Distinct neural patterns enable grasp types decoding in monkey dorsal premotor cortex

OBJECTIVE Recent studies have shown that dorsal premotor cortex (PMd), a cortical area in the dorsomedial grasp pathway, is involved in grasp movements. However, the neural ensemble firing property of PMd during grasp movements and the extent to which it can be used for grasp decoding are still unclear. APPROACH To address these issues, we used multielectrode arrays to record both spike and local field potential (LFP) signals in PMd in macaque monkeys performing reaching and grasping of one of four differently shaped objects. MAIN RESULTS Single and population neuronal activity showed distinct patterns during execution of different grip types. Cluster analysis of neural ensemble signals indicated that the grasp related patterns emerged soon (200-300 ms) after the go cue signal, and faded away during the hold period. The timing and duration of the patterns varied depending on the behaviors of individual monkey. Application of support vector machine model to stable activity patterns revealed classification accuracies of 94% and 89% for each of the two monkeys, indicating a robust, decodable grasp pattern encoded in the PMd. Grasp decoding using LFPs, especially the high-frequency bands, also produced high decoding accuracies. SIGNIFICANCE This study is the first to specify the neuronal population encoding of grasp during the time course of grasp. We demonstrate high grasp decoding performance in PMd. These findings, combined with previous evidence for reach related modulation studies, suggest that PMd may play an important role in generation and maintenance of grasp action and may be a suitable locus for brain-machine interface applications.

[1]  Simon A. Overduin,et al.  Modulation of Muscle Synergy Recruitment in Primate Grasping , 2008, The Journal of Neuroscience.

[2]  R Caminiti,et al.  Making arm movements within different parts of space: the premotor and motor cortical representation of a coordinate system for reaching to visual targets , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  Amy J Bastian,et al.  Multidigit Movement Synergies of the Human Hand in an Unconstrained Haptic Exploration Task , 2008, The Journal of Neuroscience.

[4]  Erk Subasi,et al.  Grasp Movement Decoding from Premotor and Parietal Cortex , 2011, The Journal of Neuroscience.

[5]  Chih-Jen Lin,et al.  LIBSVM: A library for support vector machines , 2011, TIST.

[6]  Eran Stark,et al.  Comparison of direction and object selectivity of local field potentials and single units in macaque posterior parietal cortex during prehension. , 2007, Journal of neurophysiology.

[7]  G. Luppino,et al.  Visual responses in the dorsal premotor area F2 of the macaque monkey , 1999, Experimental Brain Research.

[8]  Soumya Ghosh,et al.  Neurophysiology of prehension. II. Response diversity in primary somatosensory (S-I) and motor (M-I) cortices. , 2007, Journal of neurophysiology.

[9]  Jerald D. Kralik,et al.  Chronic, multisite, multielectrode recordings in macaque monkeys , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Alexander Kraskov,et al.  Selectivity for Grasp in Local Field Potential and Single Neuron Activity Recorded Simultaneously from M1 and F5 in the Awake Macaque Monkey , 2008, The Journal of Neuroscience.

[11]  S. Wise,et al.  Learning-dependent neuronal activity in the premotor cortex: activity during the acquisition of conditional motor associations , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  T. Kammer,et al.  Continuous theta-burst stimulation over the dorsal premotor cortex interferes with associative learning during object lifting , 2009, Cortex.

[13]  Arjun K. Bansal,et al.  Decoding 3D reach and grasp from hybrid signals in motor and premotor cortices: spikes, multiunit activity, and local field potentials. , 2012, Journal of neurophysiology.

[14]  Lauretta Passarelli,et al.  Cortical connections of the visuomotor parietooccipital area V6Ad of the macaque monkey , 2009, The Journal of comparative neurology.

[15]  Bastiaan R Bloem,et al.  Weight-Specific Anticipatory Coding of Grip Force in Human Dorsal Premotor Cortex , 2012, The Journal of Neuroscience.

[16]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[17]  J. F. Soechting,et al.  Postural Hand Synergies for Tool Use , 1998, The Journal of Neuroscience.

[18]  Scott T. Grafton The cognitive neuroscience of prehension: recent developments , 2010, Experimental Brain Research.

[19]  Shaomin Zhang,et al.  Dorsal premotor cortex of the macaque monkey participate grasp planning , 2015, 2015 7th International IEEE/EMBS Conference on Neural Engineering (NER).

[20]  L. Fogassi,et al.  Functional properties of grasping-related neurons in the dorsal premotor area F2 of the macaque monkey. , 2004, Journal of neurophysiology.

[21]  Michela Gamberini,et al.  ‘Arm‐reaching’ neurons in the parietal area V6A of the macaque monkey , 2001, The European journal of neuroscience.

[22]  Ahmed H. Tewfik,et al.  High Accuracy Decoding of Movement Target Direction in Non-Human Primates Based on Common Spatial Patterns of Local Field Potentials , 2010, PloS one.

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

[24]  Maria Alessandra Umiltà,et al.  Cortical control of grasp in non-human primates , 2007, Current Opinion in Neurobiology.

[25]  Nicholas Hatsopoulos,et al.  Decoding continuous and discrete motor behaviors using motor and premotor cortical ensembles. , 2004, Journal of neurophysiology.

[26]  William J Tyler,et al.  A quantitative overview of biophysical forces impinging on neural function , 2013, Physical biology.

[27]  Mikhail Belkin,et al.  Laplacian Eigenmaps for Dimensionality Reduction and Data Representation , 2003, Neural Computation.

[28]  S. P. Wise,et al.  Premotor cortex of rhesus monkeys: set-related activity during two conditional motor tasks , 2004, Experimental Brain Research.

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

[30]  Scott T. Grafton,et al.  Dorsal premotor cortex and conditional movement selection: A PET functional mapping study. , 1998, Journal of neurophysiology.

[31]  John P. Donoghue,et al.  Decoding 3-D Reach and Grasp Kinematics From High-Frequency Local Field Potentials in Primate Primary Motor Cortex , 2010, IEEE Transactions on Biomedical Engineering.

[32]  Amir Globerson,et al.  Correlations between Groups of Premotor Neurons Carry Information about Prehension , 2008, The Journal of Neuroscience.

[33]  James M. Keller,et al.  A fuzzy K-nearest neighbor algorithm , 1985, IEEE Transactions on Systems, Man, and Cybernetics.

[34]  Ivan Toni,et al.  Perceptuo-Motor Interactions during Prehension Movements , 2008, The Journal of Neuroscience.

[35]  Patrizia Fattori,et al.  Hand Orientation during Reach-to-Grasp Movements Modulates Neuronal Activity in the Medial Posterior Parietal Area V6A , 2009, The Journal of Neuroscience.

[36]  T. Ebner,et al.  Neuronal specification of direction and distance during reaching movements in the superior precentral premotor area and primary motor cortex of monkeys. , 1993, Journal of neurophysiology.

[37]  N.V. Thakor,et al.  Decoding Individuated Finger Movements Using Volume-Constrained Neuronal Ensembles in the M1 Hand Area , 2008, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[38]  M. Petrides Deficits in non-spatial conditional associative learning after periarcuate lesions in the monkey , 1985, Behavioural Brain Research.

[39]  Shaomin Zhang,et al.  Decoding grasp movement from monkey premotor cortex for real-time prosthetic hand control , 2013 .

[40]  Emilio Bizzi,et al.  The neural origin of muscle synergies , 2013, Front. Comput. Neurosci..

[41]  Marco Davare,et al.  Interactions between areas of the cortical grasping network , 2011, Current Opinion in Neurobiology.

[42]  D. Hoffman,et al.  Differential effects of muscimol microinjection into dorsal and ventral aspects of the premotor cortex of monkeys. , 1994, Journal of neurophysiology.

[43]  M. Davare,et al.  Behavioral / Systems / Cognitive Dissociating the Role of Ventral and Dorsal Premotor Cortex in Precision Grasping , 2018 .

[44]  Simon A. Overduin,et al.  Microstimulation Activates a Handful of Muscle Synergies , 2012, Neuron.

[45]  E. Bizzi,et al.  The construction of movement by the spinal cord , 1999, Nature Neuroscience.

[46]  J. Kalaska,et al.  Covariation of primate dorsal premotor cell activity with direction and amplitude during a memorized-delay reaching task. , 2000, Journal of neurophysiology.

[47]  Philippe A. Chouinard,et al.  Role of the Primary Motor and Dorsal Premotor Cortices in the Anticipation of Forces during Object Lifting , 2005, The Journal of Neuroscience.

[48]  G. Rizzolatti,et al.  Parietal Lobe: From Action Organization to Intention Understanding , 2005, Science.

[49]  Eran Stark,et al.  Predicting Movement from Multiunit Activity , 2007, The Journal of Neuroscience.

[50]  Eric O. Postma,et al.  Dimensionality Reduction: A Comparative Review , 2008 .

[51]  Byron M. Yu,et al.  Detecting neural-state transitions using hidden Markov models for motor cortical prostheses. , 2008, Journal of neurophysiology.

[52]  Jun Tanji,et al.  Differential involvement of neurons in the dorsal and ventral premotor cortex during processing of visual signals for action planning. , 2006, Journal of neurophysiology.

[53]  Paul B. Johnson,et al.  Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. , 1997, Annual review of neuroscience.

[54]  Patrizia Fattori,et al.  The Dorsomedial Pathway Is Not Just for Reaching: Grasping Neurons in the Medial Parieto-Occipital Cortex of the Macaque Monkey , 2010, The Journal of Neuroscience.

[55]  J.P. Donoghue,et al.  Reliability of signals from a chronically implanted, silicon-based electrode array in non-human primate primary motor cortex , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[56]  Gabriel Baud-Bovy,et al.  Neural bases of hand synergies , 2013, Front. Comput. Neurosci..

[57]  L. Miller,et al.  Primary motor cortical neurons encode functional muscle synergies , 2002, Experimental Brain Research.

[58]  Fang Wang,et al.  Local-learning-based neuron selection for grasping gesture prediction in motor brain machine interfaces. , 2013, Journal of neural engineering.

[59]  Arjun K. Bansal,et al.  Title: Relationships among Low-frequency Local Field Potentials, Spiking Activity and 2 3-d Reach and Grasp Kinematics in Primary Motor and Ventral Premotor Cortices 3 4 Running Head: Lf-lfp, Spikes and 3-d Reach and Grasp Kinematics 13 , 2011 .

[60]  Timothy J Ebner,et al.  Signaling of grasp dimension and grasp force in dorsal premotor cortex and primary motor cortex neurons during reach to grasp in the monkey. , 2009, Journal of neurophysiology.

[61]  T Brochier,et al.  Patterns of muscle activity underlying object-specific grasp by the macaque monkey. , 2004, Journal of neurophysiology.

[62]  Yoshua Bengio,et al.  Exploring Strategies for Training Deep Neural Networks , 2009, J. Mach. Learn. Res..

[63]  E. Stark,et al.  Encoding of reach and grasp by single neurons in premotor cortex is independent of recording site. , 2007, Journal of neurophysiology.

[64]  G. Rizzolatti,et al.  Object representation in the ventral premotor cortex (area F5) of the monkey. , 1997, Journal of neurophysiology.

[65]  L. Fogassi,et al.  Decoding the activity of grasping neurons recorded from the ventral premotor area F5 of the macaque monkey , 2011, Neuroscience.

[66]  Marc H Schieber,et al.  Hand function: peripheral and central constraints on performance. , 2004, Journal of applied physiology.

[67]  Vittorio Gallese,et al.  Somatotopic organization of the lateral part of area F2 (dorsal premotor cortex) of the macaque monkey. , 2003, Journal of neurophysiology.

[68]  Yaoyao Hao,et al.  Development of an invasive brain-machine interface with a monkey model , 2012, Chinese Science Bulletin.

[69]  Jody C Culham,et al.  Functional magnetic resonance adaptation reveals the involvement of the dorsomedial stream in hand orientation for grasping. , 2011, Journal of neurophysiology.

[70]  C. Galletti,et al.  Spatial tuning of reaching activity in the medial parieto‐occipital cortex (area V6A) of macaque monkey , 2005, The European journal of neuroscience.

[71]  C. Galletti,et al.  Role of the medial parieto-occipital cortex in the control of reaching and grasping movements , 2003, Experimental Brain Research.

[72]  S. Giszter,et al.  A Neural Basis for Motor Primitives in the Spinal Cord , 2010, The Journal of Neuroscience.