Intracranial neuronal ensemble recordings and analysis in epilepsy

Pathological neuronal firing was demonstrated 50 years ago as the hallmark of epileptically transformed cortex with the use of implanted microelectrodes. Since then, microelectrodes remained only experimental tools in humans to detect unitary neuronal activity to reveal physiological and pathological brain functions. This recording technique has evolved substantially in the past few decades; however, based on recent human data implying their usefulness as diagnostic tools, we expect a substantial increase in the development of microelectrodes in the near future. Here, we review the technological background and history of microelectrode array development for human examinations in epilepsy, including discussions on of wire-based and microelectrode arrays fabricated using micro-electro-mechanical system (MEMS) techniques and novel future techniques to record neuronal ensemble. We give an overview of clinical and surgical considerations, and try to provide a list of probes on the market with their availability for human recording. Then finally, we briefly review the literature on modulation of single neuron for the treatment of epilepsy, and highlight the current topics under examination that can be background for the future development.

[1]  K. E. Jones,et al.  A glass/silicon composite intracortical electrode array , 2006, Annals of Biomedical Engineering.

[2]  E. Halgren,et al.  Spatiotemporal dynamics of neocortical excitation and inhibition during human sleep , 2012, Proceedings of the National Academy of Sciences.

[3]  Steve S. Chung,et al.  Electrical stimulation of the anterior nucleus of thalamus for treatment of refractory epilepsy , 2010, Epilepsia.

[4]  Emery N Brown,et al.  Heterogeneous neuronal firing patterns during interictal epileptiform discharges in the human cortex. , 2010, Brain : a journal of neurology.

[5]  K. Wise,et al.  Performance of planar multisite microprobes in recording extracellular single-unit intracortical activity , 1988, IEEE Transactions on Biomedical Engineering.

[6]  T L Babb,et al.  Epileptogenesis of human limbic neurons in psychomotor epileptics. , 1976, Electroencephalography and clinical neurophysiology.

[7]  Technique and results of micro-electrode recording in human epileptogenic foci. , 1967, Electroencephalography and clinical neurophysiology.

[8]  T L Babb,et al.  Firing patterns of human limbic neurons during stereoencephalography (SEEG) and clinical temporal lobe seizures. , 1987, Electroencephalography and clinical neurophysiology.

[9]  Guglielmo Foffani,et al.  Reduced Spike-Timing Reliability Correlates with the Emergence of Fast Ripples in the Rat Epileptic Hippocampus , 2007, Neuron.

[10]  Itzhak Fried,et al.  Increased Fast ripple to ripple Ratios Correlate with Reduced Hippocampal Volumes and Neuron Loss in Temporal Lobe Epilepsy Patients , 2007, Epilepsia.

[11]  J. Csicsvari,et al.  Intracellular features predicted by extracellular recordings in the hippocampus in vivo. , 2000, Journal of neurophysiology.

[12]  G. Buzsáki,et al.  Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  Paras R. Patel,et al.  Ultrasmall implantable composite microelectrodes with bioactive surfaces for chronic neural interfaces. , 2012, Nature materials.

[14]  T. Babb,et al.  Inhibition in synchronously firing human hippocampal neurons , 1989, Epilepsy Research.

[15]  R. Yuste,et al.  Evidence of an inhibitory restraint of seizure activity in humans , 2012, Nature Communications.

[16]  Charles L. Wilson,et al.  Cell Type-Specific Firing during Ripple Oscillations in the Hippocampal Formation of Humans , 2008, The Journal of Neuroscience.

[17]  John Adams Assessing , 2020, Transport Planning.

[18]  E. Halgren,et al.  Responses of Human Anterior Cingulate Cortex Microdomains to Error Detection, Conflict Monitoring, Stimulus-Response Mapping, Familiarity, and Orienting , 2005, The Journal of Neuroscience.

[19]  B. Litt,et al.  High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings. , 2008, Brain : a journal of neurology.

[20]  E. Halgren,et al.  Properties of in vivo interictal spike generation in the human subiculum. , 2008, Brain : a journal of neurology.

[21]  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.

[22]  G. Ojemann,et al.  Neurons in human epileptic cortex: Correlation between unit and EEG activity , 1982, Annals of neurology.

[23]  Hiroshi Tamura,et al.  Tracking Spike-Amplitude Changes to Improve the Quality of Multineuronal Data Analysis , 2007, IEEE Transactions on Biomedical Engineering.

[24]  Gonzalo Alarcón,et al.  In vivo neuronal firing patterns during human epileptiform discharges replicated by electrical stimulation , 2012, Clinical Neurophysiology.

[25]  Sergey Shleev,et al.  Biofuel Cell Based on Microscale Nanostructured Electrodes with Inductive Coupling to Rat Brain Neurons , 2013, Scientific Reports.

[26]  David A. Boas,et al.  Intracranial microprobe for evaluating neuro-hemodynamic coupling in unanesthetized human neocortex , 2009, Journal of Neuroscience Methods.

[27]  Tony A. Fields,et al.  Cerebral microdialysis combined with single-neuron and electroencephalographic recording in neurosurgical patients. Technical note. , 1999, Journal of neurosurgery.

[28]  B. McNaughton,et al.  Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex , 1995, Journal of Neuroscience Methods.

[29]  E. Lettich,et al.  Cerebral Responses to Electrical Stimulation of Tooth Pulp in Man , 1974, Journal of dental research.

[30]  Nima Dehghani,et al.  The Human K-Complex Represents an Isolated Cortical Down-State , 2009, Science.

[31]  P. House High-Frequency Electroencephalographic Oscillations Correlate With Outcome of Epilepsy Surgery , 2010 .

[32]  Karen Moxon Multichannel Electrode Design: Considerations for Different Applications , 1998 .

[33]  M. Burghoff,et al.  Towards non-invasive multi-unit spike recordings: Mapping 1kHz EEG signals over human somatosensory cortex , 2011, Clinical Neurophysiology.

[34]  Justin C. Sanchez,et al.  Abiotic-biotic characterization of Pt/Ir microelectrode arrays in chronic implants , 2014, Front. Neuroeng..

[35]  Christof Koch,et al.  Single-neuron correlates of subjective vision in the human medial temporal lobe , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[36]  T. Babb,et al.  Analysis of extracellular firing patterns of deep temporal lobe structures in man. , 1973, Electroencephalography and clinical neurophysiology.

[37]  C. Koch,et al.  On the origin of the extracellular action potential waveform: A modeling study. , 2006, Journal of neurophysiology.

[38]  Erika Pastrana,et al.  Optogenetics: controlling cell function with light , 2011, Nature Methods.

[39]  C. Koch,et al.  Invariant visual representation by single neurons in the human brain , 2005, Nature.

[40]  Tsai-Wen Chen,et al.  Comprehensive imaging of cortical networks , 2015, Current Opinion in Neurobiology.

[41]  J. F. Rubinson,et al.  Histocompatibility and in vivo signal throughput for PEDOT, PEDOP, P3MT, and polycarbazole electrodes. , 2012, Journal of biomedical materials research. Part A.

[42]  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.

[43]  W. Rall Electrophysiology of a dendritic neuron model. , 1962, Biophysical journal.

[44]  István Ulbert,et al.  Multiple microelectrode-recording system for human intracortical applications , 2001, Journal of Neuroscience Methods.

[45]  H. Plenk The role of materials biocompatibility for functional electrical stimulation applications. , 2011, Artificial organs.

[46]  T. Kosaka,et al.  Quantitative analysis of GABA-like-immunoreactive and parvalbumin-containing neurons in the CA1 region of the rat hippocampus using a stereological method, the disector , 1994, Experimental Brain Research.

[47]  K. Berg,et al.  Assessing autophagy in the context of photodynamic therapy , 2010, Autophagy.

[48]  R A Normann,et al.  The Utah intracortical Electrode Array: a recording structure for potential brain-computer interfaces. , 1997, Electroencephalography and clinical neurophysiology.

[49]  David C. Martin,et al.  Chronic neural recordings using silicon microelectrode arrays electrochemically deposited with a poly(3,4-ethylenedioxythiophene) (PEDOT) film , 2006, Journal of neural engineering.

[50]  T. Blanche,et al.  Polytrodes: high-density silicon electrode arrays for large-scale multiunit recording. , 2005, Journal of neurophysiology.

[51]  E. Halgren,et al.  Laminar profile of spontaneous and evoked theta: Rhythmic modulation of cortical processing during word integration , 2015, Neuropsychologia.

[52]  Ueli Rutishauser,et al.  Single-Trial Learning of Novel Stimuli by Individual Neurons of the Human Hippocampus-Amygdala Complex , 2006, Neuron.

[53]  H Petsche,et al.  A 16-fold semi-microelectrode for intracortical recording of field potentials. , 1979, Electroencephalography and clinical neurophysiology.

[54]  E. Halgren,et al.  Interictal spike-wave complexes in the human medial temporal lobe: typical topography and comparisons with cognitive potentials. , 1986, Electroencephalography and clinical neurophysiology.

[55]  B. Renshaw,et al.  ACTIVITY OF ISOCORTEX AND HIPPOCAMPUS: ELECTRICAL STUDIES WITH MICRO-ELECTRODES , 1940 .

[56]  J. Gotman,et al.  High frequency oscillations (80–500 Hz) in the preictal period in patients with focal seizures , 2009, Epilepsia.

[57]  S. Sarasso,et al.  Local aspects of sleep: observations from intracerebral recordings in humans. , 2012, Progress in brain research.

[58]  Ravi V. Bellamkonda,et al.  Controlled release of anti-inflammatory agent alpha-MSH from neural implants. , 2005, Journal of controlled release : official journal of the Controlled Release Society.

[59]  M Steriade,et al.  Intracellular study of excitability in the seizure-prone neocortex in vivo. , 1999, Journal of neurophysiology.

[60]  J. Csicsvari,et al.  Massively parallel recording of unit and local field potentials with silicon-based electrodes. , 2003, Journal of neurophysiology.

[61]  B L McNaughton,et al.  Dynamics of the hippocampal ensemble code for space. , 1993, Science.

[62]  C. A. Marsan,et al.  Cellular Mechanisms in Experimental Epileptic Seizures , 1964, Science.

[63]  E. Reynolds Todd, Hughlings Jackson, and the electrical basis of epilepsy , 2001, The Lancet.

[64]  Philip A. Starr,et al.  Placement of Deep Brain Stimulators into the Subthalamic Nucleus or Globus pallidus internus: Technical Approach , 2003, Stereotactic and Functional Neurosurgery.

[65]  István Ulbert,et al.  In vivo laminar electrophysiology co-registered with histology in the hippocampus of patients with temporal lobe epilepsy , 2004, Experimental Neurology.

[66]  E. Halgren,et al.  Early discrimination of coherent versus incoherent motion by multiunit and synaptic activity in human putative MT+ , 2001, Human brain mapping.

[67]  G. Buzsáki,et al.  NeuroGrid: recording action potentials from the surface of the brain , 2014, Nature Neuroscience.

[68]  Valéria Csépe,et al.  A new multielectrode for chronic recording of intracortical field potentials in cats , 1982, Physiology & Behavior.

[69]  C. Nicholson,et al.  Experimental optimization of current source-density technique for anuran cerebellum. , 1975, Journal of neurophysiology.

[70]  Dim-Lee Kwong,et al.  Development of silicon electrode enhanced by carbon nanotube and gold nanoparticle composites on silicon neural probe fabricated with complementary metal-oxide-semiconductor process , 2014 .

[71]  Nicole C. Swann,et al.  Therapeutic deep brain stimulation reduces cortical phase-amplitude coupling in Parkinson's disease , 2015, Nature Neuroscience.

[72]  Arne D. Ekstrom,et al.  Brain Oscillations Control Timing of Single-Neuron Activity in Humans , 2007, The Journal of Neuroscience.

[73]  Charles L. Wilson,et al.  Single Neuron Activity in Human Hippocampus and Amygdala during Recognition of Faces and Objects , 1997, Neuron.

[74]  Huanan Zhang,et al.  Layered nanocomposites from gold nanoparticles for neural prosthetic devices. , 2012, Nano letters.

[75]  Timothy G. Constandinou,et al.  Hierarchical Adaptive Means (HAM) clustering for hardware-efficient, unsupervised and real-time spike sorting , 2014, Journal of Neuroscience Methods.

[76]  M. Curtis,et al.  Interictal spikes in focal epileptogenesis , 2001, Progress in Neurobiology.

[77]  H. Vaughan,et al.  A new multielectrode array for the simultaneous recording of field potentials and unit activity. , 1981, Electroencephalography and clinical neurophysiology.

[78]  Wei He,et al.  Nanoscale laminin coating modulates cortical scarring response around implanted silicon microelectrode arrays , 2006, Journal of neural engineering.

[79]  H. Petsche,et al.  A multielectrode for intracortical recordings produced by thin-film technology. , 1977, Electroencephalography and clinical neurophysiology.

[80]  D. Jay,et al.  Selective destruction of protein function by chromophore-assisted laser inactivation. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[81]  E. Halgren,et al.  Laminar Analysis of Human Neocortical Interictal Spike Generation and Propagation: Current Source Density and Multiunit Analysis In Vivo , 2004, Epilepsia.

[82]  K. Miller,et al.  Subthalamic Nucleus Neurons Are Synchronized to Primary Motor Cortex Local Field Potentials in Parkinson's Disease , 2013, The Journal of Neuroscience.

[83]  J. Gotman,et al.  High‐frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery , 2010, Annals of neurology.

[84]  Daniel R. Merrill Materials considerations of implantable neuroengineering devices for clinical use , 2014 .

[85]  Jean Gotman,et al.  Interictal high-frequency oscillations (100-500 Hz) in the intracerebral EEG of epileptic patients. , 2007, Brain : a journal of neurology.

[86]  O. Prohaska,et al.  Thin-Film Multiple Electrode Probes: Possibilities and Limitations , 1986, IEEE Transactions on Biomedical Engineering.

[87]  Justin C. Sanchez,et al.  Quantifying long-term microelectrode array functionality using chronic in vivo impedance testing , 2012, Journal of neural engineering.

[88]  Charles L. Wilson,et al.  Three-dimensional Hippocampal Atrophy Maps Distinguish Two Common Temporal Lobe Seizure–onset Patterns Full-length Original Research , 2022 .

[89]  C. McIntyre,et al.  Sources and effects of electrode impedance during deep brain stimulation , 2006, Clinical Neurophysiology.

[90]  Eric A. Vitriol,et al.  Chromophore-assisted laser inactivation in cell biology. , 2008, Trends in cell biology.

[91]  Klaus Obermayer,et al.  Bayes optimal template matching for spike sorting – combining fisher discriminant analysis with optimal filtering , 2015, Journal of Computational Neuroscience.

[92]  B Sakmann,et al.  Patch clamp techniques for studying ionic channels in excitable membranes. , 1984, Annual review of physiology.

[93]  M. Ward,et al.  Toward a comparison of microelectrodes for acute and chronic recordings , 2009, Brain Research.

[94]  Saeid Sanei,et al.  Extracellular spike detection from multiple electrode array using novel intelligent filter and ensemble fuzzy decision making , 2015, Journal of Neuroscience Methods.

[95]  K. Wise,et al.  An integrated-circuit approach to extracellular microelectrodes. , 1970, IEEE transactions on bio-medical engineering.

[96]  Antonio V. Delgado-Escueta,et al.  Interictal Epileptiform Discharges in Partial Epilepsy: Complex Neurobiological Mechanisms Based on Experimental and Clinical Evidence -- Jasper's Basic Mechanisms of the Epilepsies , 2012 .

[97]  Hanna Damasio,et al.  Single-neuron responses to emotional visual stimuli recorded in human ventral prefrontal cortex , 2001, Nature Neuroscience.

[98]  Joseph W. Freeman Materials Science and Engineering C: Editorial , 2011 .

[99]  A. Ward,et al.  Observations on single units in chronic cortical epileptic foci and in normal or strychninized cortex. , 1955, Electroencephalography and Clinical Neurophysiology.

[100]  Eran Stark,et al.  Large-scale, high-density (up to 512 channels) recording of local circuits in behaving animals. , 2014, Journal of neurophysiology.

[101]  Mark R. Bower,et al.  Microseizures and the spatiotemporal scales of human partial epilepsy. , 2010, Brain : a journal of neurology.

[102]  Craig T. Nordhausen,et al.  Optimizing recording capabilities of the Utah Intracortical Electrode Array , 1994, Brain Research.

[103]  Katharina T. Hofer,et al.  The hippocampal CA3 region can generate two distinct types of sharp wave‐ripple complexes, in vitro , 2015, Hippocampus.

[104]  Jean-Marc Fellous,et al.  In vitro model of glial scarring around neuroelectrodes chronically implanted in the CNS. , 2006, Biomaterials.

[105]  J. Csicsvari,et al.  Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. , 2000, Journal of neurophysiology.

[106]  O. B. Ozdoganlar,et al.  Chronic tissue response to carboxymethyl cellulose based dissolvable insertion needle for ultra-small neural probes. , 2014, Biomaterials.

[107]  E. Halgren,et al.  Laminar analysis of slow wave activity in humans. , 2010, Brain : a journal of neurology.

[108]  K. Bujarski,et al.  Exploring emotions using invasive methods: review of 60 years of human intracranial electrophysiology. , 2014, Social cognitive and affective neuroscience.

[109]  Vincenzo Crunelli,et al.  The thalamocortical network as a single slow wave-generating unit , 2015, Current Opinion in Neurobiology.

[110]  M J Kahana,et al.  Methods for implantation of micro-wire bundles and optimization of single/multi-unit recordings from human mesial temporal lobe , 2014, Journal of neural engineering.

[111]  Barjor Gimi,et al.  In vitro and in vivo evaluation of SU-8 biocompatibility. , 2013, Materials science & engineering. C, Materials for biological applications.

[112]  Richard Miles,et al.  Different mechanisms of ripple‐like oscillations in the human epileptic subiculum , 2015, Annals of neurology.

[113]  Luciano Fadiga,et al.  Smaller, softer, lower-impedance electrodes for human neuroprosthesis: a pragmatic approach , 2014, Front. Neuroeng..

[114]  Charles L. Wilson,et al.  High‐frequency oscillations recorded in human medial temporal lobe during sleep , 2004, Annals of neurology.

[115]  C. Schroeder,et al.  Microphysiology of Epileptiform Activity in Human Neocortex , 2008, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

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

[117]  Charles L. Wilson,et al.  High‐frequency oscillations in human brain , 1999, Hippocampus.

[118]  Yasin Temel,et al.  Current perspectives on deep brain stimulation for severe neurological and psychiatric disorders , 2015, Neuropsychiatric disease and treatment.

[119]  Itzhak Fried,et al.  Sleep States Differentiate Single Neuron Activity Recorded from Human Epileptic Hippocampus, Entorhinal Cortex, and Subiculum , 2002, The Journal of Neuroscience.

[120]  Patrick Ruther,et al.  In vivo validation of the electronic depth control probes , 2014, Biomedizinische Technik. Biomedical engineering.

[121]  E. Halgren,et al.  Single-neuron dynamics in human focal epilepsy , 2011, Nature Neuroscience.

[122]  Daryl R. Kipke,et al.  Wireless implantable microsystems: high-density electronic interfaces to the nervous system , 2004, Proceedings of the IEEE.

[123]  Sang Beom Jun,et al.  In-vivo Optical Measurement of Neural Activity in the Brain , 2013, Experimental neurobiology.

[124]  J. Csicsvari,et al.  Oscillatory Coupling of Hippocampal Pyramidal Cells and Interneurons in the Behaving Rat , 1999, The Journal of Neuroscience.

[125]  Szabolcs Káli,et al.  Physiological sharp wave-ripples and interictal events in vitro: what's the difference? , 2014, Brain : a journal of neurology.

[126]  R. Normann,et al.  A method for pneumatically inserting an array of penetrating electrodes into cortical tissue , 2006, Annals of Biomedical Engineering.

[127]  I. Fried,et al.  Internally Generated Reactivation of Single Neurons in Human Hippocampus During Free Recall , 2008, Science.

[128]  C. Nicholson,et al.  Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum. , 1975, Journal of neurophysiology.