Robust tactile sensory responses in finger area of primate motor cortex relevant to prosthetic control

OBJECTIVE Challenges in improving the performance of dexterous upper-limb brain-machine interfaces (BMIs) have prompted renewed interest in quantifying the amount and type of sensory information naturally encoded in the primary motor cortex (M1). Previous single unit studies in monkeys showed M1 is responsive to tactile stimulation, as well as passive and active movement of the limbs. However, recent work in this area has focused primarily on proprioception. Here we examined instead how tactile somatosensation of the hand and fingers is represented in M1. APPROACH We recorded multi- and single units and thresholded neural activity from macaque M1 while gently brushing individual finger pads at 2 Hz. We also recorded broadband neural activity from electrocorticogram (ECoG) grids placed on human motor cortex, while applying the same tactile stimulus. MAIN RESULTS Units displaying significant differences in firing rates between individual fingers (p  <  0.05) represented up to 76.7% of sorted multiunits across four monkeys. After normalizing by the number of channels with significant motor finger responses, the percentage of electrodes with significant tactile responses was 74.9%  ±  24.7%. No somatotopic organization of finger preference was obvious across cortex, but many units exhibited cosine-like tuning across multiple digits. Sufficient sensory information was present in M1 to correctly decode stimulus position from multiunit activity above chance levels in all monkeys, and also from ECoG gamma power in two human subjects. SIGNIFICANCE These results provide some explanation for difficulties experienced by motor decoders in clinical trials of cortically controlled prosthetic hands, as well as the general problem of disentangling motor and sensory signals in primate motor cortex during dextrous tasks. Additionally, examination of unit tuning during tactile and proprioceptive inputs indicates cells are often tuned differently in different contexts, reinforcing the need for continued refinement of BMI training and decoding approaches to closed-loop BMI systems for dexterous grasping.

[1]  J. Kleim,et al.  The organization of the forelimb representation of the C57BL/6 mouse motor cortex as defined by intracortical microstimulation and cytoarchitecture. , 2011, Cerebral cortex.

[2]  N. Hatsopoulos,et al.  Sensing with the Motor Cortex , 2011, Neuron.

[3]  S P Wise,et al.  Submodality distribution in sensorimotor cortex of the unanesthetized monkey. , 1981, Journal of neurophysiology.

[4]  S. Manita,et al.  A Top-Down Cortical Circuit for Accurate Sensory Perception , 2015, Neuron.

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

[6]  J. Donoghue,et al.  Plasticity and primary motor cortex. , 2000, Annual review of neuroscience.

[7]  Nicholas G. Hatsopoulos,et al.  2009 Special Issue: Exploiting multiple sensory modalities in brain-machine interfaces , 2009 .

[8]  Roberta Kwok,et al.  Neuroprosthetics: Once more, with feeling , 2013, Nature.

[9]  Anish A. Sarma,et al.  Clinical translation of a high-performance neural prosthesis , 2015, Nature Medicine.

[10]  J. Sanes,et al.  Orderly Somatotopy in Primary Motor Cortex: Does It Exist? , 2001, NeuroImage.

[11]  J. Murphy,et al.  Spatial organization of precentral cortex in awake primates. I. Somatosensory inputs. , 1978, Journal of neurophysiology.

[12]  Nitish V. Thakor,et al.  Cortical decoding of individual finger and wrist kinematics for an upper-limb neuroprosthesis , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[13]  Bagrat Amirikian,et al.  Directional tuning profiles of motor cortical cells , 2000, Neuroscience Research.

[14]  Kapil D. Katyal,et al.  Behavioral Demonstration of a Somatosensory Neuroprosthesis , 2013, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

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

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

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

[18]  Andreas Schulze-Bonhage,et al.  Decoding natural grasp types from human ECoG , 2012, NeuroImage.

[19]  R. Lemon Functional properties of monkey motor cortex neurones receiving afferent input from the hand and fingers , 1981, The Journal of physiology.

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

[21]  M L Boninger,et al.  Ten-dimensional anthropomorphic arm control in a human brain−machine interface: difficulties, solutions, and limitations , 2015, Journal of neural engineering.

[22]  David P. Friedman,et al.  Projection pattern of functional components of thalamic ventrobasal complex on monkey somatosensory cortex. , 1982, Journal of neurophysiology.

[23]  Miguel A. L. Nicolelis,et al.  Brain–machine interfaces: past, present and future , 2006, Trends in Neurosciences.

[24]  Kapil D. Katyal,et al.  Individual finger control of a modular prosthetic limb using high-density electrocorticography in a human subject , 2016, Journal of neural engineering.

[25]  A. E. Casale,et al.  Motor Cortex Feedback Influences Sensory Processing by Modulating Network State , 2013, Neuron.

[26]  Cynthia A. Chestek,et al.  Enabling Low-Power, Multi-Modal Neural Interfaces Through a Common, Low-Bandwidth Feature Space , 2016, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[27]  S. Wise,et al.  The motor cortex of the rat: Cytoarchitecture and microstimulation mapping , 1982, The Journal of comparative neurology.

[28]  L. Miller,et al.  Restoration of grasp following paralysis through brain-controlled stimulation of muscles , 2012, Nature.

[29]  T. Hackett,et al.  Predictive motor control of sensory dynamics in auditory active sensing , 2015, Current Opinion in Neurobiology.

[30]  H. Yumiya,et al.  Peripheral input pathways to the monkey motor cortex , 1980, Experimental Brain Research.

[31]  H C Kwan,et al.  Spatial organization of precentral cortex in awake primates. II. Motor outputs. , 1978, Journal of neurophysiology.

[32]  Hyun-Chool Shin,et al.  Asynchronous Decoding of Dexterous Finger Movements Using M1 Neurons , 2008, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[33]  Andrew S. Whitford,et al.  Cortical control of a prosthetic arm for self-feeding , 2008, Nature.

[34]  B. Greger,et al.  Decoding Dexterous Finger Movements in a Neural Prosthesis Model Approaching Real-World Conditions , 2012, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[35]  Michael J. Black,et al.  Neural control of cursor trajectory and click by a human with tetraplegia 1000 days after implant of an intracortical microelectrode array , 2011 .

[36]  R. Porter,et al.  What is area 3a? , 1980, Brain Research Reviews.

[37]  Josef Parvizi,et al.  Hand posture classification using electrocorticography signals in the gamma band over human sensorimotor brain areas , 2013, Journal of neural engineering.

[38]  M. H. Schieber,et al.  Decoding M 1 neurons during multiple finger movements Abbreviated title : Decoding multiple finger movements , 2007 .

[39]  R. Porter,et al.  Afferent input to movement-related precentral neurones in conscious monkeys , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[40]  Miguel A. L. Nicolelis,et al.  A Brain-Machine Interface Instructed by Direct Intracortical Microstimulation , 2009, Front. Integr. Neurosci..

[41]  Sung Shin Kim,et al.  Restoring tactile and proprioceptive sensation through a brain interface , 2015, Neurobiology of Disease.

[42]  Nicholas G Hatsopoulos,et al.  Incorporating Feedback from Multiple Sensory Modalities Enhances Brain–Machine Interface Control , 2010, The Journal of Neuroscience.