Movement imitation depends on an abstract trajectory representation in dorsal premotor cortex

Humans are particularly good at copying novel and meaningless gestures. The mechanistic and anatomical basis for this specialized imitation ability remains largely unknown. One idea is that imitation depends on a representation of the relative configurations of body parts (body schema). Here we propose an alternative route to imitation that depends on an abstract representation of the trajectory path of the end-effector. We studied a group of patients with strokes that encompassed the left premotor and posterior parietal cortices. We found that they were equally impaired at imitating movement trajectories using the ipsilateral limb (i.e., the non-paretic side) that were cued either by an actor using their whole arm or just by a cursor, suggesting that body configuration is not always critical for imitation and that a representation of abstract trajectory shape may suffice. In addition, imitation ability was uncorrelated to the ability to identify the trajectory shape, suggesting a dissociation between producing trajectory shapes and perceiving their paths. Finally, a lesion-symptom mapping analysis found that imitation deficits were associated with lesions in left dorsal premotor but not parietal cortex. Together, these findings suggest a novel body-independent route to imitation that relies on the ability to plan abstract movement paths within dorsal premotor cortex.

[1]  G. Goldenberg,et al.  The meaning of meaningless gestures: A study of visuo-imitative apraxia , 1997, Neuropsychologia.

[2]  E. Tulving Ecphoric processes in recall and recognition. , 1976 .

[3]  B. R. Moore Avian Movement Imitation and a New Form of Mimicry: Tracing the Evolution of a Complex Form of Learning , 1992 .

[4]  Jules Davidoff,et al.  A particular difficulty in discriminating between mirror images , 2001, Neuropsychologia.

[5]  F. Dick,et al.  Voxel-based lesion–symptom mapping , 2003, Nature Neuroscience.

[6]  A. Meltzoff,et al.  An fMRI study of imitation: action representation and body schema , 2005, Neuropsychologia.

[7]  Cornelius Weiller,et al.  Neural bases of imitation and pantomime in acute stroke patients: distinct streams for praxis. , 2014, Brain : a journal of neurology.

[8]  Aina Puce,et al.  Viewing the motion of human body parts activates different regions of premotor, temporal, and parietal cortex , 2004, NeuroImage.

[9]  Francys Subiaul,et al.  What’s Special about Human Imitation? A Comparison with Enculturated Apes , 2016, Behavioral sciences.

[10]  A. V. Kurganskii,et al.  Internal Representation of Movement Sequences on Reproduction of Static Drawings and the Trajectories of Moving Objects , 2014, Neuroscience and Behavioral Physiology.

[11]  J. Mattingley,et al.  Is the mirror neuron system involved in imitation? A short review and meta-analysis , 2009, Neuroscience & Biobehavioral Reviews.

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

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

[14]  K. Heilman,et al.  Hemispheric Specialization for Handwriting in Right Handers , 1993, Brain and Cognition.

[15]  L. Buxbaum,et al.  Critical brain regions for tool-related and imitative actions: a componential analysis. , 2014, Brain : a journal of neurology.

[16]  Gerard P. van Galen,et al.  The independent monitoring of form and scale factors in handwriting , 1983 .

[17]  Rieko Osu,et al.  Quantifying the quality of hand movement in stroke patients through three-dimensional curvature , 2011, Journal of NeuroEngineering and Rehabilitation.

[18]  Brice Isableu,et al.  Embodied spatial transformations: "body analogy" for the mental rotation of objects. , 2006, Journal of experimental psychology. General.

[19]  T. Flash,et al.  The coordination of arm movements: an experimentally confirmed mathematical model , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  S. Wise,et al.  Effects of hand movement path on motor cortical activity in awake, behaving rhesus monkeys , 2004, Experimental Brain Research.

[21]  Donald A. Norman,et al.  Models Of Human Memory , 1970 .

[22]  A. G. Feldman,et al.  Interjoint coordination dynamics during reaching in stroke , 2003, Experimental Brain Research.

[23]  P. Nardi Critical , 2018, Theoretical Models and Processes of Literacy.

[24]  T. Flash,et al.  Scale-Invariant Movement Encoding in the Human Motor System , 2014, Neuron.

[25]  John Brown,et al.  Recall and Recognition , 1976 .

[26]  Laurel J. Buxbaum,et al.  Critical Motor Involvement in Prediction of Human and Non-biological Motion Trajectories , 2017, Journal of the International Neuropsychological Society.

[27]  Andrew T DeMarco,et al.  A multivariate lesion symptom mapping toolbox and examination of lesion‐volume biases and correction methods in lesion‐symptom mapping , 2018, Human brain mapping.

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

[29]  Laurel J. Buxbaum,et al.  Deficient internal models for planning hand–object interactions in apraxia , 2005, Neuropsychologia.

[30]  John R. Anderson,et al.  RECOGNITION AND RETRIEVAL PROCESSES IN FREE RECALL , 1972 .

[31]  Christopher A. Buneo,et al.  Neural correlates of learning and trajectory planning in the posterior parietal cortex , 2013, Front. Integr. Neurosci..

[32]  J Hermsdörfer,et al.  Kinematic analysis of movement imitation in apraxia. , 1996, Brain : a journal of neurology.

[33]  John W Krakauer,et al.  A motor planning stage represents the shape of upcoming movement trajectories. , 2016, Journal of neurophysiology.

[34]  J P Dewald,et al.  Upper-Limb Discoordination in Hemiparetic Stroke: Implications for Neurorehabilitation , 2001, Topics in stroke rehabilitation.

[35]  Kenneth M. Heilman,et al.  Apraxia : The Neuropsychology of Action , 2014 .

[36]  A. Kertesz The Western Aphasia Battery , 1982 .

[37]  M. Schwartz,et al.  Multivariate lesion‐symptom mapping using support vector regression , 2014, Human brain mapping.

[38]  Stephen H. Scott,et al.  Hand and joint paths during reaching movements with and without vision , 1998, Experimental Brain Research.

[39]  M. Matarić,et al.  Fixation behavior in observation and imitation of human movement. , 1998, Brain research. Cognitive brain research.

[40]  S. Wise,et al.  Trajectory-selective neuronal activity in the motor cortex of rhesus monkeys (Macaca mulatta). , 1990, Behavioral neuroscience.

[41]  M. Petrides,et al.  Neural correlates of mental transformations of the body-in-space. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Laurel J. Buxbaum,et al.  Representations of the human body in the production and imitation of complex movements , 2004, Cognitive neuropsychology.

[43]  Murray Grossman,et al.  Left Inferior Parietal Representations for Skilled Hand-Object Interactions: Evidence from Stroke and Corticobasal Degeneration , 2007, Cortex.

[44]  H. Kuypers,et al.  Premotor cortical ablations in monkeys: contralateral changes in visually guided reaching behavior. , 1977, Science.

[45]  Christine E. Watson,et al.  Shared and Distinct Neuroanatomic Regions Critical for Tool-related Action Production and Recognition: Evidence from 131 Left-hemisphere Stroke Patients , 2015, Journal of Cognitive Neuroscience.

[46]  Daeyeol Lee,et al.  Activity in prefrontal cortex during dynamic selection of action sequences , 2006, Nature Neuroscience.

[47]  R. Mansfield,et al.  Analysis of visual behavior , 1982 .

[48]  Anjali Krishnan,et al.  Cluster-extent based thresholding in fMRI analyses: Pitfalls and recommendations , 2014, NeuroImage.

[49]  C. Goodall Procrustes methods in the statistical analysis of shape , 1991 .

[50]  Laurel J Buxbaum,et al.  Critical brain regions for action recognition: lesion symptom mapping in left hemisphere stroke. , 2010, Brain : a journal of neurology.

[51]  John W. Krakauer,et al.  Motor Planning , 2015, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[52]  John W. Krakauer,et al.  Broken Movement: The Neurobiology of Motor Recovery after Stroke , 2017 .

[53]  N. Geschwind The apraxias: neural mechanisms of disorders of learned movement. , 1975, American scientist.

[54]  Gregor Schöner,et al.  Goal-equivalent joint coordination in pointing: affect of vision and arm dominance. , 2002, Motor control.

[55]  A. Murata,et al.  Natural imitation induced by joint attention in Japanese monkeys. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[56]  Jeffrey M. Zacks,et al.  Neuroimaging Studies of Mental Rotation: A Meta-analysis and Review , 2008, Journal of Cognitive Neuroscience.

[57]  Ezequiel Morsella,et al.  Oxford Handbook of Human Action , 2009 .

[58]  P. H. Weiss,et al.  Motor impairment in patients with parietal lesions: disturbances of meaningless arm movement sequences , 2001, Neuropsychologia.

[59]  D. F. Fisher,et al.  Eye movements : cognition and visual perception , 1982 .

[60]  Daniel W Moran,et al.  Strategy-Dependent Encoding of Planned Arm Movements in the Dorsal Premotor Cortex , 2012, Science.

[61]  Gereon R. Fink,et al.  Common and Differential Neural Mechanisms Supporting Imitation of Meaningful and Meaningless Actions , 2005, Journal of Cognitive Neuroscience.

[62]  G. Goldenberg Apraxia – The cognitive side of motor control , 2013, Cortex.

[63]  A. Schwartz,et al.  Motor cortical activity during drawing movements: population representation during spiral tracing. , 1999, Journal of neurophysiology.

[64]  Sharon L. Thompson-Schill,et al.  Conceptual Representations of Action in the Lateral Temporal Cortex , 2005, Journal of Cognitive Neuroscience.

[65]  Stephen H Scott,et al.  Apparent and Actual Trajectory Control Depend on the Behavioral Context in Upper Limb Motor Tasks , 2015, The Journal of Neuroscience.

[66]  L. Buxbaum,et al.  The Role of the Dynamic Body Schema in Praxis: Evidence from Primary Progressive Apraxia , 2000, Brain and Cognition.

[67]  David P. Carey,et al.  Tapping, grasping and aiming in ideomotor apraxia , 2006, Neuropsychologia.

[68]  A B Schwartz,et al.  Direct cortical representation of drawing. , 1994, Science.

[69]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

[70]  Walter Kintsch,et al.  11 – Models for Free Recall and Recognition1 , 1970 .

[71]  G. Goldenberg Matching and imitation of hand and finger posturesin patients with damage in the left or right hemispheres , 1999, Neuropsychologia.

[72]  Charles E. Wright,et al.  Generalized Motor Programs: Reexamining Claims of Effector Independence in Writing , 2018, Attention and Performance XIII.

[73]  Y. Amit,et al.  Encoding of Movement Fragments in the Motor Cortex , 2007, The Journal of Neuroscience.

[74]  Georg Goldenberg,et al.  Imitating gestures and manipulating a mannikin—The representation of the human body in ideomotor apraxia , 1995, Neuropsychologia.

[75]  A. Wing,et al.  Motor control: Mechanisms of motor equivalence in handwriting , 2000, Current Biology.

[76]  E. Bizzi,et al.  Human arm trajectory formation. , 1982, Brain : a journal of neurology.

[77]  A. Lindner,et al.  How will it look like? Human posterior parietal and dorsal premotor cortex encode the visual properties of an upcoming action , 2018, bioRxiv.

[78]  Richard B. Ivry,et al.  The persistence of spatial interference after extended training in a bimanual drawing task , 2009, Cortex.

[79]  Gordon Cheng,et al.  Discovering optimal imitation strategies , 2004, Robotics Auton. Syst..

[80]  Jun Nakanishi,et al.  Trajectory formation for imitation with nonlinear dynamical systems , 2001, Proceedings 2001 IEEE/RSJ International Conference on Intelligent Robots and Systems. Expanding the Societal Role of Robotics in the the Next Millennium (Cat. No.01CH37180).

[81]  B. Milner,et al.  Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man , 1982, Neuropsychologia.

[82]  A. Whiten,et al.  How do apes ape? , 2004, Learning & behavior.

[83]  Harry Levi Hollingworth,et al.  Characteristic differences between recall and recognition. , 1913 .

[84]  Richard S. J. Frackowiak,et al.  A Blueprint for Movement: Functional and Anatomical Representations in the Human Motor System , 1999, The Journal of Neuroscience.

[85]  Angela R. Laird,et al.  ALE meta-analysis of action observation and imitation in the human brain , 2010, NeuroImage.

[86]  G. Rees,et al.  Human brain lesion-deficit inference remapped , 2014, Brain : a journal of neurology.

[87]  G. Rizzolatti,et al.  Neural Circuits Involved in the Recognition of Actions Performed by Nonconspecifics: An fMRI Study , 2004, Journal of Cognitive Neuroscience.