Cortico-Cortical Interactions during Acquisition and Use of a Neuroprosthetic Skill

A motor cortex-based brain-computer interface (BCI) creates a novel real world output directly from cortical activity. Use of a BCI has been demonstrated to be a learned skill that involves recruitment of neural populations that are directly linked to BCI control as well as those that are not. The nature of interactions between these populations, however, remains largely unknown. Here, we employed a data-driven approach to assess the interaction between both local and remote cortical areas during the use of an electrocorticographic BCI, a method which allows direct sampling of cortical surface potentials. Comparing the area controlling the BCI with remote areas, we evaluated relationships between the amplitude envelopes of band limited powers as well as non-linear phase-phase interactions. We found amplitude-amplitude interactions in the high gamma (HG, 70–150 Hz) range that were primarily located in the posterior portion of the frontal lobe, near the controlling site, and non-linear phase-phase interactions involving multiple frequencies (cross-frequency coupling between 8–11 Hz and 70–90 Hz) taking place over larger cortical distances. Further, strength of the amplitude-amplitude interactions decreased with time, whereas the phase-phase interactions did not. These findings suggest multiple modes of cortical communication taking place during BCI use that are specialized for function and depend on interaction distance.

[1]  N. Crone,et al.  High-frequency gamma oscillations and human brain mapping with electrocorticography. , 2006, Progress in brain research.

[2]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[3]  Gerwin Schalk,et al.  A brain–computer interface using electrocorticographic signals in humans , 2004, Journal of neural engineering.

[4]  Theodore S. Rappaport,et al.  Wireless communications - principles and practice , 1996 .

[5]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[6]  E. Fetz,et al.  Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys. , 1996, Journal of neurophysiology.

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

[8]  Nick F. Ramsey,et al.  Human Motor Cortical Activity Is Selectively Phase-Entrained on Underlying Rhythms , 2012, PLoS Comput. Biol..

[9]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[10]  C. L. Nikias,et al.  Signal processing with higher-order spectra , 1993, IEEE Signal Processing Magazine.

[11]  B. Balas,et al.  Personal Familiarity Influences the Processing of Upright and Inverted Faces in Infants , 2009, Front. Hum. Neurosci..

[12]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[13]  Rajesh P. N. Rao,et al.  Distributed cortical adaptation during learning of a brain–computer interface task , 2013, Proceedings of the National Academy of Sciences.

[14]  Rajesh P. N. Rao,et al.  Electrocorticography-based brain computer Interface-the seattle experience , 2006, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

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

[16]  Aaron C. Koralek,et al.  Corticostriatal plasticity is necessary for learning intentional neuroprosthetic skills , 2012, Nature.

[17]  R. Schmidt,et al.  Cross-Frequency Phase–Phase Coupling between Theta and Gamma Oscillations in the Hippocampus , 2012, The Journal of Neuroscience.

[18]  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.

[19]  R. Knight,et al.  The functional role of cross-frequency coupling , 2010, Trends in Cognitive Sciences.

[20]  Rajesh P. N. Rao,et al.  Brain–computer interfaces: a powerful tool for scientific inquiry , 2014, Current Opinion in Neurobiology.

[21]  Rajesh P. N. Rao,et al.  Dynamic Modulation of Local Population Activity by Rhythm Phase in Human Occipital Cortex During a Visual Search Task , 2010, Front. Hum. Neurosci..

[22]  P. Goldman-Rakic.  The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[23]  N. Birbaumer,et al.  BCI2000: a general-purpose brain-computer interface (BCI) system , 2004, IEEE Transactions on Biomedical Engineering.

[24]  N. Logothetis,et al.  Scaling Brain Size, Keeping Timing: Evolutionary Preservation of Brain Rhythms , 2013, Neuron.

[25]  T. Sejnowski,et al.  Correlated neuronal activity and the flow of neural information , 2001, Nature Reviews Neuroscience.

[26]  S. Bressler,et al.  Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Jeffrey G. Ojemann,et al.  Bi-phase locking — a tool for probing non-linear interaction in the human brain , 2009, NeuroImage.

[28]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[29]  P. Goldman-Rakic.  The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[30]  M. Hallett,et al.  Identifying true brain interaction from EEG data using the imaginary part of coherency , 2004, Clinical Neurophysiology.

[31]  Karunesh Ganguly,et al.  Neural Correlates of Skill Acquisition with a Cortical Brain–Machine Interface , 2010, Journal of motor behavior.

[32]  Rajesh P. N. Rao,et al.  Nonlinear Phase–Phase Cross-Frequency Coupling Mediates Communication between Distant Sites in Human Neocortex , 2009, The Journal of Neuroscience.

[33]  W. Singer.  Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[34]  Sebastiaan Overeem,et al.  Corticospinal Beta-Band Synchronization Entails Rhythmic Gain Modulation , 2010, The Journal of Neuroscience.

[35]  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.

[36]  Adriano B. L. Tort,et al.  On cross-frequency phase-phase coupling between theta and gamma oscillations in the hippocampus , 2016, eLife.

[37]  A. Schnitzler,et al.  Normal and pathological oscillatory communication in the brain , 2005, Nature Reviews Neuroscience.

[38]  Rajesh P. N. Rao,et al.  Short-time windowed covariance: A metric for identifying non-stationary, event-related covariant cortical sites , 2014, Journal of Neuroscience Methods.

[39]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[40]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[41]  A. Schnitzler,et al.  The neural basis of intermittent motor control in humans , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[42]  J. Kalaska,et al.  Learning to Move Machines with the Mind , 2022 .

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

[44]  M. Kahana.  The Cognitive Correlates of Human Brain Oscillations , 2006, The Journal of Neuroscience.

[45]  T. Hare,et al.  Behavioral / Cognitive Interactions between Dorsolateral and Ventromedial Prefrontal Cortex Underlie Context-Dependent Stimulus Valuation in Goal-Directed Choice , 2017 .

[46]  J. A. Wilson,et al.  Two-dimensional movement control using electrocorticographic signals in humans , 2008, Journal of neural engineering.

[47]  Brittany M. Young,et al.  Changes in functional connectivity correlate with behavioral gains in stroke patients after therapy using a brain-computer interface device , 2014, Front. Neuroeng..

[48]  G. Schalk,et al.  The emerging world of motor neuroprosthetics: a neurosurgical perspective. , 2006, Neurosurgery.

[49]  G. Buzsáki,et al.  Interneuron Diversity series: Circuit complexity and axon wiring economy of cortical interneurons , 2004, Trends in Neurosciences.

[50]  David M. Groppe,et al.  Corticocortical Evoked Potentials Reveal Projectors and Integrators in Human Brain Networks , 2014, The Journal of Neuroscience.

[51]  Joaquín M. Fuster,et al.  Executive frontal functions , 2000, Experimental Brain Research.

[52]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[53]  Okihide Hikosaka,et al.  Functional differences between macaque prefrontal cortex and caudate nucleus during eye movements with and without reward , 2006, Experimental Brain Research.

[54]  P. Fries.  A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[55]  Daniel M. Corcos,et al.  Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: A meta-analysis , 2006, NeuroImage.

[56]  O. Sporns,et al.  The economy of brain network organization , 2012, Nature Reviews Neuroscience.

[57]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[58]  Dragan F. Dimitrov,et al.  Reversible large-scale modification of cortical networks during neuroprosthetic control , 2011, Nature Neuroscience.

[59]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

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

[61]  Nick F. Ramsey,et al.  Automated electrocorticographic electrode localization on individually rendered brain surfaces , 2010, Journal of Neuroscience Methods.

[62]  J. Grafman,et al.  Dorsolateral prefrontal contributions to human working memory , 2013, Cortex.

[63]  Alexa B. Roggeveen,et al.  Large-scale gamma-band phase synchronization and selective attention. , 2008, Cerebral cortex.

[64]  Rajesh P. N. Rao,et al.  Robust, long-term control of an electrocorticographic brain-computer interface with fixed parameters. , 2009, Neurosurgical focus.