Critical Motor Involvement in Prediction of Human and Non-biological Motion Trajectories

Abstract Objectives: Adaptive interaction with the environment requires the ability to predict both human and non-biological motion trajectories. Prior accounts of the neurocognitive basis for prediction of these two motion classes may generally be divided into those that posit that non-biological motion trajectories are predicted using the same motor planning and/or simulation mechanisms used for human actions, and those that posit distinct mechanisms for each. Using brain lesion patients and healthy controls, this study examined critical neural substrates and behavioral correlates of human and non-biological motion prediction. Methods: Twenty-seven left hemisphere stroke patients and 13 neurologically intact controls performed a visual occlusion task requiring prediction of pantomimed tool use, real tool use, and non-biological motion videos. Patients were also assessed with measures of motor strength and speed, praxis, and action recognition. Results: Prediction impairment for both human and non-biological motion was associated with limb apraxia and, weakly, with the severity of motor production deficits, but not with action recognition ability. Furthermore, impairment for human and non-biological motion prediction was equivalently associated with lesions in the left inferior parietal cortex, left dorsal frontal cortex, and the left insula. Conclusions: These data suggest that motor planning mechanisms associated with specific loci in the sensorimotor network are critical for prediction of spatiotemporal trajectory information characteristic of both human and non-biological motions. (JINS, 2017, 23, 171–184)

[1]  R. Passingham,et al.  Action observation and acquired motor skills: an FMRI study with expert dancers. , 2005, Cerebral cortex.

[2]  Cosimo Urgesi,et al.  Neuroanatomical substrates of action perception and understanding: an anatomic likelihood estimation meta-analysis of lesion-symptom mapping studies in brain injured patients , 2014, Front. Hum. Neurosci..

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

[4]  John Whyte,et al.  A patient registry for cognitive rehabilitation research: a strategy for balancing patients' privacy rights with researchers' need for access. , 2005, Archives of physical medicine and rehabilitation.

[5]  Mark Hallett,et al.  Left parietal activation related to planning, executing and suppressing praxis hand movements , 2009, Clinical Neurophysiology.

[6]  Anne Springer,et al.  Dynamic Simulation and Static Matching for Action Prediction: Evidence From Body Part Priming , 2013, Cogn. Sci..

[7]  M. Jeannerod The formation of finger grip during prehension. A cortically mediated visuomotor pattern , 1986, Behavioural Brain Research.

[8]  Laurel J. Buxbaum,et al.  Deficits in Movement Planning and Intrinsic Coordinate Control in Ideomotor Apraxia , 2006, Journal of Cognitive Neuroscience.

[9]  Anne Springer,et al.  Repetitive TMS Suggests a Role of the Human Dorsal Premotor Cortex in Action Prediction , 2012, Front. Hum. Neurosci..

[10]  Susan V. Duff,et al.  The impact of left hemisphere stroke on force control with familiar and novel objects: Neuroanatomic substrates and relationship to apraxia , 2010, Brain Research.

[11]  J. Parkinson,et al.  Movement kinematics affect action prediction: comparing human to non-human point-light actions , 2012, Psychological Research.

[12]  Scott H. Johnson,et al.  Imagining the impossible: intact motor representations in hemiplegics , 2000, Neuroreport.

[13]  S. Tipper,et al.  Spatiotemporal judgments of observed actions: Contrasts between first- and third-person perspectives after motor priming. , 2015, Journal of experimental psychology. Human perception and performance.

[14]  Lincoln J. Colling,et al.  The effect of movement kinematics on predicting the timing of observed actions , 2014, Experimental Brain Research.

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

[16]  D. Tranel,et al.  Behavioral patterns and lesion sites associated with impaired processing of lexical and conceptual knowledge of actions , 2012, Cortex.

[17]  Elizabeth A. Hirshorn,et al.  Localizing interference during naming: Convergent neuroimaging and neuropsychological evidence for the function of Broca's area , 2009, Proceedings of the National Academy of Sciences.

[18]  Shinichi Nakagawa,et al.  A general and simple method for obtaining R2 from generalized linear mixed‐effects models , 2013 .

[19]  Janny C. Stapel,et al.  Motor system contribution to action prediction: Temporal accuracy depends on motor experience , 2016, Cognition.

[20]  Alfonso Caramazza,et al.  Embodied cognition and mirror neurons: a critical assessment. , 2014, Annual review of neuroscience.

[21]  Rainer Goebel,et al.  How Skill Expertise Shapes the Brain Functional Architecture: An fMRI Study of Visuo-Spatial and Motor Processing in Professional Racing-Car and Naïve Drivers , 2013, PloS one.

[22]  Donatella Spinelli,et al.  Spatiotemporal brain mapping during preparation, perception, and action , 2016, NeuroImage.

[23]  Alan C. Evans,et al.  Enhancement of MR Images Using Registration for Signal Averaging , 1998, Journal of Computer Assisted Tomography.

[24]  Michael Brady,et al.  Enhancement of MR Images , 1996, VBC.

[25]  L. Buxbaum,et al.  On beyond mirror neurons: internal representations subserving imitation and recognition of skilled object-related actions in humans. , 2005, Brain research. Cognitive brain research.

[26]  Brian B. Avants,et al.  Lagrangian frame diffeomorphic image registration: Morphometric comparison of human and chimpanzee cortex , 2006, Medical Image Anal..

[27]  Mårten Risling,et al.  Blast Induced Brain Injuries – A Grand Challenge in TBI Research , 2010, Front. Neur..

[28]  Lesley K. Fellows,et al.  Method Matters: An Empirical Study of Impact in Cognitive Neuroscience , 2005, Journal of Cognitive Neuroscience.

[29]  C. Urgesi,et al.  Action anticipation and motor resonance in elite basketball players , 2008, Nature Neuroscience.

[30]  Emily S. Cross,et al.  The influence of visual training on predicting complex action sequences , 2013, Human brain mapping.

[31]  D. Pandya,et al.  Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. , 2005, Cerebral cortex.

[32]  Jie Yang The influence of motor expertise on the brain activity of motor task performance: A meta-analysis of functional magnetic resonance imaging studies , 2015, Cognitive, affective & behavioral neuroscience.

[33]  Alfonso Caramazza,et al.  What is the role of motor simulation in action and object recognition? Evidence from apraxia , 2007, Cognitive neuropsychology.

[34]  D. Pandya,et al.  Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. , 2007, Brain : a journal of neurology.

[35]  Michael I. Jordan,et al.  An internal model for sensorimotor integration. , 1995, Science.

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

[37]  Harold Bekkering,et al.  Neural Evidence for Compromised Motor Imagery in Right Hemiparetic Cerebral Palsy , 2010, Front. Neur..

[38]  Paul C. Johnson Extension of Nakagawa & Schielzeth's R2GLMM to random slopes models , 2014, Methods in ecology and evolution.

[39]  Michiel van Elk,et al.  The left inferior parietal lobe represents stored hand-postures for object use and action prediction , 2014, Front. Psychol..

[40]  Steven L. Bressler,et al.  Past Makes Future: Role of pFC in Prediction , 2015, Journal of Cognitive Neuroscience.

[41]  Anne Springer,et al.  Action Semantics Modulate Action Prediction , 2010, Quarterly journal of experimental psychology.

[42]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

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

[44]  Pratik K. Mutha,et al.  Coordination deficits in ideomotor apraxia during visually targeted reaching reflect impaired visuomotor transformations , 2010, Neuropsychologia.

[45]  Axel Lindner,et al.  The Cerebellum Optimizes Perceptual Predictions about External Sensory Events , 2013, Current Biology.

[46]  S. H. Johnson,et al.  Intact Motor Imagery in Chronic Upper Limb Hemiplegics: Evidence for Activity-Independent Action Representations , 2002, Journal of Cognitive Neuroscience.

[47]  Lawrence W Barsalou,et al.  Simulation, situated conceptualization, and prediction , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[48]  Ricarda I. Schubotz,et al.  Prediction, Cognition and the Brain , 2009, Front. Hum. Neurosci..

[49]  Ben Pelzer,et al.  influence.ME: Tools for Detecting Influential Data in Mixed Effects Models , 2012, R J..

[50]  Desmond E. Mulligan,et al.  An action-incongruent secondary task modulates prediction accuracy in experienced performers: evidence for motor simulation , 2016, Psychological research.

[51]  Rudolf Stark,et al.  Prediction of human actions: Expertise and task‐related effects on neural activation of the action observation network , 2014, Human brain mapping.

[52]  R. Schubotz Prediction of external events with our motor system: towards a new framework , 2007, Trends in Cognitive Sciences.

[53]  J. Hermsdörfer,et al.  The impact of unilateral brain damage on anticipatory grip force scaling when lifting everyday objects , 2014, Neuropsychologia.

[54]  G. Knoblich,et al.  Predicting the Effects of Actions: Interactions of Perception and Action , 2001, Psychological science.

[55]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[56]  Wolfgang Prinz,et al.  Predicting point-light actions in real-time , 2007, NeuroImage.

[57]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[58]  D Yves von Cramon,et al.  Motor areas beyond motor performance: deficits in serial prediction following ventrolateral premotor lesions. , 2004, Neuropsychology.

[59]  A. Caramazza,et al.  Typical action perception and interpretation without motor simulation , 2015, Proceedings of the National Academy of Sciences.

[60]  Daniel Mirman,et al.  The Neural Basis of Inhibitory Effects of Semantic and Phonological Neighbors in Spoken Word Production , 2013, Journal of Cognitive Neuroscience.

[61]  Ekaterina P. Volkova,et al.  Emotion categorization of body expressions in narrative scenarios , 2014, Front. Psychol..

[62]  G. Rizzolatti,et al.  Neurophysiological mechanisms underlying the understanding and imitation of action , 2001, Nature Reviews Neuroscience.

[63]  K. Doya,et al.  A unifying computational framework for motor control and social interaction. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[64]  Karl J. Friston,et al.  Action understanding and active inference , 2011, Biological Cybernetics.

[65]  J. Hermsdörfer,et al.  Size–weight illusion and anticipatory grip force scaling following unilateral cortical brain lesion , 2011, Neuropsychologia.

[66]  Laurel J. Buxbaum,et al.  Accurate Reaching after Active But Not Passive Movements of the Hand: Evidence for Forward Modeling , 2008, Behavioural neurology.

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

[68]  M. Nour Surfing Uncertainty: Prediction, Action, and the Embodied Mind. , 2017, British Journal of Psychiatry.

[69]  Anne Springer,et al.  Predicting and memorizing observed action: Differential premotor cortex involvement , 2011, Human brain mapping.

[70]  D. V. Cramon,et al.  Predicting Perceptual Events Activates Corresponding Motor Schemes in Lateral Premotor Cortex: An fMRI Study , 2002, NeuroImage.

[71]  Cathy Craig,et al.  Using Time-to-Contact Information to Assess Potential Collision Modulates Both Visual and Temporal Prediction Networks , 2008, Frontiers in human neuroscience.

[72]  G. Csibra Action mirroring and action understanding: an alternative account , 1993 .

[73]  D. Bates,et al.  Parsimonious Mixed Models , 2015, 1506.04967.

[74]  Martin Wiener,et al.  Implicit timing activates the left inferior parietal cortex , 2010, Neuropsychologia.

[75]  Cosimo Urgesi,et al.  Neural underpinnings of superior action prediction abilities in soccer players. , 2015, Social cognitive and affective neuroscience.

[76]  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.

[77]  Y Agid,et al.  Congruent unilateral impairments for real and imagined hand movements , 1995, Neuroreport.

[78]  K. Heilman,et al.  Selective deficit of praxis imagery in ideomotor apraxia , 1997, Neurology.

[79]  M. Pickering,et al.  An integrated theory of language production and comprehension. , 2013, The Behavioral and brain sciences.