Modulation of cortical and subcortical brain areas at low and high exercise intensities

Introduction The brain plays a key role in the perceptual regulation of exercise, yet neuroimaging techniques have only demonstrated superficial brain areas responses during exercise, and little is known about the modulation of the deeper brain areas at different intensities. Objectives/methods Using a specially designed functional MRI (fMRI) cycling ergometer, we have determined the sequence in which the cortical and subcortical brain regions are modulated at low and high ratings perceived exertion (RPE) during an incremental exercise protocol. Results Additional to the activation of the classical motor control regions (motor, somatosensory, premotor and supplementary motor cortices and cerebellum), we found the activation of the regions associated with autonomic regulation (ie, insular cortex) (ie, positive blood-oxygen-level-dependent (BOLD) signal) during exercise. Also, we showed reduced activation (negative BOLD signal) of cognitive-related areas (prefrontal cortex), an effect that increased during exercise at a higher perceived intensity (RPE 13–17 on Borg Scale). The motor cortex remained active throughout the exercise protocol whereas the cerebellum was activated only at low intensity (RPE 6–12), not at high intensity (RPE 13–17). Conclusions These findings describe the sequence in which different brain areas become activated or deactivated during exercise of increasing intensity, including subcortical areas measured with fMRI analysis.

[1]  F. Scholkmann,et al.  Applications of Functional Near-Infrared Spectroscopy (fNIRS) Neuroimaging in Exercise–Cognition Science: A Systematic, Methodology-Focused Review , 2018, Journal of clinical medicine.

[2]  Erika K. Hussey,et al.  Affect during incremental exercise: The role of inhibitory cognition, autonomic cardiac function, and cerebral oxygenation , 2017, PloS one.

[3]  S. Sten,et al.  Neural inhibition can explain negative BOLD responses: A mechanistic modelling and fMRI study , 2017, NeuroImage.

[4]  D. Donaire-Gonzalez,et al.  The relationship between bicycle commuting and perceived stress: a cross-sectional study , 2017, BMJ Open.

[5]  C. Ugrinowitsch,et al.  Cerebral Regulation in Different Maximal Aerobic Exercise Modes , 2016, Front. Physiol..

[6]  N. Clarke,et al.  The effect of exercise intensity on cognitive performance during short duration treadmill running , 2016, Journal of human kinetics.

[7]  Gerry Leisman,et al.  Thinking, Walking, Talking: Integratory Motor and Cognitive Brain Function , 2016, Front. Public Health.

[8]  A. Oniz,et al.  Acute Supramaximal Exercise Increases the Brain Oxygenation in Relation to Cognitive Workload , 2016, Front. Hum. Neurosci..

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

[10]  G. Parfitt,et al.  Self-reported tolerance influences prefrontal cortex hemodynamics and affective responses , 2016, Cognitive, affective & behavioral neuroscience.

[11]  D. Nemet,et al.  Longitudinal Study Evaluating Postural Balance of Young Athletes , 2016, Perceptual and motor skills.

[12]  Aleksandrov Vg,et al.  The Role of Insular Cortex in Autonomic Control , 2015 .

[13]  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.

[14]  N. Aleksandrova,et al.  [The Role of Insular Cortex in Autonomic Control]. , 2015, Fiziologiia cheloveka.

[15]  Massimiliano Pau,et al.  Fatigue-induced balance impairment in young soccer players. , 2014, Journal of athletic training.

[16]  Peter Hagoort,et al.  Stimulating the Brain's Language Network: Syntactic Ambiguity Resolution after TMS to the Inferior Frontal Gyrus and Middle Temporal Gyrus , 2013, Journal of Cognitive Neuroscience.

[17]  Dan J Stein,et al.  Brain activity and perceived exertion during cycling exercise: an fMRI study , 2013, British Journal of Sports Medicine.

[18]  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.

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

[20]  A. Diamond Executive functions. , 2014, Handbook of clinical neurology.

[21]  B. Schmit,et al.  The effect of movement rate and complexity on functional magnetic resonance signal change during pedaling. , 2012, Motor control.

[22]  Lutz Jäncke,et al.  Limitation of physical performance in a muscle fatiguing handgrip exercise is mediated by thalamo‐insular activity , 2011, Human brain mapping.

[23]  P. Ekkekakis,et al.  The Pleasure and Displeasure People Feel When they Exercise at Different Intensities , 2011, Sports medicine.

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

[25]  T. Noakes,et al.  Time to move beyond a brainless exercise physiology: the evidence for complex regulation of human exercise performance. , 2011, Applied physiology, nutrition, and metabolism = Physiologie appliquee, nutrition et metabolisme.

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

[27]  I. Liberzon,et al.  The Neurocircuitry of Fear, Stress, and Anxiety Disorders , 2011, Neuropsychopharmacology.

[28]  Shigehiko Ogoh,et al.  Cerebral blood flow during exercise: mechanisms of regulation. , 2009, Journal of applied physiology.

[29]  B. Schmit,et al.  A novel technique for examining human brain activity associated with pedaling using fMRI , 2009, Journal of Neuroscience Methods.

[30]  P. Ekkekakis Let Them Roam Free? , 2009, Sports medicine.

[31]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

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

[33]  J. Viitasalo,et al.  Relationships between postural balance, rifle stability and shooting accuracy among novice rifle shooters , 2006, Scandinavian journal of medicine & science in sports.

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

[35]  E Kellis,et al.  Effects of an intermittent exercise fatigue protocol on biomechanics of soccer kick performance , 2006, Scandinavian journal of medicine & science in sports.

[36]  Mark Lyons,et al.  The impact of moderate and high intensity total body fatigue on passing accuracy in expert and novice basketball players. , 2006, Journal of sports science & medicine.

[37]  R. Malach,et al.  When the Brain Loses Its Self: Prefrontal Inactivation during Sensorimotor Processing , 2006, Neuron.

[38]  D. Caplan,et al.  Cognition, emotion and the cerebellum. , 2006, Brain : a journal of neurology.

[39]  Ross Tucker,et al.  The Role of Information Processing Between the Brain and Peripheral Physiological Systems in Pacing and Perception of Effort , 2006, Sports medicine.

[40]  Erik W Faria,et al.  The Science of Cycling , 2005, Sports medicine.

[41]  T D Noakes,et al.  Complex systems model of fatigue: integrative homoeostatic control of peripheral physiological systems during exercise in humans , 2004, British Journal of Sports Medicine.

[42]  P. Sparling,et al.  Endurance exercise selectively impairs prefrontal-dependent cognition , 2004, Brain and Cognition.

[43]  T. Noakes,et al.  From catastrophe to complexity: a novel model of integrative central neural regulation of effort and fatigue during exercise in humans , 2004, British Journal of Sports Medicine.

[44]  Jing Z. Liu,et al.  Human brain activation during sustained and intermittent submaximal fatigue muscle contractions: an FMRI study. , 2003, Journal of neurophysiology.

[45]  J. Williamson,et al.  Evidence for central command activation of the human insular cortex during exercise. , 2003, Journal of applied physiology.

[46]  M. Erb,et al.  Activation of Cortical and Cerebellar Motor Areas during Executed and Imagined Hand Movements: An fMRI Study , 1999, Journal of Cognitive Neuroscience.

[47]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[48]  A. Damasio The somatic marker hypothesis and the possible functions of the prefrontal cortex. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[49]  G. Borg Psychophysical bases of perceived exertion. , 1982, Medicine and science in sports and exercise.