Dynamic Neural State Identification in Deep Brain Local Field Potentials of Neuropathic Pain

In neuropathic pain, the neurophysiological and neuropathological function of the ventro-posterolateral nucleus of the thalamus (VPL) and the periventricular gray/periaqueductal gray area (PVAG) involves multiple frequency oscillations. Moreover, oscillations related to pain perception and modulation change dynamically over time. Fluctuations in these neural oscillations reflect the dynamic neural states of the nucleus. In this study, an approach to classifying the synchronization level was developed to dynamically identify the neural states. An oscillation extraction model based on windowed wavelet packet transform was designed to characterize the activity level of oscillations. The wavelet packet coefficients sparsely represented the activity level of theta and alpha oscillations in local field potentials (LFPs). Then, a state discrimination model was designed to calculate an adaptive threshold to determine the activity level of oscillations. Finally, the neural state was represented by the activity levels of both theta and alpha oscillations. The relationship between neural states and pain relief was further evaluated. The performance of the state identification approach achieved sensitivity and specificity beyond 80% in simulation signals. Neural states of the PVAG and VPL were dynamically identified from LFPs of neuropathic pain patients. The occurrence of neural states based on theta and alpha oscillations were correlated to the degree of pain relief by deep brain stimulation. In the PVAG LFPs, the occurrence of the state with high activity levels of theta oscillations independent of alpha and the state with low-level alpha and high-level theta oscillations were significantly correlated with pain relief by deep brain stimulation. This study provides a reliable approach to identifying the dynamic neural states in LFPs with a low signal-to-noise ratio by using sparse representation based on wavelet packet transform. Furthermore, it may advance closed-loop deep brain stimulation based on neural states integrating multiple neural oscillations.

[1]  Philip A Starr,et al.  Commentary on “Adaptive deep brain stimulation in advanced Parkinson disease” , 2013, Annals of neurology.

[2]  Hualou Liang,et al.  Wavelet Analysis , 2014, Encyclopedia of Computational Neuroscience.

[3]  Ronald R. Coifman,et al.  Fast wavelet packet image compression , 1998, Proceedings DCC '98 Data Compression Conference (Cat. No.98TB100225).

[4]  Aviva Abosch,et al.  Variation in Deep Brain Stimulation Electrode Impedance over Years Following Electrode Implantation , 2014, Stereotactic and Functional Neurosurgery.

[5]  Qi Wu,et al.  An Improved Sparse Representation over Learned Dictionary Method for Seizure Detection , 2016, Int. J. Neural Syst..

[6]  Alec B. O’Connor Neuropathic Pain , 2012, PharmacoEconomics.

[7]  CuiMinshan,et al.  Sparse representation-based classification , 2016 .

[8]  A. Chiu,et al.  Common time–frequency analysis of local field potential and pyramidal cell activity in seizure-like events of the rat hippocampus , 2011, Journal of neural engineering.

[9]  Jian Yang,et al.  Learning a structure adaptive dictionary for sparse representation based classification , 2016, Neurocomputing.

[10]  John-Stuart Brittain,et al.  Oscillations and the basal ganglia: Motor control and beyond , 2014, NeuroImage.

[11]  S. Haber,et al.  Closed-Loop Deep Brain Stimulation Is Superior in Ameliorating Parkinsonism , 2011, Neuron.

[12]  H. Bergman,et al.  Pathological synchronization in Parkinson's disease: networks, models and treatments , 2007, Trends in Neurosciences.

[13]  Peter Brown,et al.  Subthalamic beta dynamics mirror Parkinsonian bradykinesia months after neurostimulator implantation , 2017, Movement disorders : official journal of the Movement Disorder Society.

[14]  J. Stein,et al.  Measuring complex behaviors of local oscillatory networks in deep brain local field potentials , 2016, Journal of Neuroscience Methods.

[15]  Tipu Z. Aziz,et al.  Oscillatory neural representations in the sensory thalamus predict neuropathic pain relief by deep brain stimulation , 2018, Neurobiology of Disease.

[16]  Nicola J. Ray,et al.  Local field potential beta activity in the subthalamic nucleus of patients with Parkinson's disease is associated with improvements in bradykinesia after dopamine and deep brain stimulation , 2008, Experimental Neurology.

[17]  G. Buzsáki Large-scale recording of neuronal ensembles , 2004, Nature Neuroscience.

[18]  Abdulhamit Subasi,et al.  Classification of EEG signals using neural network and logistic regression , 2005, Comput. Methods Programs Biomed..

[19]  Tipu Z. Aziz,et al.  Stimulating the human midbrain to reveal the link between pain and blood pressure , 2006, Pain.

[20]  Vladimir Litvak,et al.  Synchronized neural oscillations and the pathophysiology of Parkinson's disease. , 2013, Current opinion in neurology.

[21]  Qian Liu Kernel Local Sparse Representation Based Classifier , 2014, Neural Processing Letters.

[22]  Alessandro Ulrici,et al.  WPTER: wavelet packet transform for efficient pattern recognition of signals , 2001 .

[23]  Michel Le Van Quyen,et al.  Analysis of dynamic brain oscillations: methodological advances , 2007, Trends in Neurosciences.

[24]  Alexander L Green,et al.  Long-term outcomes of deep brain stimulation for neuropathic pain. , 2013, Neurosurgery.

[25]  Saurabh Prasad,et al.  Sparse representation-based classification: Orthogonal least squares or orthogonal matching pursuit? , 2016, Pattern Recognit. Lett..

[26]  Alexander L Green,et al.  Deep Brain Stimulation for Neuropathic Pain , 2006, Neuromodulation : journal of the International Neuromodulation Society.

[27]  Tipu Aziz,et al.  Comparison of oscillatory activity in subthalamic nucleus in Parkinson's disease and dystonia , 2017, Neurobiology of Disease.

[28]  K. Zaghloul,et al.  Temporal macrodynamics and microdynamics of the postoperative impedance at the tissue–electrode interface in deep brain stimulation patients , 2013, Journal of Neurology, Neurosurgery & Psychiatry.

[29]  T. Aziz,et al.  Characteristics of local field potentials correlate with pain relief by deep brain stimulation , 2016, Clinical Neurophysiology.

[30]  Desire L. Massart,et al.  Noise suppression and signal compression using the wavelet packet transform , 1997 .

[31]  Xingxing Jin,et al.  Neuronal Entropy-Rate Feature of Entopeduncular Nucleus in Rat Model of Parkinson's Disease , 2016, Int. J. Neural Syst..

[32]  W R Jankel,et al.  Sleep Spindles , 1985, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[33]  Wen Zheng,et al.  The role of local field potential coupling in epileptic synchronization , 2013, Neural regeneration research.

[34]  Tipu Z. Aziz,et al.  Deep brain stimulation for pain relief: A meta-analysis , 2005, Journal of Clinical Neuroscience.

[35]  A. Priori,et al.  Rhythm-specific pharmacological modulation of subthalamic activity in Parkinson's disease , 2004, Experimental Neurology.

[36]  P. Brown,et al.  Different patterns of local field potentials from limbic DBS targets in patients with major depressive and obsessive compulsive disorder , 2014, Molecular Psychiatry.

[37]  Victoria Peterson,et al.  Local Discriminant Wavelet Packet Basis for Signal Classification in Brain Computer Interface , 2015 .

[38]  David L. Donoho,et al.  De-noising by soft-thresholding , 1995, IEEE Trans. Inf. Theory.

[39]  V. Samar,et al.  Wavelet Analysis of Neuroelectric Waveforms: A Conceptual Tutorial , 1999, Brain and Language.

[40]  Bruno Averbeck,et al.  Resonance in subthalamo-cortical circuits in Parkinson's disease , 2009, Brain : a journal of neurology.

[41]  Ahmad Reza Naghsh-Nilchi,et al.  Efficient Image Denoising Method Based on a New Adaptive Wavelet Packet Thresholding Function , 2012, IEEE Transactions on Image Processing.

[42]  I. Johnstone,et al.  Ideal spatial adaptation by wavelet shrinkage , 1994 .

[43]  Johannes Sarnthein,et al.  High thalamocortical theta coherence in patients with neurogenic pain , 2008, NeuroImage.

[44]  J. Gross,et al.  Brain Rhythms of Pain , 2017, Trends in Cognitive Sciences.

[45]  Nouna Kettaneh,et al.  Statistical Modeling by Wavelets , 1999, Technometrics.

[46]  Bin Feng,et al.  Pattern Identification of Subthalamic Local Field Potentials in Parkinson’s Disease , 2017 .

[47]  Zarko Cucej,et al.  Entropy-threshold method for best basis selection , 2001, Image Vis. Comput..

[48]  P. Brown,et al.  Beta band stability over time correlates with Parkinsonian rigidity and bradykinesia , 2012, Experimental Neurology.

[49]  J. Stein,et al.  NEURAL SIGNATURES IN PATIENTS WITH NEUROPATHIC PAIN , 2009, Neurology.

[50]  P. Brown,et al.  Adaptive Deep Brain Stimulation In Advanced Parkinson Disease , 2013, Annals of neurology.

[51]  Aimin Wang,et al.  A spatial-frequency-temporal optimized feature sparse representation-based classification method for motor imagery EEG pattern recognition , 2017, Medical & Biological Engineering & Computing.

[52]  Dong Wen,et al.  Review of Sparse Representation-Based Classification Methods on EEG Signal Processing for Epilepsy Detection, Brain-Computer Interface and Cognitive Impairment , 2016, Front. Aging Neurosci..

[53]  N. Ince,et al.  Long-term recordings of local field potentials from implanted deep brain stimulation electrodes. , 2012, Neurosurgery.

[54]  Zuoqiang Shi,et al.  Sparse time-frequency decomposition based on dictionary adaptation , 2016, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[55]  A. Priori,et al.  Adaptive deep brain stimulation (aDBS) controlled by local field potential oscillations , 2013, Experimental Neurology.

[56]  Karl J. Friston,et al.  LFP and oscillations—what do they tell us? , 2015, Current Opinion in Neurobiology.

[57]  Reza Tafreshi,et al.  Automated Real-Time Epileptic Seizure Detection in Scalp EEG Recordings Using an Algorithm Based on Wavelet Packet Transform , 2010, IEEE Transactions on Biomedical Engineering.

[58]  Wolf-Julian Neumann,et al.  Enhanced low‐frequency oscillatory activity of the subthalamic nucleus in a patient with dystonia , 2012, Movement disorders : official journal of the Movement Disorder Society.

[59]  P. E. Tikkanen,et al.  Nonlinear wavelet and wavelet packet denoising of electrocardiogram signal , 1999, Biological Cybernetics.

[60]  J. Sarnthein,et al.  The Size of Neuronal Assemblies, Their Frequency of Synchronization, and Their Cognitive Function , 2009 .

[61]  Jun Zhou,et al.  Local and global regularized sparse coding for data representation , 2016, Neurocomputing.

[62]  Suyi Zhang,et al.  An automatic classifier of pain scores in chronic pain patients from local field potentials recordings , 2013, 2013 6th International IEEE/EMBS Conference on Neural Engineering (NER).

[63]  Tipu Z. Aziz,et al.  Ventral periaqueductal grey stimulation alters heart rate variability in humans with chronic pain , 2010, Experimental Neurology.

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

[65]  Tipu Z. Aziz,et al.  Deep brain stimulation for the alleviation of post-stroke neuropathic pain , 2006, Pain.

[66]  Hong Yu,et al.  Resting Beta Hypersynchrony in Secondary Dystonia and Its Suppression During Pallidal Deep Brain Stimulation in DYT3+ Lubag Dystonia , 2013, Neuromodulation : journal of the International Neuromodulation Society.

[67]  Berj L. Bardakjian,et al.  A Wavelet Packet-Based Algorithm for the Extraction of Neural Rhythms , 2009, Annals of Biomedical Engineering.

[68]  C. Phillips,et al.  Sleep Spindles as an Electrographic Element: Description and Automatic Detection Methods , 2016, Neural plasticity.

[69]  Ribana Roscher,et al.  Shapelet-Based Sparse Representation for Landcover Classification of Hyperspectral Images , 2016, IEEE Transactions on Geoscience and Remote Sensing.

[70]  Charles L. Wilson,et al.  Quantitative analysis of high-frequency oscillations (80-500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. , 2002, Journal of neurophysiology.