Thinking, Walking, Talking: Integratory Motor and Cognitive Brain Function

In this article, we argue that motor and cognitive processes are functionally related and most likely share a similar evolutionary history. This is supported by clinical and neural data showing that some brain regions integrate both motor and cognitive functions. In addition, we also argue that cognitive processes coincide with complex motor output. Further, we also review data that support the converse notion that motor processes can contribute to cognitive function, as found by many rehabilitation and aerobic exercise training programs. Support is provided for motor and cognitive processes possessing dynamic bidirectional influences on each other.

[1]  D. Lindsley,et al.  After-Effects of Brain Injuries in War , 1943, Journal of The Royal Naval Medical Service.

[2]  M. Jeannerod.  TO ACT OR NOT TO ACT : PERSPECTIVES ON THE REPRESENTATION OF ACTIONS , 1999 .

[3]  Edmund Jacobson,et al.  ELECTRICAL MEASUREMENTS OF NEUROMUSCULAR STATES DURING MENTAL ACTIVITIES: VII. Imagination, Recollection and Abstract Thinking Involving the Speech Musculature , 1931 .

[4]  L. Garey.  Brodmann's localisation in the cerebral cortex , 1999 .

[5]  I. Deary,et al.  Neuroprotective lifestyles and the aging brain , 2012, Neurology.

[6]  E. McAuley,et al.  Exercise training increases size of hippocampus and improves memory , 2011, Proceedings of the National Academy of Sciences.

[7]  J. Decety,et al.  The power of simulation: Imagining one's own and other's behavior , 2006, Brain Research.

[8]  W. T. Thach,et al.  Functional mapping of the human cerebellum with positron emission tomography. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[9]  D. Nieman,et al.  Physical activity predicts gray matter volume in late adulthood: The Cardiovascular Health Study , 2011 .

[10]  J. Ratey,et al.  The positive impact of physical activity on cognition during adulthood: a review of underlying mechanisms, evidence and recommendations , 2011, Reviews in the neurosciences.

[11]  B. Popkin,et al.  Time use and physical activity: a shift away from movement across the globe , 2012, Obesity reviews : an official journal of the International Association for the Study of Obesity.

[12]  V. Gallese,et al.  What is so special about embodied simulation? , 2011, Trends in Cognitive Sciences.

[13]  W. Prinz.  Motor images are action plans. Commentary of M. Jeannerod: The representing brain: Neural correlates of motor intention and imagery , 1994 .

[14]  P. Haggard.  Conscious intention and motor cognition , 2005, Trends in Cognitive Sciences.

[15]  Gerry Leisman,et al.  Intentionality and “free-will” from a neurodevelopmental perspective , 2012, Front. Integr. Neurosci..

[16]  C. Zollikofer,et al.  Metopic suture of Taung (Australopithecus africanus) and its implications for hominin brain evolution , 2012, Proceedings of the National Academy of Sciences.

[17]  Christine D. Wilson,et al.  Grounding conceptual knowledge in modality-specific systems , 2003, Trends in Cognitive Sciences.

[18]  C. Koch,et al.  Constraints on cortical and thalamic projections: the no-strong-loops hypothesis , 1998, Nature.

[19]  U. Frith,et al.  The Weak Coherence Account: Detail-focused Cognitive Style in Autism Spectrum Disorders , 2006, Journal of autism and developmental disorders.

[20]  Linda B. Smith,et al.  Grounding development in cognitive processes. , 2000, Child development.

[21]  C. Eriksen,et al.  Effects of noise letters upon the identification of a target letter in a nonsearch task , 1974 .

[22]  D. Long.  Networks of the Brain , 2011 .

[23]  W. Penfield,et al.  SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION , 1937 .

[24]  B. Hale.  The effects of internal and external imagery on muscular and ocular concomitants , 1982 .

[25]  Gerry Leisman,et al.  Cognitive-motor interactions of the basal ganglia in development , 2014, Front. Syst. Neurosci..

[26]  Arthur F. Kramer,et al.  A neuroimaging investigation of the association between aerobic fitness, hippocampal volume, and memory performance in preadolescent children , 2010, Brain Research.

[27]  Rolf A. Zwaan,et al.  Language Comprehenders Mentally Represent the Shapes of Objects , 2002, Psychological science.

[28]  J. Atkinson,et al.  Motion- and orientation-specific cortical responses in infancy , 2005, Vision Research.

[29]  J. Booth,et al.  The Differential Role of Verbal and Spatial Working Memory in the Neural Basis of Arithmetic , 2014, Developmental neuropsychology.

[30]  Arthur F. Kramer,et al.  Effects of physical activity on cognition, well-being, and brain: Human interventions , 2007, Alzheimer's & Dementia.

[31]  J. Deutsch.  Perception and Communication , 1958, Nature.

[32]  Andrew T. Duchowski,et al.  Eye Tracking Methodology: Theory and Practice , 2003, Springer London.

[33]  E. Knudsen.  Instructed learning in the auditory localization pathway of the barn owl , 2002, Nature.

[34]  Jacquelyn Schachter,et al.  On the issue of completeness in second language acquisition , 1990 .

[35]  Nikos K. Logothetis,et al.  Frontiers in Computational Neuroscience Computational Neuroscience , 2022 .

[36]  F. Sofi,et al.  Physical activity and risk of cognitive decline: a meta‐analysis of prospective studies , 2011, Journal of internal medicine.

[37]  T. Schack.  The cognitive architecture of complex movement , 2004 .

[38]  Leslie G. Ungerleider,et al.  Imaging Brain Plasticity during Motor Skill Learning , 2002, Neurobiology of Learning and Memory.

[39]  Karl J. Friston,et al.  PHRENOLOGY : What Can Neuroimaging Tell Us About Distributed Circuitry ? , 2005 .

[40]  J. Decety,et al.  The cerebellum participates in mental activity: tomographic measurements of regional cerebral blood flow , 1990, Brain Research.

[41]  Masao Ito,et al.  Consensus Paper: The Cerebellum's Role in Movement and Cognition , 2013, The Cerebellum.

[42]  M. Jeannerod.  The representing brain: Neural correlates of motor intention and imagery , 1994, Behavioral and Brain Sciences.

[43]  Michael J. Martinez,et al.  Music and language side by side in the brain: a PET study of the generation of melodies and sentences , 2006, The European journal of neuroscience.

[44]  Arthur F. Kramer,et al.  Aerobic fitness is associated with greater white matter integrity in children , 2014, Front. Hum. Neurosci..

[45]  Arthur F. Kramer,et al.  Basal Ganglia Volume Is Associated with Aerobic Fitness in Preadolescent Children , 2010, Developmental Neuroscience.

[46]  Stewart M. McCauley,et al.  Evidence from Event-related Brain Potentials Perception and Bias in the Processing of Compound versus Phrasal Stress : , 2013 .

[47]  M. Hallett,et al.  Involvement of primary motor cortex in motor imagery and mental practice , 1994, Behavioral and Brain Sciences.

[48]  M. Land.  Eye movements and the control of actions in everyday life , 2006, Progress in Retinal and Eye Research.

[49]  Hideaki Soya,et al.  Cessation of voluntary wheel running increases anxiety-like behavior and impairs adult hippocampal neurogenesis in mice , 2013, Behavioural Brain Research.

[50]  J. Sanes.  Neurophysiology of preparation, movement and imagery , 1994, Behavioral and Brain Sciences.

[51]  GyuChang Lee,et al.  Effects of motor imagery training on balance and gait abilities in post-stroke patients: a randomized controlled trial , 2013, Clinical rehabilitation.

[52]  Julia Herschensohn,et al.  Language development and age , 2007 .

[53]  G. Rizzolatti,et al.  The organization of the cortical motor system: new concepts. , 1998, Electroencephalography and clinical neurophysiology.

[54]  Arthur F. Kramer,et al.  Neurobiological markers of exercise-related brain plasticity in older adults , 2013, Brain, Behavior, and Immunity.

[55]  Jeffrey N. Browndyke,et al.  Aerobic Exercise and Neurocognitive Performance: A Meta-Analytic Review of Randomized Controlled Trials , 2010, Psychosomatic medicine.

[56]  A. Kramer,et al.  Be smart, exercise your heart: exercise effects on brain and cognition , 2008, Nature Reviews Neuroscience.

[57]  Peter B. Jones,et al.  Infant Developmental Milestones and Subsequent Cognitive Function , 2007, Annals of neurology.

[58]  S. Keele,et al.  The cognitive and neural architecture of sequence representation. , 2003, Psychological review.

[59]  H. Kuypers,et al.  Splitbrain Monkeys: Cerebral Control of Ipsilateral and Contralateral Arm, Hand, and Finger Movements , 1972, Science.

[60]  Anusha Sivaramakrishnan,et al.  Quantifying the effect of posture on intracranial physiology in humans by MRI flow studies , 2005, Journal of magnetic resonance imaging : JMRI.

[61]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[62]  A. L. Yarbus,et al.  Eye Movements and Vision , 1967, Springer US.

[63]  R.N.Dej.,et al.  The Cerebral Cortex of Man , 1951, Neurology.

[64]  Naiman A. Khan,et al.  The Relation of Adiposity to Cognitive Control and Scholastic Achievement in Preadolescent Children , 2012, Obesity.

[65]  R. E. Passingham,et al.  The cerebellum and cognition: cerebellar lesions impair sequence learning but not conditional visuomotor learning in monkeys , 2000, Neuropsychologia.

[66]  Michael P. Kaschak,et al.  Body posture facilitates retrieval of autobiographical memories , 2007, Cognition.

[67]  Christa Neuper,et al.  Future prospects of ERD/ERS in the context of brain-computer interface (BCI) developments. , 2006, Progress in brain research.

[68]  Peter Carruthers,et al.  Evolution of working memory , 2013, Proceedings of the National Academy of Sciences.

[69]  F. Bartolomei,et al.  Imaging structural and functional connectivity: towards a unified definition of human brain organization? , 2008, Current opinion in neurology.

[70]  M. Posner,et al.  Attention and the detection of signals. , 1980, Journal of experimental psychology.

[71]  J B Poline,et al.  Partially overlapping neural networks for real and imagined hand movements. , 2000, Cerebral cortex.

[72]  M. Kinsbourne.  From Unilateral Neglect to the Brain Basis of Consciousness , 2006, Cortex.

[73]  F. Garbarini,et al.  At the root of embodied cognition: Cognitive science meets neurophysiology , 2004, Brain and Cognition.

[74]  Robert Melillo,et al.  The Plasticity of Brain Networks as a Basis for a Science of Nervous System Rehabilitation , 2014 .

[75]  E. Bates,et al.  Linguistic , Cognitive and Affective Development in Children with Pre-and Perinatal Focal Brain Injury : A Ten-Year Overview from the San Diego Longitudinal Project , 2004 .

[76]  A. Kramer,et al.  Fitness Effects on the Cognitive Function of Older Adults , 2003, Psychological science.

[77]  P. Strick,et al.  Basal ganglia and cerebellar loops: motor and cognitive circuits , 2000, Brain Research Reviews.

[78]  L. Squire.  Declarative and Nondeclarative Memory: Multiple Brain Systems Supporting Learning and Memory , 1992, Journal of Cognitive Neuroscience.

[79]  J. Donoghue,et al.  Plasticity and primary motor cortex. , 2000, Annual review of neuroscience.

[80]  K. Zentgraf,et al.  Cognitive motor processes: The role of motor imagery in the study of motor representations , 2009, Brain Research Reviews.

[81]  Daniel S. Margulies,et al.  Low frequency fluctuations reveal integrated and segregated processing among the cerebral hemispheres , 2011, NeuroImage.

[82]  Paige E. Scalf,et al.  Aerobic exercise training increases brain volume in aging humans. , 2006, The journals of gerontology. Series A, Biological sciences and medical sciences.

[83]  R. Llinás,et al.  Thalamocortical dysrhythmia: A neurological and neuropsychiatric syndrome characterized by magnetoencephalography. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[84]  M. Ridding,et al.  A single bout of aerobic exercise promotes motor cortical neuroplasticity. , 2013, Journal of applied physiology.

[85]  Peter B. Jones,et al.  Fronto-cerebellar systems are associated with infant motor and adult executive functions in healthy adults but not in schizophrenia , 2006, Proceedings of the National Academy of Sciences.

[86]  E. McAuley,et al.  The association between aerobic fitness and executive function is mediated by prefrontal cortex volume , 2012, Brain, Behavior, and Immunity.

[87]  H. Shibasaki,et al.  Movement-related change of electrocorticographic activity in human supplementary motor area proper. , 2000, Brain : a journal of neurology.

[88]  Li Wang,et al.  Exercise Is Associated with Reduced Risk for Incident Dementia among Persons 65 Years of Age and Older , 2006, Annals of Internal Medicine.

[89]  G. Vallortigara,et al.  Possible evolutionary origins of cognitive brain lateralization , 1999, Brain Research Reviews.

[90]  A. Sanabria,et al.  Randomized controlled trial. , 2005, World journal of surgery.

[91]  M. Inase,et al.  Neuronal activity in the primate premotor, supplementary, and precentral motor cortex during visually guided and internally determined sequential movements. , 1991, Journal of neurophysiology.

[92]  M. Isohanni,et al.  Infant developmental milestones: a 31-year follow-up. , 2005, Developmental medicine and child neurology.

[93]  Friedemann Pulvermüller,et al.  Can language-action links explain language laterality?: An ERP study of perceptual and articulatory learning of novel pseudowords , 2012, Cortex.

[94]  R. Passingham,et al.  Functional anatomy of the mental representation of upper extremity movements in healthy subjects. , 1995, Journal of neurophysiology.

[95]  Gerry Leisman,et al.  Measurement of axonal fiber connectivity in consciousness evaluation , 2014, 2014 IEEE 28th Convention of Electrical & Electronics Engineers in Israel (IEEEI).

[96]  M. Jeannerod.  Neural Simulation of Action: A Unifying Mechanism for Motor Cognition , 2001, NeuroImage.

[97]  Claudia Voelcker-Rehage,et al.  Structural and functional brain changes related to different types of physical activity across the life span , 2013, Neuroscience & Biobehavioral Reviews.

[98]  Barry Horwitz,et al.  The elusive concept of brain connectivity , 2003, NeuroImage.

[99]  C. Hillman,et al.  Physical fitness and academic achievement in third- and fifth-grade students. , 2007, Journal of sport & exercise psychology.

[100]  D. Long.  I of the Vortex: From Neurons to Self , 2002 .

[101]  R. Cotterill.  Cooperation of the basal ganglia, cerebellum, sensory cerebrum and hippocampus: possible implications for cognition, consciousness, intelligence and creativity , 2001, Progress in Neurobiology.

[102]  W. J. Robinson,et al.  The effects of skill level on EMG activity during internal and external imagery , 1986 .

[103]  P. Strick,et al.  Skill representation in the primary motor cortex after long-term practice. , 2007, Journal of neurophysiology.

[104]  O. Sporns,et al.  The economy of brain network organization , 2012, Nature Reviews Neuroscience.

[105]  E. McAuley,et al.  Frontiers in Aging Neuroscience Aging Neuroscience , 2022 .

[106]  J. Reggia,et al.  The callosal dilemma: Explaining diaschisis in the context of hemispheric rivalry via a neural network model , 2001, Neurological research.

[107]  M. Hallett,et al.  The relative metabolic demand of inhibition and excitation , 2000, Nature.

[108]  Liang Wang,et al.  Dynamic functional reorganization of the motor execution network after stroke. , 2010, Brain : a journal of neurology.

[109]  S. Langenecker,et al.  Emotion regulation through execution, observation, and imagery of emotional movements , 2013, Brain and Cognition.

[110]  Tyrone D. Cannon,et al.  Infant motor development is associated with adult cognitive categorisation in a longitudinal birth cohort study. , 2006, Journal of child psychology and psychiatry, and allied disciplines.

[111]  N. Logothetis,et al.  In Vivo Measurement of Cortical Impedance Spectrum in Monkeys: Implications for Signal Propagation , 2007, Neuron.

[112]  Matthew B. Pontifex,et al.  Aerobic fitness and cognitive development: Event-related brain potential and task performance indices of executive control in preadolescent children. , 2009, Developmental psychology.

[113]  H. Ridley.  Eye and Brain , 1973 .

[114]  Gerry Leisman,et al.  Networks of Conscious Experience: Computational Neuroscience in Understanding Life, Death, and Consciousness , 2009, Reviews in the neurosciences.

[115]  Catherine R. Harrison,et al.  Ageing, fitness and neurocognitive function , 1999, Nature.

[116]  M. Hallett.  Transcranial magnetic stimulation and the human brain , 2000, Nature.

[117]  A. Berthoz,et al.  Mental representations of movements. Brain potentials associated with imagination of hand movements. , 1995, Electroencephalography and clinical neurophysiology.

[118]  A. F. Kramer,et al.  The effect of acute treadmill walking on cognitive control and academic achievement in preadolescent children , 2009, Neuroscience.

[119]  J. Mazziotta,et al.  Mapping motor representations with positron emission tomography , 1994, Nature.

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

[121]  Ewald Moser,et al.  Premovement activity of the pre-supplementary motor area and the readiness for action: studies of time-resolved event-related functional MRI. , 2005, Human movement science.

[122]  Cuntai Guan,et al.  Temporal classification of multichannel near-infrared spectroscopy signals of motor imagery for developing a brain–computer interface , 2007, NeuroImage.

[123]  Christine Chiarello,et al.  Right hemisphere language comprehension : perspectives from cognitive neuroscience , 1998 .

[124]  Simon B. Eickhoff,et al.  Modulating cortical connectivity in stroke patients by rTMS assessed with fMRI and dynamic causal modeling , 2010, NeuroImage.

[125]  Jonathan D. Nelson,et al.  Human cortical representations for reaching: Mirror neurons for execution, observation, and imagery , 2007, NeuroImage.

[126]  G. Fink,et al.  Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging , 2008, Annals of neurology.

[127]  J. Schmahmann.  From movement to thought: Anatomic substrates of the cerebellar contribution to cognitive processing , 1996, Human brain mapping.

[128]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[129]  Helen J. Neville,et al.  Language comprehension and cerebral specialization from 13 to 20 months , 1997 .

[130]  C. Cotman,et al.  Exercise: a behavioral intervention to enhance brain health and plasticity , 2002, Trends in Neurosciences.

[131]  C. Kentros,et al.  Hippocampal place cells: The “where” of episodic memory? , 2006, Hippocampus.

[132]  M Hallett,et al.  Studies of neuroplasticity with transcranial magnetic stimulation. , 1998, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[133]  E. McAuley,et al.  Functional connectivity: A source of variance in the association between cardiorespiratory fitness and cognition? , 2010, Neuropsychologia.

[134]  Arthur F. Kramer,et al.  The Influence of Childhood Aerobic Fitness on Learning and Memory , 2013, PloS one.

[135]  Gerry Leisman,et al.  Clinical Motor and Cognitive Neurobehavioral Relationships in the Basal Ganglia , 2013 .

[136]  M. Garrett,et al.  Syntactically Based Sentence Processing Classes: Evidence from Event-Related Brain Potentials , 1991, Journal of Cognitive Neuroscience.

[137]  R. Beer.  Dynamical approaches to cognitive science , 2000, Trends in Cognitive Sciences.

[138]  J. Doyon,et al.  Reorganization and plasticity in the adult brain during learning of motor skills , 2005, Current Opinion in Neurobiology.

[139]  M. Ridding,et al.  The influence of a single bout of aerobic exercise on short-interval intracortical excitability , 2014, Experimental Brain Research.

[140]  J. Rothwell,et al.  Transcranial magnetic stimulation in cognitive neuroscience – virtual lesion, chronometry, and functional connectivity , 2000, Current Opinion in Neurobiology.

[141]  M. Schmuckler,et al.  The representing brain : Neural correlates of motor intention and imagery , 2009 .

[142]  C Bundesen,et al.  A computational theory of visual attention. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[143]  Gerry Leisman,et al.  The neurological development of the child with the educational enrichment in mind , 2015 .

[144]  Philippe A. Chouinard,et al.  Human Neuroscience , 2022 .

[145]  M. Steinling,et al.  Tomographic measurements of regional cerebral blood flow in progressive supranuclear palsy and Parkinson's disease , 1995, Acta neurologica Scandinavica.

[146]  O. R. T.-Braude.  Cognitive Rehabilitation in Developmental Disabilities , 2015 .

[147]  P. Strick,et al.  Motor areas in the frontal lobe of the primate , 2002, Physiology & Behavior.

[148]  Matthew B. Pontifex,et al.  Exercise improves behavioral, neurocognitive, and scholastic performance in children with attention-deficit/hyperactivity disorder. , 2013, The Journal of pediatrics.

[149]  U Proske,et al.  The role of muscle receptors in the detection of movements , 2000, Progress in Neurobiology.

[150]  Rani Lueder,et al.  Hard facts about soft machines : the ergonomics of seating , 1994 .

[151]  R Weinberg,et al.  New Concepts... , 1995 .

[152]  G Pfurtscheller,et al.  Separability of EEG signals recorded during right and left motor imagery using adaptive autoregressive parameters. , 1998, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[153]  M. Jeannerod,et al.  Mental simulation of an action modulates the excitability of spinal reflex pathways in man. , 1997, Brain research. Cognitive brain research.

[154]  N. Gregersen,et al.  A Comparison of Eye Movement Behavior of Inexperienced and Experienced Drivers in Real Traffic Environments , 2005, Optometry and vision science : official publication of the American Academy of Optometry.

[155]  M. Schieber.  New Views of the Primary Motor Cortex , 2000 .

[156]  F. Pulvermüller,et al.  Walking or Talking?: Behavioral and Neurophysiological Correlates of Action Verb Processing , 2001, Brain and Language.

[157]  K. Zilles,et al.  Functional neuroanatomy of the primate isocortical motor system , 2000, Anatomy and Embryology.

[158]  Gerry Leisman,et al.  Cortical Activity waves are the physical carriers of memory and thought , 2015, 2015 7th International IEEE/EMBS Conference on Neural Engineering (NER).

[159]  Lea Fleischer,et al.  The Senses Considered As Perceptual Systems , 2016 .

[160]  Peter H. Sudmant,et al.  Evolution of Human-Specific Neural SRGAP2 Genes by Incomplete Segmental Duplication , 2012, Cell.

[161]  R. Lickliter,et al.  Intersensory redundancy guides attentional selectivity and perceptual learning in infancy. , 2000, Developmental psychology.

[162]  Hugo Merchant,et al.  Motor system evolution and the emergence of high cognitive functions , 2014, Progress in Neurobiology.

[163]  Nancy W Glynn,et al.  Physical activity predicts microstructural integrity in memory-related networks in very old adults. , 2014, The journals of gerontology. Series A, Biological sciences and medical sciences.

[164]  O. Foerster,et al.  THE MOTOR CORTEX IN MAN IN THE LIGHT OF HUGHLINGS JACKSON'S DOCTRINES , 1936 .

[165]  W. Harcourt‐Smith.  The First Hominins and the Origins of Bipedalism , 2010, Evolution: Education and Outreach.

[166]  Gerry Leisman,et al.  The basal ganglia: motor and cognitive relationships in a clinical neurobehavioral context , 2013, Reviews in the neurosciences.

[167]  Irene P. Kan,et al.  ROLE OF MENTAL IMAGERY IN A PROPERTY VERIFICATION TASK: FMRI EVIDENCE FOR PERCEPTUAL REPRESENTATIONS OF CONCEPTUAL KNOWLEDGE , 2003, Cognitive neuropsychology.

[168]  Arthur F. Kramer,et al.  Capitalizing on cortical plasticity: influence of physical activity on cognition and brain function , 2007, Trends in Cognitive Sciences.

[169]  A. Treisman,et al.  A feature-integration theory of attention , 1980, Cognitive Psychology.

[170]  K. Erickson,et al.  Exercise Effects on Brain and Cognition in Older Adults , 2013 .