Movement Imitation via 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 occurs by matching body configurations. Here we propose an alternative route to imitation that depends on a body-independent representation of the trajectory path of the end-effector. We studied a group of patients with strokes in the left frontoparietal cortices. We found that they were equally impaired at imitating movement trajectories using the ipsilesional limb (i.e., the nonparetic side) that were cued either by an actor using their whole arm or just by a cursor, suggesting that body configuration information 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 that imitation deficits were unlikely to arise from perceptual impairments. 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 trajectories within dorsal premotor cortex. SIGNIFICANCE STATEMENT The ability to imitate is critical for rapidly learning to produce new gestures and actions, but how the brain translates observed movements into motor commands is poorly understood. Examining the ability of patients with strokes affecting the left hemisphere revealed that meaningless gestures can be imitated by succinctly representing only the motion of the hand in space, rather than the posture of the entire arm. Moreover, performance deficits correlated with lesions in dorsal premotor cortex, an area not previously associated with impaired imitation of arm postures. These findings thus describe a novel route to imitation that may also be impaired in some patients with apraxia.

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

[2]  Hans-Otto Karnath,et al.  An empirical evaluation of multivariate lesion behaviour mapping using support vector regression , 2018, bioRxiv.

[3]  A. Lindner,et al.  Human posterior parietal and dorsal premotor cortex encode the visual properties of an upcoming action , 2018, PloS one.

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

[5]  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.

[6]  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.

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

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

[9]  Daniel Mirman,et al.  Corrections for multiple comparisons in voxel-based lesion-symptom mapping , 2016, Neuropsychologia.

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

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

[12]  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.

[13]  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.

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

[15]  Christine E. Watson,et al.  A distributed network critical for selecting among tool-directed actions , 2015, Cortex.

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

[17]  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.

[18]  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.

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

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

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

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

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

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

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

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

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

[28]  L. Buxbaum,et al.  Dissociations of action means and outcome processing in left-hemisphere stroke , 2013, Neuropsychologia.

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

[49]  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.

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

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

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

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

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

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

[56]  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).

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

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

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

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

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

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

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

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

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

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

[67]  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.

[68]  K. Mauritz,et al.  Human Motor Planning, Motor Programming, and Use of New Task‐relevant Information with Different Apraxic Syndromes , 1995, The European journal of neuroscience.

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

[70]  Christine M. Johnson,et al.  Trained Motor Imitation by Bottlenose Dolphins (Tursiops Truncatus) , 1994, Perceptual and motor skills.

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

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

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

[74]  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.

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

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

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

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

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

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

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

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

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

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

[85]  Lyn S. Turkstra,et al.  Western Aphasia Battery , 2018 .

[86]  Andrea Bergmann,et al.  Statistical Parametric Mapping The Analysis Of Functional Brain Images , 2016 .

[87]  P. Eling Apraxia: The cognitive side of motor control , 2014 .

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

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

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

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

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

[93]  M. Goodale,et al.  The visual brain in action , 1995 .

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

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

[96]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

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

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

[99]  C. K. Tayler,et al.  Imitative Behaviour By Indian Ocean Bottlenose Dolphins (t uRsiops Aduncus) in Captivity , 1973 .

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

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