Adaptive tracking of human ECoG network dynamics

Objective. Extracting and modeling the low-dimensional dynamics of multi-site electrocorticogram (ECoG) network activity is important in studying brain functions and dysfunctions and for developing translational neurotechnologies. Dynamic latent state models can be used to describe the ECoG network dynamics with low-dimensional latent states. But so far, non-stationarity of ECoG network dynamics has largely not been addressed in these latent state models. Such non-stationarity can happen due to a change in brain state or recording instability over time. A critical question is whether adaptive tracking of ECoG network dynamics can lead to further dimensionality reduction and more parsimonious and precise modeling. This question is largely unaddressed. Approach. We investigate this question by employing an adaptive linear state-space model for ECoG network activity constructed from ECoG power feature time-series over tens of hours from 10 human subjects with epilepsy. We study how adaptive modeling affects the prediction and dimensionality reduction for ECoG network dynamics compared with prior non-adaptive models, which do not track non-stationarity. Main results. Across the 10 subjects, adaptive modeling significantly improved the prediction of ECoG network dynamics compared with non-adaptive modeling, especially for lower latent state dimensions. Also, compared with non-adaptive modeling, adaptive modeling allowed for additional dimensionality reduction without degrading prediction performance. Finally, these results suggested that ECoG network dynamics over our recording periods exhibit non-stationarity, which can be tracked with adaptive modeling. Significance. These results have important implications for studying low-dimensional neural representations using ECoG, and for developing future adaptive neurotechnologies for more precise decoding and modulation of brain states in neurological and neuropsychiatric disorders.

[1]  Omid G. Sani,et al.  Modeling behaviorally relevant neural dynamics enabled by preferential subspace identification , 2020, Nature Neuroscience.

[2]  P. Uhlhaas,et al.  Working memory and neural oscillations: alpha–gamma versus theta–gamma codes for distinct WM information? , 2014, Trends in Cognitive Sciences.

[3]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[4]  R. Nicoll A Brief History of Long-Term Potentiation , 2017, Neuron.

[5]  Michael J. Kahana,et al.  Direct brain recordings fuel advances in cognitive electrophysiology , 2010, Trends in Cognitive Sciences.

[6]  Han-Lin Hsieh,et al.  Optimizing the learning rate for adaptive estimation of neural encoding models , 2018, PLoS Comput. Biol..

[7]  L. Williams,et al.  Defining biotypes for depression and anxiety based on large‐scale circuit dysfunction: a theoretical review of the evidence and future directions for clinical translation , 2017, Depression and anxiety.

[8]  Edward F. Chang,et al.  Speech synthesis from neural decoding of spoken sentences , 2019, Nature.

[9]  S. Cash,et al.  Brain‐responsive neurostimulation in patients with medically intractable mesial temporal lobe epilepsy , 2017, Epilepsia.

[10]  Ronald G. García,et al.  Complexity Variability Assessment of Nonlinear Time-Varying Cardiovascular Control , 2017, Scientific Reports.

[11]  Thomas M. Hall,et al.  A Common Structure Underlies Low-Frequency Cortical Dynamics in Movement, Sleep, and Sedation , 2014, Neuron.

[12]  N. Thakor,et al.  Electrocorticographic amplitude predicts finger positions during slow grasping motions of the hand , 2010, Journal of neural engineering.

[13]  Kristofer E. Bouchard,et al.  Functional Organization of Human Sensorimotor Cortex for Speech Articulation , 2013, Nature.

[14]  Mirela V. Simon,et al.  Neural encoding and production of functional morphemes in the posterior temporal lobe , 2018, Nature Communications.

[15]  Michael J. Randazzo,et al.  Movement-related dynamics of cortical oscillations in Parkinson's disease and essential tremor. , 2016, Brain : a journal of neurology.

[16]  Luca Citi,et al.  A Real-Time Automated Point-Process Method for the Detection and Correction of Erroneous and Ectopic Heartbeats , 2012, IEEE Transactions on Biomedical Engineering.

[17]  Zhuo Chen,et al.  Neural decoding of attentional selection in multi-speaker environments without access to clean sources , 2017, Journal of neural engineering.

[18]  Alexander A. Fingelkurts,et al.  Altered Structure of Dynamic Electroencephalogram Oscillatory Pattern in Major Depression , 2015, Biological Psychiatry.

[19]  Birgit Dietrich,et al.  Model Reduction For Control System Design , 2016 .

[20]  Bijan Pesaran,et al.  Investigating large-scale brain dynamics using field potential recordings: analysis and interpretation , 2018, Nature Neuroscience.

[21]  Warren M Grill,et al.  Implanted neural interfaces: biochallenges and engineered solutions. , 2009, Annual review of biomedical engineering.

[22]  P. Brown,et al.  The functional role of beta oscillations in Parkinson's disease. , 2014, Parkinsonism & related disorders.

[23]  N. Volkow,et al.  Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications , 2011, Nature Reviews Neuroscience.

[24]  Nitish V. Thakor,et al.  Simultaneous Neural Control of Simple Reaching and Grasping With the Modular Prosthetic Limb Using Intracranial EEG , 2014, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[25]  Heather E. Dawes,et al.  Pilot Study of An Intracranial Electroencephalography Biomarker of Depressive Symptoms in Epilepsy. , 2019, The Journal of neuropsychiatry and clinical neurosciences.

[26]  Chengyuan Wu,et al.  Chronically Implanted Intracranial Electrodes: Tissue Reaction and Electrical Changes , 2018, Micromachines.

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

[28]  Chethan Pandarinath,et al.  Inferring single-trial neural population dynamics using sequential auto-encoders , 2017, Nature Methods.

[29]  Mehdi Aghagolzadeh,et al.  Inference and Decoding of Motor Cortex Low-Dimensional Dynamics via Latent State-Space Models , 2016, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[30]  L. Frank,et al.  New Experiences Enhance Coordinated Neural Activity in the Hippocampus , 2008, Neuron.

[31]  L. Carin,et al.  Relationship between intracortical electrode design and chronic recording function. , 2013, Biomaterials.

[32]  E. Halgren,et al.  High-frequency neural activity and human cognition: Past, present and possible future of intracranial EEG research , 2012, Progress in Neurobiology.

[33]  Z. Bashir,et al.  Long-term depression: multiple forms and implications for brain function , 2007, Trends in Neurosciences.

[34]  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.

[35]  Byron M. Yu,et al.  Dimensionality reduction for large-scale neural recordings , 2014, Nature Neuroscience.

[36]  H. Yokoi,et al.  Electrocorticographic control of a prosthetic arm in paralyzed patients , 2012, Annals of neurology.

[37]  Omid G. Sani,et al.  Compression and amplification algorithms in hearing aids impair the selectivity of neural responses to speech , 2021, Nature Biomedical Engineering.

[38]  Bijan Pesaran,et al.  A point-process matched filter for event detection and decoding from population spike trains , 2019, Journal of neural engineering.

[39]  M. Bushnell,et al.  How neuroimaging studies have challenged us to rethink: is chronic pain a disease? , 2009, The journal of pain : official journal of the American Pain Society.

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

[41]  Matthew T. Kaufman,et al.  Neural population dynamics during reaching , 2012, Nature.

[42]  Robert T Knight,et al.  Intracranial recordings and human memory , 2015, Current Opinion in Neurobiology.

[43]  J. Kaiser,et al.  Human gamma-frequency oscillations associated with attention and memory , 2007, Trends in Neurosciences.

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

[45]  Yuxiao Yang,et al.  Dynamic tracking of non-stationarity in human ECoG activity , 2017, 2017 39th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[46]  John P. Cunningham,et al.  Dynamical segmentation of single trials from population neural data , 2011, NIPS.

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

[48]  Robert T. Knight,et al.  Task-related activity in sensorimotor cortex in Parkinson's disease and essential tremor: changes in beta and gamma bands , 2015, Front. Hum. Neurosci..

[49]  A. Beuter,et al.  Closed-loop cortical neuromodulation in Parkinson’s disease: An alternative to deep brain stimulation? , 2014, Clinical Neurophysiology.

[50]  Eric Leuthardt,et al.  Decoding covert spatial attention using electrocorticographic (ECoG) signals in humans , 2012, NeuroImage.

[51]  Paul Nuyujukian,et al.  A high performing brain–machine interface driven by low-frequency local field potentials alone and together with spikes , 2015, bioRxiv.

[52]  John P. Cunningham,et al.  Empirical models of spiking in neural populations , 2011, NIPS.

[53]  J. Cavanaugh,et al.  The Akaike information criterion: Background, derivation, properties, application, interpretation, and refinements , 2019, WIREs Computational Statistics.

[54]  John P. Cunningham,et al.  Single-trial dynamics of motor cortex and their applications to brain-machine interfaces , 2015, Nature Communications.

[55]  Bart De Moor,et al.  Subspace Identification for Linear Systems: Theory ― Implementation ― Applications , 2011 .

[56]  Yuxiao Yang,et al.  An adaptive and generalizable closed-loop system for control of medically induced coma and other states of anesthesia , 2016, Journal of neural engineering.

[57]  P. Brown,et al.  Adaptive Deep Brain Stimulation for Movement Disorders: The Long Road to Clinical Therapy , 2017, Movement disorders : official journal of the Movement Disorder Society.

[58]  Yuxiao Yang,et al.  Dynamic network modeling and dimensionality reduction for human ECoG activity , 2019, Journal of neural engineering.

[59]  K. Miller,et al.  Exaggerated phase–amplitude coupling in the primary motor cortex in Parkinson disease , 2013, Proceedings of the National Academy of Sciences.

[60]  Daniel Moran,et al.  Evolution of brain–computer interface: action potentials, local field potentials and electrocorticograms , 2010, Current Opinion in Neurobiology.

[61]  Robin C. Ashmore,et al.  An Electrocorticographic Brain Interface in an Individual with Tetraplegia , 2013, PloS one.

[62]  Alexandre Hyafil,et al.  Neural Cross-Frequency Coupling: Connecting Architectures, Mechanisms, and Functions , 2015, Trends in Neurosciences.

[63]  K. Tye,et al.  Resolving the neural circuits of anxiety , 2015, Nature Neuroscience.

[64]  P. Starr,et al.  Oscillations in sensorimotor cortex in movement disorders: an electrocorticography study. , 2012, Brain : a journal of neurology.

[65]  A. Engel,et al.  Invasive recordings from the human brain: clinical insights and beyond , 2005, Nature Reviews Neuroscience.

[66]  L. Frank,et al.  Behavioral/Systems/Cognitive Hippocampal Plasticity across Multiple Days of Exposure to Novel Environments , 2022 .

[67]  V. Solo,et al.  Contrasting Patterns of Receptive Field Plasticity in the Hippocampus and the Entorhinal Cortex: An Adaptive Filtering Approach , 2002, The Journal of Neuroscience.

[68]  Bijan Pesaran,et al.  Multiscale modeling and decoding algorithms for spike-field activity , 2018, Journal of neural engineering.

[69]  Allison T. Connolly,et al.  A control-theoretic system identification framework and a real-time closed-loop clinical simulation testbed for electrical brain stimulation , 2018, Journal of neural engineering.

[70]  Maryam M. Shanechi,et al.  Estimating Multiscale Direct Causality Graphs in Neural Spike-Field Networks , 2019, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[71]  Yuxiao Yang,et al.  Investigating the effect of forgetting factor on tracking non-stationary neural dynamics , 2019, 2019 9th International IEEE/EMBS Conference on Neural Engineering (NER).

[72]  Yuxiao Yang,et al.  Mood variations decoded from multi-site intracranial human brain activity , 2018, Nature Biotechnology.

[73]  W. Drevets Neuroimaging and neuropathological studies of depression: implications for the cognitive-emotional features of mood disorders , 2001, Current Opinion in Neurobiology.

[74]  Maryam M Shanechi,et al.  Brain-Machine Interface Control Algorithms. , 2017, IEEE transactions on neural systems and rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[75]  John P. Cunningham,et al.  Gaussian-process factor analysis for low-dimensional single-trial analysis of neural population activity , 2008, NIPS.

[76]  Maryam M Shanechi,et al.  A Multiscale Dynamical Modeling and Identification Framework for Spike-Field Activity , 2019, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[77]  Warren M. Grill,et al.  Continuous Deep Brain Stimulation of the Subthalamic Nucleus may not Modulate Beta Bursts in Patients with Parkinson’s Disease , 2019, Brain Stimulation.

[78]  Geertjan Huiskamp,et al.  Neocortical electrical stimulation for epilepsy: Closed-loop versus open-loop , 2018, Epilepsy Research.

[79]  Karen Livescu,et al.  Differential Representation of Articulatory Gestures and Phonemes in Precentral and Inferior Frontal Gyri , 2018, The Journal of Neuroscience.

[80]  Robert E Kass,et al.  Functional network reorganization during learning in a brain-computer interface paradigm , 2008, Proceedings of the National Academy of Sciences.

[81]  F. Mormann,et al.  Seizure prediction for therapeutic devices: A review , 2016, Journal of Neuroscience Methods.

[82]  Virginia Woods,et al.  Long-term recording reliability of liquid crystal polymer µECoG arrays , 2018, Journal of neural engineering.

[83]  Deanna L. Wallace,et al.  Direct Electrical Stimulation of Lateral Orbitofrontal Cortex Acutely Improves Mood in Individuals with Symptoms of Depression , 2018, Current Biology.

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

[85]  Y. Salimpour,et al.  Cross-Frequency Coupling Based Neuromodulation for Treating Neurological Disorders , 2019, Front. Neurosci..

[86]  M. Shanechi Brain–machine interfaces from motor to mood , 2019, Nature Neuroscience.

[87]  Byron M. Yu,et al.  New neural activity patterns emerge with long-term learning , 2019, Proceedings of the National Academy of Sciences.

[88]  G B Stanley,et al.  Design strategies for dynamic closed-loop optogenetic neurocontrol in vivo , 2018, Journal of neural engineering.

[89]  Byron M. Yu,et al.  Single-Trial Neural Correlates of Arm Movement Preparation , 2011, Neuron.

[90]  Bijan Pesaran,et al.  Sparse model-based estimation of functional dependence in high-dimensional field and spike multiscale networks , 2019, Journal of neural engineering.

[91]  W. Grill,et al.  Biomarkers and Stimulation Algorithms for Adaptive Brain Stimulation , 2017, Front. Neurosci..

[92]  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.

[93]  Justin K. Romberg,et al.  Sparsity penalties in dynamical system estimation , 2011, 2011 45th Annual Conference on Information Sciences and Systems.

[94]  Daniel C Millard,et al.  System identification of the nonlinear dynamics in the thalamocortical circuit in response to patterned thalamic microstimulation in vivo , 2013, Journal of neural engineering.

[95]  Emery N Brown,et al.  Developing a personalized closed-loop controller of medically-induced coma in a rodent model , 2019, Journal of neural engineering.