 2014, NeuroImage.

[68]  P. Ragert,et al.  Hemodynamic Response Alterations in Sensorimotor Areas as a Function of Barbell Load Levels during Squatting: An fNIRS Study , 2017, Front. Hum. Neurosci..

[69]  Anmin Li,et al.  “Neural Efficiency” of Athletes’ Brain during Visuo-Spatial Task: An fMRI Study on Table Tennis Players , 2017, Front. Behav. Neurosci..

[70]  Sabrina Brigadoi,et al.  How short is short? Optimum source–detector distance for short-separation channels in functional near-infrared spectroscopy , 2015, Neurophotonics.

[71]  M. Banissy,et al.  Transcranial Direct Current Stimulation in Sports Training: Potential Approaches , 2013, Front. Hum. Neurosci..

[72]  M. Taubert,et al.  Cortical Brain Activity is Influenced by Cadence in Cyclists , 2013 .

[73]  Stéphane Perrey,et al.  Prefrontal cortex oxygenation and neuromuscular responses to exhaustive exercise. , 2007 .

[74]  I. Karanasiou Functional Brain Imaging Using Non-Invasive Non-Ionizing Methods: Towards Multimodal and Multiscale Imaging , 2012 .

[75]  S. Schneider,et al.  Activation patterns of different brain areas during incremental exercise measured by near-infrared spectroscopy , 2015, Experimental Brain Research.

[76]  Franck Multon,et al.  Virtual reality, a serious game for understanding performance and training players in sport , 2009 .

[77]  B. Schmit,et al.  EEG during pedaling: Evidence for cortical control of locomotor tasks , 2013, Clinical Neurophysiology.

[78]  Stéphane Perrey,et al.  NIRS for Measuring Cerebral Hemodynamic Responses During Exercise , 2012 .

[79]  Hellmuth Obrig,et al.  A wearable multi-channel fNIRS system for brain imaging in freely moving subjects , 2014, NeuroImage.

[80]  M. Arns,et al.  Golf performance enhancement and real-life neurofeedback training using personalized event-locked EEG profiles , 2008 .

[81]  A. Dietrich Mind on the run. , 2008, Methods.

[82]  Charles H Hillman,et al.  Neuroelectric measurement of cognition during aerobic exercise. , 2008, Methods.

[83]  F. E. Marino,et al.  Prefrontal and motor cortex EEG responses and their relationship to ventilatory thresholds during exhaustive incremental exercise , 2015, European Journal of Applied Physiology.

[84]  Ippeita Dan,et al.  Spatial registration for functional near-infrared spectroscopy: From channel position on the scalp to cortical location in individual and group analyses , 2014, NeuroImage.

[85]  Claudio Babiloni,et al.  Visuo‐attentional and sensorimotor alpha rhythms are related to visuo‐motor performance in athletes , 2009, Human brain mapping.

[86]  M. Iacoboni,et al.  “Neural efficiency” of experts’ brain during judgment of actions: A high-resolution EEG study in elite and amateur karate athletes , 2010, Behavioural Brain Research.

[87]  Guy A Dumont,et al.  Wavelet-based motion artifact removal for functional near-infrared spectroscopy , 2012, Physiological measurement.

[88]  Jacques Duysens,et al.  Cortical control of normal gait and precision stepping: An fNIRS study , 2014, NeuroImage.

[89]  Jose L. Contreras-Vidal,et al.  Simultaneous scalp electroencephalography (EEG), electromyography (EMG), and whole-body segmental inertial recording for multi-modal neural decoding. , 2013, Journal of visualized experiments : JoVE.

[90]  Vinzenz von Tscharner,et al.  Methodological aspects of EEG and body dynamics measurements during motion , 2014, Front. Hum. Neurosci..

[91]  Kouhyar Tavakolian,et al.  Preliminary results of residual deficits observed in athletes with concussion history: Combined EEG and cognitive study , 2016, 2016 38th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[92]  R. Saager,et al.  Direct characterization and removal of interfering absorption trends in two-layer turbid media. , 2005, Journal of the Optical Society of America. A, Optics, image science, and vision.

[93]  A. Coutts,et al.  Prediction: The Modern-Day Sport-Science and Sports-Medicine "Quest for the Holy Grail". , 2017, International journal of sports physiology and performance.

[94]  Maarten A. S. Boksem,et al.  Mental fatigue: Costs and benefits , 2008, Brain Research Reviews.

[95]  Thorsten,et al.  Electrocortical and Hemodynamic Changes within the Brain during Incremental Bicycle Exercise in Normoxia and Hypoxiam--A Combined EEG/NIRS Study , 2015 .

[96]  Marc Jubeau,et al.  Muscle, prefrontal, and motor cortex oxygenation profiles during prolonged fatiguing exercise. , 2013, Advances in experimental medicine and biology.

[97]  Jeremy C. Hebden,et al.  Functional imaging of the human brain using a modular, fibre-less, high-density diffuse optical tomography system , 2016, Biomedical optics express.

[98]  Trevor Thompson,et al.  EEG applications for sport and performance. , 2008, Methods.

[99]  V. Brümmer,et al.  Brain cortical activity is influenced by exercise mode and intensity. , 2011, Medicine and science in sports and exercise.

[100]  S. Perrey Brain activation associated with eccentric movement: A narrative review of the literature , 2018, European journal of sport science.

[101]  C. Hillman,et al.  Functional Neuroimaging in Exercise and Sport Sciences , 2012, Springer New York.

[102]  D. Benton,et al.  The supply of glucose to the brain and cognitive functioning , 1996, Journal of Biosocial Science.

[103]  Á. Pascual-Leone,et al.  Transcranial Direct Current Stimulation and Sports Performance , 2017, Front. Hum. Neurosci..