Automatic Detection of High Frequency Oscillations of Neural Signals in Epileptic Patients

Epilepsy is one the most common neurological disorders. For patients suffering from epilepsy who are medically intractable, in certain cases surgical resection of pathologic brain tissue is one remaining possibility. Prior to surgery, intracranial Electroencephalography (IEEG) study is conducted to localize seizure-generating zones. IEEG typically consists of studying epileptiform spikes and seizure discharges; however some researchers have observed short bursts of high frequency oscillations (HFOs), mostly in the range of 100-500 Hz in the seizure generating areas. A retrospective correlation analysis between the post-surgical outcome and HFO generating tissue supports the idea that HFO events may play a fundamental role in epilepsy and epileptogenesis. Recently, HFO events have been scored visually by clinicians. Typically, it is necessary to record IEEG for several days or weeks to collect sufficient epileptiform activities for precise evaluation. Needless to say, manual review of the data makes visual scoring an extremely tiresome process in which subjectivity is inevitable. Due to the recent explosion of HFO research, the development of algorithms for automatic detection of HFO events poses a great benefit to researchers and clinicians. In the literature, two methods have been widely used for automatic detection of HFO events based on the energy of the signal in the 100-500 Hz frequency band. In this thesis, we present three new methods for automatic detection of HFO events based on the sharpness property of the IEEG signals. By using simulated and real-data signals, the performance of the proposed methods are compared to the existing energy-based approaches using sensitivity and specificity metrics. Additionally, we present the clinical implication of the HFO event detections for four epileptic patients. The results indicate that the performance of the proposed detectors are robust and stable and do not deteriorate in the presence of the noise and artifacts.

[1]  Use of intracranial neurophysiologic recording techniques in the evaluation for epilepsy surgery in children. , 1992, Singapore medical journal.

[2]  Charles L. Wilson,et al.  High‐frequency Oscillations after Status Epilepticus: Epileptogenesis and Seizure Genesis , 2004, Epilepsia.

[3]  John Nolte,et al.  The Human Brain An Introduction to Its Functional Anatomy , 2013 .

[4]  J C Principe,et al.  A study on the best order for autoregressive EEG modelling. , 1987, International journal of bio-medical computing.

[5]  D. Barth,et al.  Submillisecond Synchronization of Fast Electrical Oscillations in Neocortex , 2003, The Journal of Neuroscience.

[6]  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.

[7]  W. Walter Slow potential waves in the human brain associated with expectancy, attention and decision , 1964, Archiv für Psychiatrie und Nervenkrankheiten.

[8]  J. W. Tukey,et al.  The Measurement of Power Spectra from the Point of View of Communications Engineering , 1958 .

[9]  L. Zetterberg Estimation of parameters for a linear difference equation with application to EEG analysis , 1969 .

[10]  Michel Le Van Quyen,et al.  Epileptogenic Actions of GABA and Fast Oscillations in the Developing Hippocampus , 2005, Neuron.

[11]  M. A. Werz,et al.  The Human Brain , 1993, Neurology.

[12]  J. Fell,et al.  Ripples in the medial temporal lobe are relevant for human memory consolidation. , 2008, Brain : a journal of neurology.

[13]  Charles L. Wilson,et al.  Hippocampal and Entorhinal Cortex High‐Frequency Oscillations (100–500 Hz) in Human Epileptic Brain and in Kainic Acid‐Treated Rats with Chronic Seizures , 1999, Epilepsia.

[14]  J R Smith,et al.  Automatic analysis and detection of EEG spikes. , 1974, IEEE transactions on bio-medical engineering.

[15]  G. Flint,et al.  Seizures and epilepsy. , 1988, British journal of neurosurgery.

[16]  A. Pérez-Villalba Rhythms of the Brain, G. Buzsáki. Oxford University Press, Madison Avenue, New York (2006), Price: GB £42.00, p. 448, ISBN: 0-19-530106-4 , 2008 .

[17]  Akio Ikeda,et al.  Ictal wideband ECoG: Direct comparison between ictal slow shifts and high frequency oscillations , 2011, Clinical Neurophysiology.

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

[19]  Jean Gotman,et al.  Improving the identification of High Frequency Oscillations , 2009, Clinical Neurophysiology.

[20]  H. Berger Über das Elektrenkephalogramm des Menschen , 1938, Archiv für Psychiatrie und Nervenkrankheiten.

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

[22]  G. Buzsáki,et al.  High-Frequency Oscillations in the Output Networks of the Hippocampal–Entorhinal Axis of the Freely Behaving Rat , 1996, The Journal of Neuroscience.

[23]  J. Gotman,et al.  High-frequency oscillations (HFOs) in clinical epilepsy , 2012, Progress in Neurobiology.

[24]  Jean Gotman,et al.  Value of electrical stimulation and high frequency oscillations (80–500 Hz) in identifying epileptogenic areas during intracranial EEG recordings , 2010, Epilepsia.

[25]  Brian Litt,et al.  Human and automated detection of high-frequency oscillations in clinical intracranial EEG recordings , 2007, Clinical Neurophysiology.

[26]  K. Baba,et al.  P6-4 Very high frequency oscillations (over 1000 Hz) in human epilepsy , 2010, Clinical Neurophysiology.

[27]  Ayako Ochi,et al.  Focal resection of fast ripples on extraoperative intracranial EEG improves seizure outcome in pediatric epilepsy , 2011, Epilepsia.

[28]  Jean Gotman,et al.  Automatic detector of High Frequency Oscillations for human recordings with macroelectrodes , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

[29]  B. McNaughton,et al.  EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus. , 2007, Journal of neurophysiology.

[30]  Ayako Ochi,et al.  Dynamic Changes of Ictal High‐Frequency Oscillations in Neocortical Epilepsy: Using Multiple Band Frequency Analysis , 2007, Epilepsia.

[31]  P B Fenwick,et al.  Application of the autoregressive model to E.E.G. analysis. , 1969, Agressologie: revue internationale de physio-biologie et de pharmacologie appliquees aux effets de l'agression.

[32]  E. Niedermeyer The epilepsies : diagnosis and management , 1990 .

[33]  R. Ward,et al.  EMG and EOG artifacts in brain computer interface systems: A survey , 2007, Clinical Neurophysiology.

[34]  H. Jasper Report of the committee on methods of clinical examination in electroencephalography , 1958 .

[35]  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.

[36]  Ayako Ochi,et al.  Topographic Movie of Ictal High‐Frequency Oscillations on the Brain Surface Using Subdural EEG in Neocortical Epilepsy , 2006, Epilepsia.

[37]  Jean Gotman,et al.  High frequency oscillations and seizure frequency in patients with focal epilepsy , 2009, Epilepsy Research.

[38]  Katsuhiro Kobayashi,et al.  High‐frequency oscillations in idiopathic partial epilepsy of childhood , 2011, Epilepsia.

[39]  Charles L. Wilson,et al.  Local Generation of Fast Ripples in Epileptic Brain , 2002, The Journal of Neuroscience.

[40]  Y. Xiao,et al.  Steady-state analysis of a plain gradient algorithm for a second-order adaptive IIR notch filter with constrained poles and zeros , 2001 .

[41]  G. Buzsáki,et al.  Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  Rüdiger Köhling,et al.  Network mechanisms for fast ripple activity in epileptic tissue , 2011, Epilepsy Research.

[43]  R. Pearson,et al.  The Human Nervous System. Basic Elements of Structure and Function , 1967, The Yale Journal of Biology and Medicine.

[44]  J. Gotman,et al.  Automatic recognition and quantification of interictal epileptic activity in the human scalp EEG. , 1976, Electroencephalography and Clinical Neurophysiology.

[45]  G. Paxinos,et al.  THE HUMAN NERVOUS SYSTEM , 1975 .

[46]  Gregory Worrell,et al.  High-Frequency Oscillations Recorded on Scalp EEG , 2012, Epilepsy currents.

[47]  C. Schroeder,et al.  Spatial characterization of interictal high frequency oscillations in epileptic neocortex , 2009, Brain : a journal of neurology.

[48]  M.N.S. Swamy,et al.  Model-based seizure detection method using statistically optimal null filters , 2004, The 26th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[49]  J. Gotman,et al.  High frequency oscillations in intracranial EEGs mark epileptogenicity rather than lesion type. , 2009, Brain : a journal of neurology.

[50]  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.

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

[52]  Jan Chrastina,et al.  Interictal high-frequency oscillations indicate seizure onset zone in patients with focal cortical dysplasia , 2010, Epilepsy Research.

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

[54]  J. Gotman,et al.  High-frequency oscillations during human focal seizures. , 2006, Brain : a journal of neurology.

[55]  Song Zhang,et al.  Ictal high‐frequency oscillations in neocortical epilepsy: implications for seizure localization and surgical resection , 2011, Epilepsia.

[56]  Helmut L. Haas,et al.  High frequency (200 Hz) oscillations and firing patterns in the basolateral amygdala and dorsal endopiriform nucleus of the behaving rat , 2003, Behavioural Brain Research.

[57]  Helen J. Cross,et al.  A Possible Role for Gap Junctions in Generation of Very Fast EEG Oscillations Preceding the Onset of, and Perhaps Initiating, Seizures , 2001, Epilepsia.

[58]  Seward B. Rutkove,et al.  The clinical neurophysiology primer , 2007 .

[59]  Itzhak Fried,et al.  Large-Scale Microelectrode Recordings of High-Frequency Gamma Oscillations in Human Cortex during Sleep , 2010, The Journal of Neuroscience.

[60]  B. Litt,et al.  Automatic detection of high frequency epileptiform oscillations from intracranial EEG recordings of patients with neocortical epilepsy , 2005, 2005 IEEE Region 5 and IEEE Denver Section Technical, Professional and Student Development Workshop.

[61]  H W Shipton,et al.  EGG analysis: a history and a prospectus. , 1975, Annual review of biophysics and bioengineering.

[62]  I. Módy,et al.  High-frequency oscillations : What is normal and what is not ? , 2008 .

[63]  Shuang Wang,et al.  Ripple classification helps to localize the seizure‐onset zone in neocortical epilepsy , 2013, Epilepsia.

[64]  P. Prior,et al.  EEG Technology, 3rd ed , 1982 .

[65]  Eileen Luders,et al.  Three‐dimensional surface maps link local atrophy and fast ripples in human epileptic hippocampus , 2009, Annals of neurology.

[66]  G. Buzsáki,et al.  High-frequency network oscillation in the hippocampus. , 1992, Science.

[67]  H R Townsend,et al.  The automatic estimation of epileptic spike activity. , 1973, International journal of bio-medical computing.

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

[69]  Ernst Fernando Lopes Da Silva Niedermeyer,et al.  Electroencephalography, basic principles, clinical applications, and related fields , 1982 .

[70]  B Saltzberg,et al.  Detection of focal depth spiking in the scalp EEG of monkeys. , 1971, Electroencephalography and clinical neurophysiology.

[71]  Eishi Asano,et al.  Spontaneous and visually driven high‐frequency oscillations in the occipital cortex: Intracranial recording in epileptic patients , 2012, Human brain mapping.

[72]  R. Caton,et al.  IV.—Interim Report on Investigation of the Electric Currents of the Brain. , 1971 .

[73]  Jeffery A. Hall,et al.  Interictal high‐frequency oscillations (80–500 Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain , 2008, Epilepsia.

[74]  G. Li,et al.  Plain gradient based direct frequency estimation using second-order constrained adaptive IIR notch filter , 2004 .

[75]  B. Litt,et al.  High-frequency oscillations and seizure generation in neocortical epilepsy. , 2004, Brain : a journal of neurology.

[76]  Houman Khosravani,et al.  Spatial localization and time‐dependant changes of electrographic high frequency oscillations in human temporal lobe epilepsy , 2009, Epilepsia.

[77]  J. Martinerie,et al.  Mapping interictal oscillations greater than 200 Hz recorded with intracranial macroelectrodes in human epilepsy. , 2010, Brain : a journal of neurology.

[78]  Jean Gotman,et al.  Detection of changes of high-frequency activity by statistical time-frequency analysis in epileptic spikes , 2009, Clinical Neurophysiology.

[79]  Brian Litt,et al.  High-Frequency Oscillations Detected in Epileptic Networks Using Swarmed Neural-Network Features , 2007, Annals of Biomedical Engineering.

[80]  Pierre LeVan,et al.  High‐Frequency Intracerebral EEG Activity (100–500 Hz) Following Interictal Spikes , 2006, Epilepsia.

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