A high performing brain–machine interface driven by low-frequency local field potentials alone and together with spikes

OBJECTIVE Brain-machine interfaces (BMIs) seek to enable people with movement disabilities to directly control prosthetic systems with their neural activity. Current high performance BMIs are driven by action potentials (spikes), but access to this signal often diminishes as sensors degrade over time. Decoding local field potentials (LFPs) as an alternative or complementary BMI control signal may improve performance when there is a paucity of spike signals. To date only a small handful of LFP decoding methods have been tested online; there remains a need to test different LFP decoding approaches and improve LFP-driven performance. There has also not been a reported demonstration of a hybrid BMI that decodes kinematics from both LFP and spikes. Here we first evaluate a BMI driven by the local motor potential (LMP), a low-pass filtered time-domain LFP amplitude feature. We then combine decoding of both LMP and spikes to implement a hybrid BMI. APPROACH Spikes and LFP were recorded from two macaques implanted with multielectrode arrays in primary and premotor cortex while they performed a reaching task. We then evaluated closed-loop BMI control using biomimetic decoders driven by LMP, spikes, or both signals together. MAIN RESULTS LMP decoding enabled quick and accurate cursor control which surpassed previously reported LFP BMI performance. Hybrid decoding of both spikes and LMP improved performance when spikes signal quality was mediocre to poor. SIGNIFICANCE These findings show that LMP is an effective BMI control signal which requires minimal power to extract and can substitute for or augment impoverished spikes signals. Use of this signal may lengthen the useful lifespan of BMIs and is therefore an important step towards clinically viable BMIs.

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

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

[3]  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.

[4]  Eun Jung Hwang,et al.  The utility of multichannel local field potentials for brain–machine interfaces , 2013, Journal of neural engineering.

[5]  Michael J. Black,et al.  Neural control of computer cursor velocity by decoding motor cortical spiking activity in humans with tetraplegia , 2008, Journal of neural engineering.

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

[7]  Bijan Pesaran,et al.  Optimizing the Decoding of Movement Goals from Local Field Potentials in Macaque Cortex , 2011, The Journal of Neuroscience.

[8]  Shaomin Zhang,et al.  Long-term decoding stability of local field potentials from silicon arrays in primate motor cortex during a 2D center out task , 2014, Journal of neural engineering.

[9]  Nicholas G Hatsopoulos,et al.  Early visuomotor representations revealed from evoked local field potentials in motor and premotor cortical areas. , 2006, Journal of neurophysiology.

[10]  P.R. Kennedy,et al.  Computer control using human intracortical local field potentials , 2004, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

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

[12]  Robert D Flint,et al.  Local field potentials allow accurate decoding of muscle activity. , 2012, Journal of neurophysiology.

[13]  L R Hochberg,et al.  Efficient Decoding With Steady-State Kalman Filter in Neural Interface Systems , 2011, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[14]  Sarah A. Douglas,et al.  Testing pointing device performance and user assessment with the ISO 9241, Part 9 standard , 1999, CHI '99.

[15]  Krishna V. Shenoy,et al.  Monkey models for brain-machine interfaces: The need for maintaining diversity , 2011, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[16]  Paul Nuyujukian,et al.  Intention estimation in brain–machine interfaces , 2014, Journal of neural engineering.

[17]  Nicolas Y. Masse,et al.  Neural Point-and-Click Communication by a Person With Incomplete Locked-In Syndrome , 2015, Neurorehabilitation and neural repair.

[18]  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.

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

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

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

[22]  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.

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

[24]  I. Scott MacKenzie,et al.  Extending Fitts' law to two-dimensional tasks , 1992, CHI.

[25]  D.A. Heldman,et al.  Local field potential spectral tuning in motor cortex during reaching , 2006, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[26]  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 .

[27]  Steven M Chase,et al.  Control of a brain–computer interface without spike sorting , 2009, Journal of neural engineering.

[28]  A. TUSTIN,et al.  Automatic Control Systems , 1950, Nature.

[29]  Robert E. Kass,et al.  2009 Special Issue: Bias, optimal linear estimation, and the differences between open-loop simulation and closed-loop performance of spiking-based brain-computer interface algorithms , 2009 .

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

[31]  Shaomin Zhang,et al.  Reliability of directional information in unsorted spikes and local field potentials recorded in human motor cortex , 2014, Journal of neural engineering.

[32]  Stephen I. Ryu,et al.  Hybrid decoding of both spikes and low-frequency local field potentials for brain-machine interfaces , 2014, 2014 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[33]  Shaomin Zhang,et al.  Corrigendum: Long-term decoding stability of local field potentials from silicon arrays in primate motor cortex during a 2D center out task (2014 J. Neural Eng. 11 036009) , 2014 .

[34]  Vikash Gilja,et al.  Long-term Stability of Neural Prosthetic Control Signals from Silicon Cortical Arrays in Rhesus Macaque Motor Cortex , 2010 .

[35]  Kwabena Boahen,et al.  Design and validation of a real-time spiking-neural-network decoder for brain–machine interfaces , 2013, Journal of neural engineering.

[36]  I. Scott MacKenzie,et al.  Lag as a determinant of human performance in interactive systems , 1993, INTERCHI.

[37]  Krishna V. Shenoy,et al.  Combining Decoder Design and Neural Adaptation in Brain-Machine Interfaces , 2014, Neuron.

[38]  Krishna V Shenoy,et al.  Human cortical prostheses: lost in translation? , 2009, Neurosurgical focus.

[39]  John P. Cunningham,et al.  A High-Performance Neural Prosthesis Enabled by Control Algorithm Design , 2012, Nature Neuroscience.

[40]  M. Carandini,et al.  Local Origin of Field Potentials in Visual Cortex , 2009, Neuron.

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

[42]  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.

[43]  G. Rizzolatti,et al.  Seven Years of Recording from Monkey Cortex with a Chronically Implanted Multiple Microelectrode , 2010, Front. Neuroeng..

[44]  Michael Gastpar,et al.  Brain-machine interface control using broadband spectral power from local field potentials , 2013, 2013 35th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[45]  Paul Nuyujukian,et al.  Performance sustaining intracortical neural prostheses , 2014, Journal of neural engineering.

[46]  Francis R. Willett,et al.  Compensating for delays in brain-machine interfaces by decoding intended future movement , 2012, 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

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

[48]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

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

[50]  P. Fitts The information capacity of the human motor system in controlling the amplitude of movement. , 1954, Journal of experimental psychology.

[51]  L. Miller,et al.  Accurate decoding of reaching movements from field potentials in the absence of spikes , 2012, Journal of neural engineering.

[52]  Bijan Pesaran,et al.  Temporal structure in neuronal activity during working memory in macaque parietal cortex , 2000, Nature Neuroscience.

[53]  S. Meagher Instant neural control of a movement signal , 2002 .

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

[55]  Weng Khuen Ho,et al.  Automatic control systems, 7th edition : By Benjamin C. Kuo. Prentice-Hall, Englewood Cliffs, NJ (1995). ISBN 0-13-304759-8 , 1997, Autom..

[56]  Stefano Panzeri,et al.  Modelling and analysis of local field potentials for studying the function of cortical circuits , 2013, Nature Reviews Neuroscience.

[57]  Robert D Flint,et al.  Long term, stable brain machine interface performance using local field potentials and multiunit spikes , 2013, Journal of neural engineering.

[58]  Kelvin So,et al.  Subject-specific modulation of local field potential spectral power during brain–machine interface control in primates , 2014, Journal of neural engineering.

[59]  Vikash Gilja,et al.  A closed-loop human simulator for investigating the role of feedback control in brain-machine interfaces. , 2011, Journal of neurophysiology.

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

[61]  Alexander Kraskov,et al.  Influence of spiking activity on cortical local field potentials , 2013, The Journal of physiology.

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

[63]  Bijan Pesaran,et al.  A Method for Detection and Classification of Events in Neural Activity , 2006, IEEE Transactions on Biomedical Engineering.

[64]  J. Donoghue,et al.  Failure mode analysis of silicon-based intracortical microelectrode arrays in non-human primates , 2013, Journal of neural engineering.