Neural and Behavioral Outcomes Differ Following Equivalent Bouts of Motor Imagery or Physical Practice

Despite its reported effectiveness for the acquisition of motor skills, we know little about how motor imagery (MI)-based brain activation and performance evolves when MI (the imagined performance of a motor task) is used to learn a complex motor skill compared to physical practice (PP). The current study examined changes in MI-related brain activity and performance driven by an equivalent bout of MI- or PP-based training. Participants engaged in 5 days of either MI or PP of a dart-throwing task. Brain activity (via fMRI) and performance-related outcomes were obtained using a pre/post/retention design. Relative to PP, MI-based training did not drive robust changes in brain activation and was inferior for realizing improvements in performance: Greater activation in regions critical to refining the motor program was observed in the PP versus MI group posttraining, and relative to those driven via PP, MI led only to marginal improvements in performance. Findings indicate that the modality of practice (i.e., MI vs. PP) used to learn a complex motor skill manifests as differences in both resultant patterns of brain activity and performance. Ultimately, by directly comparing brain activity and behavioral outcomes after equivalent training through MI versus PP, this work provides unique knowledge regarding the neural mechanisms underlying learning through MI.

[1]  L Nyberg,et al.  Motor imagery: if you can't do it, you won't think it , 2010, Scandinavian journal of medicine & science in sports.

[2]  William M. Land,et al.  Perceptual-Cognitive Changes During Motor Learning: The Influence of Mental and Physical Practice on Mental Representation, Gaze Behavior, and Performance of a Complex Action , 2016, Front. Psychol..

[3]  R. Emmerik,et al.  The effects of practice on limb kinematics in a throwing task. , 1989, Journal of motor behavior.

[4]  Jing Wang,et al.  The Study of Object-Oriented Motor Imagery Based on EEG Suppression , 2015, PloS one.

[5]  Alice F. Healy,et al.  Judging joint angles and movement outcome: Shifting the focus of attention in dart-throwing. , 2014, Journal of experimental psychology. Human perception and performance.

[6]  Jessica X. Brooks,et al.  The Primate Cerebellum Selectively Encodes Unexpected Self-Motion , 2013, Current Biology.

[7]  J. Schorer,et al.  Influence of varying focus of attention conditions on dart throwing performance in experts and novices , 2012, Experimental Brain Research.

[8]  Sarah N. Kraeutner,et al.  Disruption of motor imagery performance following inhibition of the left inferior parietal lobe , 2019, Neuropsychologia.

[9]  Daniel M. Wolpert,et al.  Forward Models for Physiological Motor Control , 1996, Neural Networks.

[10]  H. Nakata,et al.  Effector-independent brain activity during motor imagery of the upper and lower limbs: An fMRI study , 2014, Neuroscience Letters.

[11]  Jessica A Turner,et al.  Cerebral and cerebellar sensorimotor plasticity following motor imagery-based mental practice of a sequential movement. , 2004, Journal of rehabilitation research and development.

[12]  Adam J. Toth,et al.  Cognitive to physical performance: a conceptual model for the role of motor simulation in performance , 2019, International Review of Sport and Exercise Psychology.

[13]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[14]  Yongmin Chang,et al.  Neural correlates of motor imagery for elite archers , 2010, NMR in biomedicine.

[15]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[16]  J. Doyon,et al.  Online and Offline Performance Gains Following Motor Imagery Practice: A Comprehensive Review of Behavioral and Neuroimaging Studies , 2016, Front. Hum. Neurosci..

[17]  Laurentiu S. Popa,et al.  Predictive and Feedback Performance Errors Are Signaled in the Simple Spike Discharge of Individual Purkinje Cells , 2012, The Journal of Neuroscience.

[18]  Sarah N. Kraeutner,et al.  Skill acquisition via motor imagery relies on both motor and perceptual learning. , 2016, Behavioral neuroscience.

[19]  Nicolas Schweighofer,et al.  Motor learning without doing: trial-by-trial improvement in motor performance during mental training. , 2010, Journal of neurophysiology.

[20]  D. Wolpert,et al.  Internal models in the cerebellum , 1998, Trends in Cognitive Sciences.

[21]  Aymeric Guillot,et al.  Experts bodies, experts minds: How physical and mental training shape the brain , 2014, Front. Hum. Neurosci..

[22]  Martin G Edwards,et al.  Kinesthetic Imagery Provides Additive Benefits to Internal Visual Imagery on Slalom Task Performance. , 2017, Journal of sport & exercise psychology.

[23]  William M. Land,et al.  Mental Representation and Mental Practice: Experimental Investigation on the Functional Links between Motor Memory and Motor Imagery , 2014, PloS one.

[24]  Philippe Gorce,et al.  Is the time of release during a precision throwing task, predictable? , 2012, Computer methods in biomechanics and biomedical engineering.

[25]  Y. Wu,et al.  The effect of motor imagery with specific implement in expert badminton player , 2014, Neuroscience.

[26]  J Tanji,et al.  Supplementary motor cortex in organization of movement. , 1996, European neurology.

[27]  G. Rizzolatti,et al.  Cortical mechanisms underlying the organization of goal-directed actions and mirror neuron-based action understanding. , 2014, Physiological reviews.

[28]  S. Swinnen,et al.  Neural correlates of action: Comparing meta-analyses of imagery, observation, and execution , 2018, Neuroscience & Biobehavioral Reviews.

[29]  S. Swinnen,et al.  Kinesthetic, but not visual, motor imagery modulates corticomotor excitability , 2005, Experimental Brain Research.

[30]  Sarah N. Kraeutner,et al.  Motor imagery-based brain activity parallels that of motor execution: Evidence from magnetic source imaging of cortical oscillations , 2014, Brain Research.

[31]  A. Boyadjian,et al.  Plasticity of motor cortex induced by coordination and training , 2011, Clinical Neurophysiology.

[32]  Stefan Skare,et al.  How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging , 2003, NeuroImage.

[33]  J Tanji,et al.  Comparison of movement-related activity in two cortical motor areas of primates. , 1982, Journal of neurophysiology.

[34]  E. Bizzi,et al.  Neuronal Correlates of Kinematics-to-Dynamics Transformation in the Supplementary Motor Area , 2002, Neuron.

[35]  Steven L. Small,et al.  The mind of expert motor performance is cool and focused , 2007, NeuroImage.

[36]  A. Healy,et al.  How changing the focus of attention affects performance, kinematics, and electromyography in dart throwing. , 2010, Human movement science.

[37]  A. Canavan,et al.  Successive roles of the cerebellum and premotor cortices in trajectorial learning. , 1994, Neuroreport.

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

[39]  Jin-Chern Chiou,et al.  A Comparison of Independent Event-Related Desynchronization Responses in Motor-Related Brain Areas to Movement Execution, Movement Imagery, and Movement Observation , 2016, PloS one.

[40]  P. Jackson,et al.  The neural network of motor imagery: An ALE meta-analysis , 2013, Neuroscience & Biobehavioral Reviews.

[41]  F. Binkofski,et al.  Two action systems in the human brain , 2013, Brain and Language.

[42]  D. Westwood,et al.  Movement related sensory feedback is not necessary for learning to execute a motor skill , 2019, Behavioural Brain Research.

[43]  M. D. de Lussanet,et al.  An Internal Focus Leads to Longer Quiet Eye Durations in Novice Dart Players , 2016, Front. Psychol..

[44]  J. Annett Motor imagery: Perception or action? , 1995, Neuropsychologia.

[45]  Peter Svensson,et al.  Training-induced dynamics of accuracy and precision in human motor control , 2017, Scientific Reports.

[46]  J. Krakauer,et al.  Inside the brain of an elite athlete: the neural processes that support high achievement in sports , 2009, Nature Reviews Neuroscience.

[47]  W. Zijlstra,et al.  The role of motor imagery in learning a totally novel movement , 2003, Experimental Brain Research.

[48]  M. Bove,et al.  Provision of somatosensory inputs during motor imagery enhances learning-induced plasticity in human motor cortex , 2017, Scientific Reports.

[49]  Timothy Bardouille,et al.  Laterality of brain activity during motor imagery is modulated by the provision of source level neurofeedback , 2014, NeuroImage.

[50]  G. Rizzolatti,et al.  Two different streams form the dorsal visual system: anatomy and functions , 2003, Experimental Brain Research.

[51]  A. Moran,et al.  Does Motor Simulation Theory Explain the Cognitive Mechanisms Underlying Motor Imagery? A Critical Review , 2017, Front. Hum. Neurosci..

[52]  M. Hallett,et al.  Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. , 2008, Cerebral cortex.

[53]  William M. Land,et al.  Effects of Physical Practice and Imagery Practice on Bilateral Transfer in Learning a Sequential Tapping Task , 2016, PloS one.

[54]  J. Cumming,et al.  The Nature, Measurement, and Development of Imagery Ability , 2018 .

[55]  M. Spittle,et al.  Mental Practice and the Retention of Motor Learning: A Pilot Study , 2010, Perceptual and motor skills.

[56]  Jing Luo,et al.  Sport expert's motor imagery: Functional imaging of professional motor skills and simple motor skills , 2010, Brain Research.

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

[58]  Charalambos Papaxanthis,et al.  Neural plasticity during motor learning with motor imagery practice: Review and perspectives , 2017, Neuroscience.

[59]  G. A. Miller,et al.  Current trends and challenges in MRI acquisitions to investigate brain function. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[60]  M. Lotze,et al.  Task-Dependent Interaction between Parietal and Contralateral Primary Motor Cortex during Explicit versus Implicit Motor Imagery , 2012, PloS one.

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

[62]  Ben J Edwards,et al.  Effect of time of day on the accuracy and consistency of the badminton serve , 2005, Ergonomics.

[63]  Yanling Pi,et al.  Motor experience with a sport-specific implement affects motor imagery , 2018, PeerJ.

[64]  Thomas Schack,et al.  The Representation of Motor (Inter)action, States of Action, and Learning: Three Perspectives on Motor Learning by Way of Imagery and Execution , 2017, Front. Psychol..

[65]  E. Bizzi,et al.  Neuronal activity in the supplementary motor area of monkeys adapting to a new dynamic environment. , 2004, Journal of neurophysiology.

[66]  J. Doyon,et al.  Dynamic Cortical and Subcortical Networks in Learning and Delayed Recall of Timed Motor Sequences , 2002, The Journal of Neuroscience.

[67]  J. Culham,et al.  The role of parietal cortex in visuomotor control: What have we learned from neuroimaging? , 2006, Neuropsychologia.

[68]  Hang Zhang,et al.  Behavioral improvements and brain functional alterations by motor imagery training , 2011, Brain Research.

[69]  C. Hall,et al.  The imagery ability, imagery use, and performance relationship , 2005 .

[70]  Eli Brenner,et al.  Throwing darts: timing is not the limiting factor , 2002, Experimental Brain Research.

[71]  G. Pfurtscheller,et al.  Motor imagery activates primary sensorimotor area in humans , 1997, Neuroscience Letters.

[72]  R. Elliott,et al.  Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. , 2000, Cerebral cortex.

[73]  Emilio Bizzi,et al.  Cortical circuits and modules in movement generation: experiments and theories , 2016, Current Opinion in Neurobiology.

[74]  G. R. Hancock,et al.  On the Problem of Two-Dimensional Error Scores: Measures and Analyses of Accuracy, Bias, and Consistency. , 1995, Journal of motor behavior.

[75]  Sarah N. Kraeutner,et al.  Motor imagery-based skill acquisition disrupted following rTMS of the inferior parietal lobule , 2016, Experimental Brain Research.

[76]  Konstantina Kilteni,et al.  Motor imagery involves predicting the sensory consequences of the imagined movement , 2018, Nature Communications.

[77]  T. Reilly,et al.  Effects of time of day and distance upon accuracy and consistency of throwing darts , 2007, Journal of sports sciences.

[78]  P. Holmes,et al.  The PETTLEP Approach to Motor Imagery: A Functional Equivalence Model for Sport Psychologists , 2001 .

[79]  Yongmin Chang,et al.  Brain activation patterns of motor imagery reflect plastic changes associated with intensive shooting training , 2012, Behavioural Brain Research.

[80]  M. Bove,et al.  The tool as the last piece of the athlete’s gesture imagery puzzle , 2014, Neuroscience.

[81]  E. Bizzi,et al.  Neuronal Correlates of Motor Performance and Motor Learning in the Primary Motor Cortex of Monkeys Adapting to an External Force Field , 2001, Neuron.

[82]  Steven C. Cramer,et al.  Brain activation during execution and motor imagery of novel and skilled sequential hand movements , 2005, NeuroImage.

[83]  L. Nyberg,et al.  Motor Representations and Practice Affect Brain Systems Underlying Imagery: An fMRI Study of Internal Imagery in Novices and Active High Jumpers , 2008, The open neuroimaging journal.

[84]  James W. Roberts,et al.  The effect of action observation and motor imagery combinations on upper limb kinematics and EMG during dart‐throwing , 2019, Scandinavian journal of medicine & science in sports.

[85]  C. Shea,et al.  Principles derived from the study of simple skills do not generalize to complex skill learning , 2002, Psychonomic bulletin & review.

[86]  M. Hallett,et al.  Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. , 1995, Journal of neurophysiology.

[87]  C. Kennard,et al.  Functional role of the supplementary and pre-supplementary motor areas , 2008, Nature Reviews Neuroscience.

[88]  C. Schuster,et al.  Best practice for motor imagery: a systematic literature review on motor imagery training elements in five different disciplines , 2011, BMC medicine.

[89]  Leonardo G. Cohen,et al.  Cortico-subcortical neuronal circuitry associated with reconsolidation of human procedural memories , 2014, Cortex.

[90]  L. Cohen,et al.  Neuroplasticity Subserving Motor Skill Learning , 2011, Neuron.

[91]  T. Pozzo,et al.  Improvement and generalization of arm motor performance through motor imagery practice , 2006, Neuroscience.

[92]  Sarah N. Kraeutner,et al.  Experience modulates motor imagery‐based brain activity , 2018, The European journal of neuroscience.

[93]  S. Small,et al.  Fine modulation in network activation during motor execution and motor imagery. , 2004, Cerebral cortex.

[94]  Sarah N. Kraeutner,et al.  The effector independent nature of motor imagery: Evidence from rTMS induced inhibition to the primary motor cortices , 2017, Neuropsychologia.

[95]  H Wichman,et al.  “Inner” Darts: Effects of Mental Practice on Performance of Dart Throwing , 1978, Perceptual and motor skills.

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

[97]  Anina N. Rich,et al.  Multimodal functional imaging of motor imagery using a novel paradigm , 2013, NeuroImage.

[98]  Craig Hall,et al.  The MIQ-RS: A Suitable Option for Examining Movement Imagery Ability , 2007, Evidence-based complementary and alternative medicine : eCAM.

[99]  Amount of Mental Practice and Performance of a Simple Motor Task , 2009, Perceptual and motor skills.

[100]  Bert Jonsson,et al.  Learning by Doing and Learning by Thinking: An fMRI Study of Combining Motor and Mental Training , 2008, Frontiers in human neuroscience.

[101]  Magdalena Ietswaart,et al.  Perceptual decisions regarding object manipulation are selectively impaired in apraxia or when tDCS is applied over the left IPL , 2016, Neuropsychologia.

[102]  J. DeSouza,et al.  Tracking Plasticity: Effects of Long-Term Rehearsal in Expert Dancers Encoding Music to Movement , 2016, PloS one.

[103]  Sarah N. Kraeutner,et al.  Characterizing skill acquisition through motor imagery with no prior physical practice. , 2016, Journal of experimental psychology. Human perception and performance.

[104]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[105]  H. Akaike A new look at the statistical model identification , 1974 .

[106]  R. Magill,et al.  Environmental Context Affects Outcome and Kinematic Changes at Different Rates during Skill Learning , 2013, Perceptual and motor skills.

[107]  Sarah N. Kraeutner,et al.  Generate, maintain, manipulate? Exploring the multidimensional nature of motor imagery , 2020 .

[108]  A. Bastian Learning to predict the future: the cerebellum adapts feedforward movement control , 2006, Current Opinion in Neurobiology.

[109]  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.

[110]  A. Healy,et al.  Mental Practice in the Intermanual Transfer of Motor Skills , 2010 .

[111]  Carolyn Copper,et al.  Does mental practice enhance performance , 1994 .

[112]  Jianfeng Hu,et al.  Automated Detection of Driver Fatigue Based on AdaBoost Classifier with EEG Signals , 2017, Front. Comput. Neurosci..

[113]  Simon B. Eickhoff,et al.  A quantitative meta-analysis and review of motor learning in the human brain , 2013, NeuroImage.

[114]  Akito Miura,et al.  Characteristics of the athletes' brain: Evidence from neurophysiology and neuroimaging , 2010, Brain Research Reviews.

[115]  Julien Doyon,et al.  Functional cerebral reorganization following motor sequence learning through mental practice with motor imagery , 2003, NeuroImage.

[116]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[117]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[118]  P. Roland,et al.  Supplementary motor area and other cortical areas in organization of voluntary movements in man. , 1980, Journal of neurophysiology.

[119]  D. Eaves,et al.  Imagery ability: the individual difference gradient and novel training methods (Commentary on Kraeutner et al. (2018)) , 2018, The European journal of neuroscience.

[120]  J. Decety,et al.  Functional anatomy of execution, mental simulation, observation, and verb generation of actions: A meta‐analysis , 2001, Human brain mapping.