Motor imagery involves predicting the sensory consequences of the imagined movement

Research on motor imagery has identified many similarities between imagined and executed actions at the behavioral, physiological and neural levels, thus supporting their “functional equivalence”. In contrast, little is known about their possible “computational equivalence”—specifically, whether the brain’s internal forward models predict the sensory consequences of imagined movements as they do for overt movements. Here, we address this question by assessing whether imagined self-generated touch produces an attenuation of real tactile sensations. Previous studies have shown that self-touch feels less intense compared with touch of external origin because the forward models predict the tactile feedback based on a copy of the motor command. Our results demonstrate that imagined self-touch is attenuated just as real self-touch is and that the imagery-induced attenuation follows the same spatiotemporal principles as does the attenuation elicited by overt movements. We conclude that motor imagery recruits the forward models to predict the sensory consequences of imagined movements.Forward models predict and attenuate the sensory feedback of voluntary movement yet their involvement in motor imagery has only been theorized. Here the authors show that motor imagery recruits forward models to elicit sensory attenuation to the same extent as real movements.

[1]  David Poeppel,et al.  The Effect of Imagination on Stimulation: The Functional Specificity of Efference Copies in Speech Processing , 2013, Journal of Cognitive Neuroscience.

[2]  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..

[3]  M. Jeannerod,et al.  Mental motor imagery: a window into the representational stages of action , 1995, Current Opinion in Neurobiology.

[4]  M. Jeannerod,et al.  Mentally simulated movements in virtual reality: does Fitt's law hold in motor imagery? , 1995, Behavioural Brain Research.

[5]  P. Haggard,et al.  Sensorimotor foundations of higher cognition , 1993 .

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

[7]  K. R. Ridderinkhof,et al.  How Kinesthetic Motor Imagery works: A predictive-processing theory of visualization in sports and motor expertise , 2015, Journal of Physiology-Paris.

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

[9]  C. Richards,et al.  Brain activity during visual versus kinesthetic imagery: An fMRI study , 2009, Human brain mapping.

[10]  D. Wolpert,et al.  The cerebellum is involved in predicting the sensory consequences of action , 1999, Neuroreport.

[11]  D. Poeppel,et al.  Health, USA Reviewed by: , 2010 .

[12]  R. Andersen,et al.  Decoding motor imagery from the posterior parietal cortex of a tetraplegic human , 2015, Science.

[13]  K. Jellinger Motor Cognition What Actions Tell the Self , 2007 .

[14]  T. Mulder Motor imagery and action observation: cognitive tools for rehabilitation , 2007, Journal of Neural Transmission.

[15]  D. Holdstock Past, present--and future? , 2005, Medicine, conflict, and survival.

[16]  Zoubin Ghahramani,et al.  Computational principles of movement neuroscience , 2000, Nature Neuroscience.

[17]  Klaus-Robert Müller,et al.  Motor Imagery for Severely Motor-Impaired Patients: Evidence for Brain-Computer Interfacing as Superior Control Solution , 2014, PloS one.

[18]  M. Jeannerod,et al.  Vegetative response during imagined movement is proportional to mental effort , 1991, Behavioural Brain Research.

[19]  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.

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

[21]  Christopher C. Berger,et al.  Mental Imagery Changes Multisensory Perception , 2013, Current Biology.

[22]  S. Blakemore,et al.  Action prediction in the cerebellum and in the parietal lobe , 2003, Experimental Brain Research.

[23]  M. Lotze,et al.  Motor imagery , 2006, Journal of Physiology-Paris.

[24]  M. Jeannerod,et al.  The timing of mentally represented actions , 1989, Behavioural Brain Research.

[25]  Martin Lotze,et al.  Kinesthetic imagery of musical performance , 2013, Front. Hum. Neurosci..

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

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

[28]  David W. Franklin,et al.  Computational Mechanisms of Sensorimotor Control , 2011, Neuron.

[29]  Marco Schieppati,et al.  Imagined and actual arm movements have similar durations when performed under different conditions of direction and mass , 2002, Experimental Brain Research.

[30]  J. Krakauer,et al.  Error correction, sensory prediction, and adaptation in motor control. , 2010, Annual review of neuroscience.

[31]  Arne Dietrich,et al.  Imaging the imagination: the trouble with motor imagery. , 2008, Methods.

[32]  R. Stark,et al.  Activation of the Parieto-Premotor Network Is Associated with Vivid Motor Imagery—A Parametric fMRI Study , 2011, PloS one.

[33]  Miguel A. L. Nicolelis,et al.  Brain–machine interfaces: past, present and future , 2006, Trends in Neurosciences.

[34]  Jeff H. Duyn,et al.  Cortical Systems Associated with Covert Music Rehearsal , 2002, NeuroImage.

[35]  P. R. Davidson,et al.  Widespread access to predictive models in the motor system: a short review , 2005, Journal of neural engineering.

[36]  E Ryding,et al.  Motor imagery activates the cerebellum regionally. A SPECT rCBF study with 99mTc-HMPAO. , 1993, Brain research. Cognitive brain research.

[37]  D. Wolpert,et al.  Perception of the Consequences of Self-Action Is Temporally Tuned and Event Driven , 2005, Current Biology.

[38]  P. Strick,et al.  Supplementary Motor Area and Presupplementary Motor Area: Targets of Basal Ganglia and Cerebellar Output , 2007, The Journal of Neuroscience.

[39]  Marco Schieppati,et al.  Does order and timing in performance of imagined and actual movements affect the motor imagery process? The duration of walking and writing task , 2002, Behavioural Brain Research.

[40]  M Jeannerod,et al.  Central activation of autonomic effectors during mental simulation of motor actions in man. , 1993, The Journal of physiology.

[41]  Marc Jeannerod,et al.  Motor Cognition: What Actions Tell the Self , 2006 .

[42]  H. Ehrsson,et al.  Sensorimotor predictions and tool use: Hand-held tools attenuate self-touch , 2017, Cognition.

[43]  P. Mahadevan,et al.  An overview , 2007, Journal of Biosciences.

[44]  J Decety,et al.  Analysis of actual and mental movement times in graphic tasks. , 1993, Acta psychologica.

[45]  D. Wolpert,et al.  Central cancellation of self-produced tickle sensation , 1998, Nature Neuroscience.

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

[47]  P. Strick,et al.  Cerebellum and nonmotor function. , 2009, Annual review of neuroscience.

[48]  F. Q. Ribeiro The meta-analysis , 2017, Brazilian journal of otorhinolaryngology.

[49]  C. E. Chapman,et al.  Sensory perception during movement in man , 2004, Experimental Brain Research.

[50]  Christopher C. Berger,et al.  The Content of Imagined Sounds Changes Visual Motion Perception in the Cross-Bounce Illusion , 2017, Scientific Reports.

[51]  D. Wolpert,et al.  Two Eyes for an Eye: The Neuroscience of Force Escalation , 2003, Science.

[52]  Stefan Geyer,et al.  Imagery of voluntary movement of fingers, toes, and tongue activates corresponding body-part-specific motor representations. , 2003, Journal of neurophysiology.

[53]  D. Wolpert,et al.  Evidence for sensory prediction deficits in schizophrenia. , 2005, The American journal of psychiatry.

[54]  D. Wolpert,et al.  Attenuation of Self-Generated Tactile Sensations Is Predictive, not Postdictive , 2006, PLoS biology.

[55]  H. Ehrsson,et al.  Body ownership determines the attenuation of self-generated tactile sensations , 2017, Proceedings of the National Academy of Sciences.

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

[57]  P. Maruff,et al.  Asymmetries between dominant and non-dominanthands in real and imagined motor task performance , 1999, Neuropsychologia.

[58]  D. Poeppel,et al.  Mental imagery of speech implicates two mechanisms of perceptual reactivation , 2016, Cortex.

[59]  Paul Maruff,et al.  The effect of an external load on the force and timing components of mentally represented actions , 2000, Behavioural Brain Research.

[60]  J. Krakauer,et al.  A computational neuroanatomy for motor control , 2008, Experimental Brain Research.

[61]  J. Grayson Reactions of the peripheral circulation to external heat , 1949, The Journal of physiology.

[62]  D. Wolpert,et al.  Why can't you tickle yourself? , 2000, Neuroreport.

[63]  E. Naito,et al.  Internally Simulated Movement Sensations during Motor Imagery Activate Cortical Motor Areas and the Cerebellum , 2002, The Journal of Neuroscience.

[64]  A. Haith,et al.  Model-based and model-free mechanisms of human motor learning. , 2013, Advances in experimental medicine and biology.

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

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

[67]  P. Strick,et al.  Chapter 32 Dentate output channels: motor and cognitive components , 1997 .

[68]  D. Wolpert,et al.  Spatio-Temporal Prediction Modulates the Perception of Self-Produced Stimuli , 1999, Journal of Cognitive Neuroscience.

[69]  Daniël Lakens,et al.  Calculating and reporting effect sizes to facilitate cumulative science: a practical primer for t-tests and ANOVAs , 2013, Front. Psychol..

[70]  Simon C Gandevia,et al.  Overestimation of force during matching of externally generated forces , 2011, The Journal of physiology.

[71]  J. Baron,et al.  Motor Imagery: A Backdoor to the Motor System After Stroke? , 2006, Stroke.

[72]  R. Dickstein,et al.  Motor Imagery in Physical Therapist Practice , 2007, Physical Therapy.

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

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

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

[76]  D. Poeppel,et al.  Imagined speech influences perceived loudness of sound , 2018, Nature Human Behaviour.

[77]  A. Sirigu,et al.  The Mental Representation of Hand Movements After Parietal Cortex Damage , 1996, Science.

[78]  R. Johansson,et al.  Prediction Precedes Control in Motor Learning , 2003, Current Biology.

[79]  M. Scott Corollary Discharge Provides the Sensory Content of Inner Speech , 2013, Psychological science.

[80]  Rick Grush,et al.  The emulation theory of representation: Motor control, imagery, and perception , 2004, Behavioral and Brain Sciences.

[81]  D. Wolpert,et al.  Motor prediction , 2001, Current Biology.

[82]  Herta Flor,et al.  Sensorimotor training and cortical reorganization. , 2009, NeuroRehabilitation.

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

[84]  Mitsuo Kawato,et al.  Internal models for motor control and trajectory planning , 1999, Current Opinion in Neurobiology.

[85]  Masao Ito Control of mental activities by internal models in the cerebellum , 2008, Nature Reviews Neuroscience.

[86]  A. Guillot,et al.  Re-imagining motor imagery: building bridges between cognitive neuroscience and sport psychology. , 2012, British journal of psychology.

[87]  J. Decety,et al.  Comparative analysis of actual and mental movement times in two graphic tasks , 1989, Brain and Cognition.

[88]  T. Whitford,et al.  Neurophysiological evidence of efference copies to inner speech , 2017, eLife.

[89]  P. Strick,et al.  Dentate output channels: motor and cognitive components. , 1997, Progress in brain research.

[90]  Bertram Walter,et al.  Your mind's hand: Motor imagery of pointing movements with different accuracy , 2010, NeuroImage.

[91]  Lesley Jones,et al.  The uses of mental imagery in athletics: An overview , 1997 .

[92]  M. Hallett,et al.  Functional properties of brain areas associated with motor execution and imagery. , 2003, Journal of neurophysiology.