Hand Knob Area of Premotor Cortex Represents the Whole Body in a Compositional Way

Decades after the motor homunculus was first proposed, it is still unknown how different body parts are intermixed and interrelated in human motor cortical areas at single-neuron resolution. Using multi-unit recordings, we studied how face, head, arm, and leg movements are represented in the hand knob area of premotor cortex (precentral gyrus) in people with tetraplegia. Contrary to traditional expectations, we found strong representation of all movements and a partially "compositional" neural code that linked together all four limbs. The code consisted of (1) a limb-coding component representing the limb to be moved and (2) a movement-coding component where analogous movements from each limb (e.g., hand grasp and toe curl) were represented similarly. Compositional coding might facilitate skill transfer across limbs, and it provides a useful framework for thinking about how the motor system constructs movement. Finally, we leveraged these results to create a whole-body intracortical brain-computer interface that spreads targets across all limbs.

[1]  Haim Sompolinsky,et al.  Cortical Representation of Bimanual Movements , 2003, The Journal of Neuroscience.

[2]  Jörn Diedrichsen,et al.  Effector-Independent Motor Sequence Representations Exist in Extrinsic and Intrinsic Reference Frames , 2014, The Journal of Neuroscience.

[3]  Solaiman Shokur,et al.  A Brain-Machine Interface Enables Bimanual Arm Movements in Monkeys , 2013, Science Translational Medicine.

[4]  Kasey C. Soska,et al.  On the other hand: overflow movements of infants' hands and legs during unimanual object exploration. , 2012, Developmental psychobiology.

[5]  Martín Abadi,et al.  TensorFlow: Large-Scale Machine Learning on Heterogeneous Distributed Systems , 2016, ArXiv.

[6]  Susanne M. Morton,et al.  Asymmetric generalization between the arm and leg following prism-induced visuomotor adaptation , 2008, Experimental Brain Research.

[7]  K. Zilles,et al.  Functional neuroanatomy of the primate isocortical motor system , 2000, Anatomy and Embryology.

[8]  Angela R. Laird,et al.  The heterogeneity of the left dorsal premotor cortex evidenced by multimodal connectivity-based parcellation and functional characterization , 2017, NeuroImage.

[9]  K. Kurata,et al.  Distribution of neurons with set- and movement-related activity before hand and foot movements in the premotor cortex of rhesus monkeys , 2004, Experimental Brain Research.

[10]  A. Schwartz,et al.  High-performance neuroprosthetic control by an individual with tetraplegia , 2013, The Lancet.

[11]  Stephen H Scott,et al.  Limited transfer of learning between unimanual and bimanual skills within the same limb , 2006, Nature Neuroscience.

[12]  Jimmy Ba,et al.  Adam: A Method for Stochastic Optimization , 2014, ICLR.

[13]  Mark L. Latash,et al.  Mirror Writing: Learning, Transfer, and Implications for Internal Inverse Models. , 1999, Journal of motor behavior.

[14]  Tianzi Jiang,et al.  The Right Dorsal Premotor Mosaic: Organization, Functions, and Connectivity , 2016, Cerebral cortex.

[15]  Nicholas P. Szrama,et al.  Unilateral, 3D Arm Movement Kinematics Are Encoded in Ipsilateral Human Cortex , 2018, The Journal of Neuroscience.

[16]  A. Schleicher,et al.  Mapping of human and macaque sensorimotor areas by integrating architectonic, transmitter receptor, MRI and PET data. , 1995, Journal of anatomy.

[17]  Rajesh P. N. Rao,et al.  Spectral Changes in Cortical Surface Potentials during Motor Movement , 2007, The Journal of Neuroscience.

[18]  M. Erb,et al.  fMRI Evaluation of Somatotopic Representation in Human Primary Motor Cortex , 2000, NeuroImage.

[19]  Evangelos A Christou,et al.  Time but not Force Is Transferred Between Ipsilateral Upper and Lower Limbs , 2008, Journal of motor behavior.

[20]  Dragan F. Dimitrov,et al.  Cortical Representation of Ipsilateral Arm Movements in Monkey and Man , 2009, The Journal of Neuroscience.

[21]  Joe Whittaker,et al.  Application of the Parametric Bootstrap to Models that Incorporate a Singular Value Decomposition , 1995 .

[22]  John-Dylan Haynes,et al.  Searchlight-based multi-voxel pattern analysis of fMRI by cross-validated MANOVA , 2014, NeuroImage.

[23]  Mark M Churchland,et al.  Motor cortex signals for each arm are mixed across hemispheres and neurons yet partitioned within the population response , 2019, eLife.

[24]  Nasser M. Nasrabadi,et al.  Pattern Recognition and Machine Learning , 2006, Technometrics.

[25]  M. Schieber Constraints on somatotopic organization in the primary motor cortex. , 2001, Journal of neurophysiology.

[26]  A. Schleicher,et al.  Two different areas within the primary motor cortex of man , 1996, Nature.

[27]  Rieko Osu,et al.  Neural pattern similarity between contra- and ipsilateral movements in high-frequency band of human electrocorticograms , 2017, NeuroImage.

[28]  João A. Carriço,et al.  Evaluation of Jackknife and Bootstrap for Defining Confidence Intervals for Pairwise Agreement Measures , 2011, PloS one.

[29]  Dr. Stefan Geyer The Microstructural Border Between the Motor and the Cognitive Domain in the Human Cerebral Cortex , 2004, Advances in Anatomy Embryology and Cell Biology.

[30]  W. Craelius,et al.  Inter-limb transfer of learned ankle movements , 2008, Experimental Brain Research.

[31]  S. Kastner,et al.  Complex organization of human primary motor cortex: a high-resolution fMRI study. , 2008, Journal of neurophysiology.

[32]  Francis R. Willett,et al.  Restoration of reaching and grasping in a person with tetraplegia through brain-controlled muscle stimulation: a proof-of-concept demonstration , 2017, The Lancet.

[33]  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.

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

[35]  Nicholas V. Annetta,et al.  Restoring cortical control of functional movement in a human with quadriplegia , 2016, Nature.

[36]  Jörn Diedrichsen,et al.  Two Distinct Ipsilateral Cortical Representations for Individuated Finger Movements , 2012, Cerebral cortex.

[37]  J. Rademacher,et al.  Variability and asymmetry in the human precentral motor system. A cytoarchitectonic and myeloarchitectonic brain mapping study. , 2001, Brain : a journal of neurology.

[38]  Xiaoxiang Zheng,et al.  Electrocorticographic signals comparison in sensorimotor cortex between contralateral and ipsilateral hand movements , 2016, 2016 38th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[39]  Jörn Diedrichsen,et al.  Representational models: A common framework for understanding encoding, pattern-component, and representational-similarity analysis , 2017, bioRxiv.

[40]  Stefan Panzer,et al.  The Coding and Inter-Manual Transfer of Movement Sequences , 2011, Front. Psychology.

[41]  Stephen H Scott,et al.  Independent representations of ipsilateral and contralateral limbs in primary motor cortex , 2019, eLife.

[42]  James C. Houk,et al.  Cerebellar learning for control of a two-link arm in muscle space , 1997, Proceedings of International Conference on Robotics and Automation.

[43]  Pier-Giorgio Zanone,et al.  Coordination dynamics of learning and transfer across different effector systems. , 2002, Journal of experimental psychology. Human perception and performance.

[44]  J. Kaas,et al.  Reorganization of primary motor cortex in adult macaque monkeys with long-standing amputations. , 2000, Journal of neurophysiology.

[45]  C. Sherrington,et al.  OBSERVATIONS ON THE EXCITABLE CORTEX OF THE CHIMPANZEE, ORANG‐UTAN, AND GORILLA , 1917 .

[46]  L. White,et al.  Structure of the human sensorimotor system. I: Morphology and cytoarchitecture of the central sulcus. , 1997, Cerebral cortex.

[47]  W. Penfield,et al.  SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION , 1937 .

[48]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. , 1998, Brain : a journal of neurology.

[50]  Nicolas Y. Masse,et al.  Virtual typing by people with tetraplegia using a self-calibrating intracortical brain-computer interface , 2015, Science Translational Medicine.

[51]  Stephen I. Ryu,et al.  A High-Performance Keyboard Neural Prosthesis Enabled by Task Optimization , 2015, IEEE Transactions on Biomedical Engineering.

[52]  Xiao-Jing Wang,et al.  Task representations in neural networks trained to perform many cognitive tasks , 2019, Nature Neuroscience.

[53]  M. Kawato,et al.  Formation and control of optimal trajectory in human multijoint arm movement , 1989, Biological Cybernetics.

[54]  L. White,et al.  Structure of the human sensorimotor system. II: Lateral symmetry. , 1997, Cerebral cortex.

[55]  H. Alkadhi,et al.  Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. , 1997, Brain : a journal of neurology.

[56]  John L. Bradshaw,et al.  Investigating the cortical origins of motor overflow , 2004, Brain Research Reviews.

[57]  Johanna Ruescher,et al.  Somatotopic mapping of natural upper- and lower-extremity movements and speech production with high gamma electrocorticography , 2013, NeuroImage.

[58]  J. Diedrichsen,et al.  Restricted transfer of learning between unimanual and bimanual finger sequences. , 2017, Journal of neurophysiology.

[59]  John-Dylan Haynes,et al.  Compositionality of rule representations in human prefrontal cortex. , 2012, Cerebral cortex.

[60]  Nicolas Y. Masse,et al.  Reach and grasp by people with tetraplegia using a neurally controlled robotic arm , 2012, Nature.

[61]  K. Brodmann Vergleichende Lokalisationslehre der Großhirnrinde : in ihren Prinzipien dargestellt auf Grund des Zellenbaues , 1985 .

[62]  Byron M. Yu,et al.  A high-performance brain–computer interface , 2006, Nature.

[63]  I. Kaufman The Cerebral Cortex of Man: A Clinical Study of Localization of Function , 1951 .

[64]  R. Andersen,et al.  Partially Mixed Selectivity in Human Posterior Parietal Association Cortex , 2017, Neuron.

[65]  Francis R. Willett,et al.  High performance communication by people with paralysis using an intracortical brain-computer interface , 2017, eLife.

[66]  W. Penfield,et al.  The Cerebral Cortex of Man: A Clinical Study of Localization of Function , 1968 .

[67]  Paul Cisek,et al.  Neural activity in primary motor and dorsal premotor cortex in reaching tasks with the contralateral versus ipsilateral arm. , 2003, Journal of neurophysiology.

[68]  Jon A. Mukand,et al.  Neuronal ensemble control of prosthetic devices by a human with tetraplegia , 2006, Nature.

[69]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. , 1998, Brain : a journal of neurology.

[70]  R. Andersen,et al.  Cognitive Control Signals for Neural Prosthetics , 2004, Science.

[71]  Krishna V. Shenoy,et al.  Accurate Estimation of Neural Population Dynamics without Spike Sorting , 2019, Neuron.

[72]  G. Rizzolatti,et al.  The organization of the cortical motor system: new concepts. , 1998, Electroencephalography and clinical neurophysiology.

[73]  A. Galaburda,et al.  Topographical variation of the human primary cortices: implications for neuroimaging, brain mapping, and neurobiology. , 1993, Cerebral cortex.

[74]  Reza Shadmehr,et al.  Learned dynamics of reaching movements generalize from dominant to nondominant arm. , 2003, Journal of neurophysiology.