Subjective vividness of motor imagery has a neural signature in human premotor and parietal cortex

Motor imagery (MI) is the process in which subjects imagine executing a body movement with a strong kinesthetic component from a first-person perspective. The individual capacity to elicit such mental images is not universal but varies within and between subjects. Neuroimaging studies have shown that these inter-as well as intra-individual differences in imagery quality mediate the amplitude of neural activity during MI on a group level. However, these analyses were not sensitive to forms of representation that may not map onto a simple modulation of overall amplitude. Therefore, the present study asked how far the subjective impression of motor imagery vividness is reflected by a spatial neural code, and how patterns of neural activation in different motor regions relate to specific imagery impressions. During fMRI scanning, 20 volunteers imagined three different types of right-hand actions. After each imagery trial, subjects were asked to evaluate the perceived vividness of their imagery. A correlation analysis compared the rating differences and neural dissimilarity values of the rating groups separately for each region of interest. Results showed a significant positive correlation in the left vPMC and right IPL, indicating that these regions particularly reflect perceived imagery vividness in that similar rated trials evoke more similar neural patterns. A decoding analysis revealed that the vividness of the motor image related systematically to the action specificity of neural activation patterns in left vPMC and right SPL. Imagined actions accompanied by higher vividness ratings were significantly more distinguishable within these areas. Altogether, results showed that spatial patterns of neural activity within the human motor cortices reflect the individual vividness of imagined actions. Hence, the findings reveal a link between the subjective impression of motor imagery vividness and objective physiological markers.

[1]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[2]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

[3]  John-Dylan Haynes,et al.  Decoding and predicting intentions , 2011, Annals of the New York Academy of Sciences.

[4]  G. E. Alexander,et al.  Preparation for movement: neural representations of intended direction in three motor areas of the monkey. , 1990, Journal of neurophysiology.

[5]  Adam K. Anderson,et al.  Population coding of affect across stimuli, modalities and individuals , 2014, Nature Neuroscience.

[6]  Dieter Vaitl,et al.  Neural simulation of actions: Effector‐ versus action‐specific motor maps within the human premotor and posterior parietal area? , 2014, Human brain mapping.

[7]  Nikolaus Kriegeskorte,et al.  Unique semantic space in the brain of each beholder predicts perceived similarity , 2014, Proceedings of the National Academy of Sciences.

[8]  A. Canavan,et al.  Neural correlates of visuospatial imagery , 2002, Behavioural Brain Research.

[9]  V. Gallese Embodied simulation: From neurons to phenomenal experience , 2005 .

[10]  Rupert Lanzenberger,et al.  The suppressive influence of SMA on M1 in motor imagery revealed by fMRI and dynamic causal modeling , 2008, NeuroImage.

[11]  Nikolaus Kriegeskorte,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[12]  Lisa Aziz-Zadeh,et al.  Embodied semantics for actions: Findings from functional brain imaging , 2008, Journal of Physiology-Paris.

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

[14]  V. Gallese The Roots of Empathy: The Shared Manifold Hypothesis and the Neural Basis of Intersubjectivity , 2003, Psychopathology.

[15]  S. Scott,et al.  Cortical control of reaching movements , 1997, Current Opinion in Neurobiology.

[16]  A. Fuchs,et al.  Cortical and cerebellar activity of the human brain during imagined and executed unimanual and bimanual action sequences: a functional MRI study. , 2003, Brain research. Cognitive brain research.

[17]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[18]  A. P. Georgopoulos,et al.  Cognitive spatial-motor processes , 1989, Experimental Brain Research.

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

[20]  C. Gross,et al.  Spatial maps for the control of movement , 1998, Current Opinion in Neurobiology.

[21]  Aymeric Guillot,et al.  The modulation of motor cortex excitability during motor imagery depends on imagery quality , 2012, The European journal of neuroscience.

[22]  L. Fogassi,et al.  A Touching Sight SII/PV Activation during the Observation and Experience of Touch , 2004, Neuron.

[23]  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.

[24]  D. Markland,et al.  Movement imagery ability: development and assessment of a revised version of the vividness of movement imagery questionnaire. , 2008, Journal of sport & exercise psychology.

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

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

[27]  Li Su,et al.  A Toolbox for Representational Similarity Analysis , 2014, PLoS Comput. Biol..

[28]  D. Wolpert,et al.  Maintaining internal representations: the role of the human superior parietal lobe , 1998, Nature Neuroscience.

[29]  Anders M. Dale,et al.  Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature , 2010, NeuroImage.

[30]  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.

[31]  M. Bozkurt,et al.  Functional anatomy. , 1980, Equine veterinary journal.

[32]  Robert Turner,et al.  Image Distortion Correction in fMRI: A Quantitative Evaluation , 2002, NeuroImage.

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

[34]  Richard Goldstein,et al.  Human Neuroscience , 2010 .

[35]  L. Craighero,et al.  Human motor cortex excitability during the perception of others’ action , 2005, Current Opinion in Neurobiology.

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

[37]  N. Kriegeskorte,et al.  Author ' s personal copy Representational geometry : integrating cognition , computation , and the brain , 2013 .

[38]  Christopher A. Buneo,et al.  Direct visuomotor transformations for reaching , 2002, Nature.

[39]  G. Rizzolatti,et al.  The Cortical Motor System , 2001, Neuron.

[40]  D. Landers,et al.  The effects of mental practice on motor skill learning and performance: A meta-analysis. , 1983 .

[41]  S. Wise The primate premotor cortex: past, present, and preparatory. , 1985, Annual review of neuroscience.

[42]  Rudolf Stark,et al.  The embodied nature of motor imagery: the influence of posture and perspective , 2009, Experimental Brain Research.

[43]  Kenneth F. Valyear,et al.  Human parietal cortex in action , 2006, Current Opinion in Neurobiology.

[44]  S. Holm A Simple Sequentially Rejective Multiple Test Procedure , 1979 .

[45]  M. Desmurget,et al.  Movement Intention After Parietal Cortex Stimulation in Humans , 2009, Science.

[46]  A. Baddeley,et al.  Working memory and the vividness of imagery. , 2000, Journal of experimental psychology. General.

[47]  Masato Taira,et al.  Motor cortical activity preceding a memorized movement trajectory with an orthogonal bend , 1993, Experimental Brain Research.

[48]  K. Amunts,et al.  Broca's region subserves imagery of motion: A combined cytoarchitectonic and fMRI study , 2000, Human brain mapping.

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

[50]  Y. Okamoto,et al.  Reduced activation of posterior cingulate cortex during imagery in subjects with high degrees of alexithymia: A functional magnetic resonance imaging study , 2005, Biological Psychiatry.

[51]  P Baraldi,et al.  Ipsilateral involvement of primary motor cortex during motor imagery , 2000, The European journal of neuroscience.

[52]  Leonardo Fogassi,et al.  Motor functions of the parietal lobe , 2005, Current Opinion in Neurobiology.

[53]  P. Dechent,et al.  Is the human primary motor cortex involved in motor imagery? , 2004, Brain research. Cognitive brain research.

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

[55]  Scott T. Grafton,et al.  Motor task difficulty and brain activity: investigation of goal-directed reciprocal aiming using positron emission tomography. , 1997, Journal of neurophysiology.

[56]  Julien Doyon,et al.  Functional neuroanatomical networks associated with expertise in motor imagery , 2008, NeuroImage.

[57]  Anne R. Isaac,et al.  Mental practice: Does it work in the field? , 1992 .

[58]  D. F. Marks,et al.  Individual differences in mental imagery experience: developmental changes and specialization. , 1994, British journal of psychology.

[59]  M. Lotze,et al.  Motor imagery training: Kinesthetic imagery strategy and inferior parietal fMRI activation , 2018, Human brain mapping.

[60]  Geraint Rees,et al.  Better Ways to Improve Standards in Brain-Behavior Correlation Analysis , 2012, Front. Hum. Neurosci..

[61]  S. Murphy Imagery interventions in sport. , 1994, Medicine and science in sports and exercise.

[62]  H. Nakata,et al.  Motor imagery beyond the motor repertoire: Activity in the primary visual cortex during kinesthetic motor imagery of difficult whole body movements , 2016, Neuroscience.

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

[64]  J. Kalaska,et al.  Cerebral cortical mechanisms of reaching movements. , 1992, Science.

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

[66]  Garrison W Cottrell,et al.  Observed, Executed, and Imagined Action Representations can be Decoded From Ventral and Dorsal Areas. , 2015, Cerebral cortex.

[67]  M. Diamond,et al.  Primary Motor and Sensory Cortex Activation during Motor Performance and Motor Imagery: A Functional Magnetic Resonance Imaging Study , 1996, The Journal of Neuroscience.

[68]  Rudolf Stark,et al.  Motor imagery of hand actions: Decoding the content of motor imagery from brain activity in frontal and parietal motor areas , 2015, Human brain mapping.

[69]  Jörn Diedrichsen,et al.  Reliability of dissimilarity measures for multi-voxel pattern analysis , 2016, NeuroImage.

[70]  Rudolf Stark,et al.  Imagined and Executed Actions in the Human Motor System: Testing Neural Similarity Between Execution and Imagery of Actions with a Multivariate Approach , 2016, Cerebral cortex.

[71]  G. Rizzolatti,et al.  Parietal cortex: from sight to action , 1997, Current Opinion in Neurobiology.

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

[73]  K. Zentgraf,et al.  Motor imagery and its implications for understanding the motor system. , 2009, Progress in brain research.

[74]  J. Mazziotta,et al.  Grasping the Intentions of Others with One's Own Mirror Neuron System , 2005, PLoS biology.

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

[76]  Brigitte Röder,et al.  Functional Rather than Effector-Specific Organization of Human Posterior Parietal Cortex , 2011, The Journal of Neuroscience.

[77]  M. Desmurget,et al.  A parietal-premotor network for movement intention and motor awareness , 2009, Trends in Cognitive Sciences.

[78]  Laehyun Kim,et al.  Which motor cortical region best predicts imagined movement? , 2015, NeuroImage.

[79]  M. Behrmann,et al.  Parietal cortex and attention , 2004, Current Opinion in Neurobiology.

[80]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

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

[82]  R. Andersen Visual and eye movement functions of the posterior parietal cortex. , 1989, Annual review of neuroscience.

[83]  Angela Sirigu,et al.  Body and movement: Consciousness in the parietal lobes , 2010, Neuropsychologia.

[84]  Dieter Vaitl,et al.  How equivalent are the action execution, imagery, and observation of intransitive movements? Revisiting the concept of somatotopy during action simulation , 2013, Brain and Cognition.