Decoding 3D reach and grasp from hybrid signals in motor and premotor cortices: spikes, multiunit activity, and local field potentials.

Neural activity in motor cortex during reach and grasp movements shows modulations in a broad range of signals from single-neuron spiking activity (SA) to various frequency bands in broadband local field potentials (LFPs). In particular, spatiotemporal patterns in multiband LFPs are thought to reflect dendritic integration of local and interareal synaptic inputs, attentional and preparatory processes, and multiunit activity (MUA) related to movement representation in the local motor area. Nevertheless, the relationship between multiband LFPs and SA, and their relationship to movement parameters and their relative value as brain-computer interface (BCI) control signals, remain poorly understood. Also, although this broad range of signals may provide complementary information channels in primary (MI) and ventral premotor (PMv) areas, areal differences in information have not been systematically examined. Here, for the first time, the amount of information in SA and multiband LFPs was compared for MI and PMv by recording from dual 96-multielectrode arrays while monkeys made naturalistic reach and grasp actions. Information was assessed as decoding accuracy for 3D arm end point and grip aperture kinematics based on SA or LFPs in MI and PMv, or combinations of signal types across areas. In contrast with previous studies with ≤16 simultaneous electrodes, here ensembles of >16 units (on average) carried more information than multiband, multichannel LFPs. Furthermore, reach and grasp information added by various LFP frequency bands was not independent from that in SA ensembles but rather typically less than and primarily contained within the latter. Notably, MI and PMv did not show a particular bias toward reach or grasp for this task or for a broad range of signal types. For BCIs, our results indicate that neuronal ensemble spiking is the preferred signal for decoding, while LFPs and combined signals from PMv and MI can add robustness to BCI control.

[1]  E. Fetz Operant Conditioning of Cortical Unit Activity , 1969, Science.

[2]  J. Kamiya,et al.  The control of electroencephalographic alpha rhythms through auditory feedback and the associated mental activity. , 1970, Psychophysiology.

[3]  M. Craggs Cortical control of motor prostheses: using the cord-transected baboon as the primate model for human paraplegia. , 1975, Advances in neurology.

[4]  W. B. Plotkin On the self-regulation of the occipital alpha rhythm: control strategies, states of consciousness, and the role of physiological feedback. , 1976, Journal of experimental psychology. General.

[5]  U. Mitzdorf Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. , 1985, Physiological reviews.

[6]  J. Tanji,et al.  Premotor cortex neurons in macaques: activity before distal and proximal forelimb movements , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  Lemon Rn,et al.  The G. L. Brown Prize Lecture. Cortical control of the primate hand , 1993 .

[8]  R N Lemon,et al.  The G. L. Brown Prize Lecture. Cortical control of the primate hand , 1993, Experimental physiology.

[9]  Scott T. Grafton,et al.  Cortical control of movement , 1994, Annals of neurology.

[10]  Jerald D. Kralik,et al.  Real-time prediction of hand trajectory by ensembles of cortical neurons in primates , 2000, Nature.

[11]  N. Logothetis The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[12]  G. Rizzolatti,et al.  Motor and cognitive functions of the ventral premotor cortex , 2002, Current Opinion in Neurobiology.

[13]  Dylan F. Cooke,et al.  The Cortical Control of Movement Revisited , 2002, Neuron.

[14]  David M. Santucci,et al.  Learning to Control a Brain–Machine Interface for Reaching and Grasping by Primates , 2003, PLoS biology.

[15]  C. Mehring,et al.  Inference of hand movements from local field potentials in monkey motor cortex , 2003, Nature Neuroscience.

[16]  Jonathan R Wolpaw,et al.  Control of a two-dimensional movement signal by a noninvasive brain-computer interface in humans. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[17]  G. Rizzolatti,et al.  Functional organization of inferior area 6 in the macaque monkey , 2004, Experimental Brain Research.

[18]  J. Joseph,et al.  Effects of two neuroleptic drugs on focal somatoparietal rhythms in free awake cats , 1979, Psychopharmacology.

[19]  E. Bizzi,et al.  Neuronal correlates of movement dynamics in the dorsal and ventral premotor area in the monkey , 2005, Experimental Brain Research.

[20]  C. Mehring,et al.  Encoding of Movement Direction in Different Frequency Ranges of Motor Cortical Local Field Potentials , 2005, The Journal of Neuroscience.

[21]  David M. Santucci,et al.  Frontal and parietal cortical ensembles predict single‐trial muscle activity during reaching movements in primates , 2005, The European journal of neuroscience.

[22]  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.

[23]  R. Andersen,et al.  Cortical Local Field Potential Encodes Movement Intentions in the Posterior Parietal Cortex , 2005, Neuron.

[24]  Wei Wu,et al.  Bayesian Population Decoding of Motor Cortical Activity Using a Kalman Filter , 2006, Neural Computation.

[25]  David T. Westwick,et al.  Identification of Multiple-Input Systems with Highly Coupled Inputs: Application to EMG Prediction from Multiple Intracortical Electrodes , 2006, Neural Computation.

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

[27]  Michael J. Black,et al.  Decoding grasp aperture from motor-cortical population activity , 2007, 2007 3rd International IEEE/EMBS Conference on Neural Engineering.

[28]  J. Wolpaw,et al.  Decoding two-dimensional movement trajectories using electrocorticographic signals in humans , 2007, Journal of neural engineering.

[29]  John P. Donoghue,et al.  Automated spike sorting using density grid contour clustering and subtractive waveform decomposition , 2007, Journal of Neuroscience Methods.

[30]  T Brochier,et al.  Simultaneous recording of macaque premotor and primary motor cortex neuronal populations reveals different functional contributions to visuomotor grasp. , 2007, Journal of neurophysiology.

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

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

[33]  Arthur Gretton,et al.  Low-Frequency Local Field Potentials and Spikes in Primary Visual Cortex Convey Independent Visual Information , 2008, The Journal of Neuroscience.

[34]  Andreas Schulze-Bonhage,et al.  Prediction of arm movement trajectories from ECoG-recordings in humans , 2008, Journal of Neuroscience Methods.

[35]  M. Nicolelis,et al.  Decoding of temporal intervals from cortical ensemble activity. , 2008, Journal of neurophysiology.

[36]  E. Fetz,et al.  Direct control of paralyzed muscles by cortical neurons , 2008, Nature.

[37]  C. Braun,et al.  Hand Movement Direction Decoded from MEG and EEG , 2008, The Journal of Neuroscience.

[38]  Arthur Gretton,et al.  Inferring spike trains from local field potentials. , 2008, Journal of neurophysiology.

[39]  M. Budoff,et al.  National Institute of Neurological Disorders and Stroke , 2008 .

[40]  C. Braun,et al.  A review on directional information in neural signals for brain-machine interfaces , 2009, Journal of Physiology-Paris.

[41]  Yali Amit,et al.  Single-unit stability using chronically implanted multielectrode arrays. , 2009, Journal of neurophysiology.

[42]  Miguel A. L. Nicolelis,et al.  Principles of neural ensemble physiology underlying the operation of brain–machine interfaces , 2009, Nature Reviews Neuroscience.

[43]  John P. Cunningham,et al.  Neural prosthetic systems: Current problems and future directions , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[44]  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.

[45]  Eun Jung Hwang,et al.  Brain Control of Movement Execution Onset Using Local Field Potentials in Posterior Parietal Cortex , 2009, The Journal of Neuroscience.

[46]  J. Carmena,et al.  Emergence of a Stable Cortical Map for Neuroprosthetic Control , 2009, PLoS biology.

[47]  Hideki Shimazu,et al.  Modulation of primary motor cortex outputs from ventral premotor cortex during visually guided grasp in the macaque monkey , 2009, The Journal of physiology.

[48]  Leigh R. Hochberg,et al.  Application of system identification methods for decoding imagined single-joint movements in an individual with high tetraplegia , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

[49]  Nicolas Brunel,et al.  Sensory neural codes using multiplexed temporal scales , 2010, Trends in Neurosciences.

[50]  Stefano Panzeri,et al.  Sensory information in local field potentials and spikes from visual and auditory cortices: time scales and frequency bands , 2010, Journal of Computational Neuroscience.

[51]  Naotaka Fujii,et al.  Long-Term Asynchronous Decoding of Arm Motion Using Electrocorticographic Signals in Monkeys , 2009, Front. Neuroeng..

[52]  Michael J. Black,et al.  Decoding Complete Reach and Grasp Actions from Local Primary Motor Cortex Populations , 2010, The Journal of Neuroscience.

[53]  Hansjörg Scherberger,et al.  Context-Specific Grasp Movement Representation in Macaque Ventral Premotor Cortex , 2010, The Journal of Neuroscience.

[54]  Trent J. Bradberry,et al.  Reconstructing Three-Dimensional Hand Movements from Noninvasive Electroencephalographic Signals , 2010, The Journal of Neuroscience.

[55]  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.

[56]  Brendan Z. Allison,et al.  The Hybrid BCI , 2010, Frontiers in Neuroscience.

[57]  Arjun K. Bansal,et al.  Relationships among low-frequency local field potentials, spiking activity, and three-dimensional reach and grasp kinematics in primary motor and ventral premotor cortices. , 2011, Journal of neurophysiology.