Frequency and time-frequency analysis of intraoperative ECoG during awake brain stimulation

Electrocortical stimulation remains the standard for functional brain mapping of eloquent areas to prevent postoperative functional deficits. The aim of this study was to investigate whether the short-train technique (monopolar stimulation) and Penfield's technique (bipolar stimulation) would induce different effects on brain oscillatory activity in awake patients, as quantified by electrocorticography (ECoG). The study population was seven patients undergoing brain tumor surgery. Intraoperative bipolar and monopolar electrical stimulation for cortical mapping was performed during awake surgery. ECoG was recorded using 1 × 8 electrode strip. Spectral estimation was calculated using a parametric approach based on an autoregressive model. Wavelet-based time-frequency analysis was then applied to evaluate the temporal evolution of brain oscillatory activity. Both monopolar and bipolar stimulation produced an increment in delta and a decrease in beta powers for the motor and the sensory channels. These phenomena lasted about 4 s. Comparison between monopolar and bipolar stimulation showed no significant difference in brain activity. Given the importance of quantitative signal analysis for evaluating response accuracy, ECoG recording during electrical stimulation is necessary to characterize the dynamic processes underlying changes in cortical responses in vivo. This study is a preliminary approach to the quantitative analysis of post-stimulation ECoG signals.

[1]  Elena L. Glassman,et al.  A wavelet-like filter based on neuron action potentials for analysis of human scalp electroencephalographs , 2005, IEEE Transactions on Biomedical Engineering.

[2]  B. Gordon,et al.  Induced electrocorticographic gamma activity during auditory perception , 2001, Clinical Neurophysiology.

[3]  G. Pfurtscheller,et al.  Event-related synchronization (ERS) in the alpha band--an electrophysiological correlate of cortical idling: a review. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[4]  H. Duffau,et al.  Intra-Operative Direct Electrical Stimulations of the Central Nervous System: The Salpêtrière Experience With 60 Patients , 1999, Acta Neurochirurgica.

[5]  G A Ojemann,et al.  Brain mapping techniques to maximize resection, safety, and seizure control in children with brain tumors. , 1989, Neurosurgery.

[6]  G. Ojemann,et al.  Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. , 1989, Journal of neurosurgery.

[7]  J. Schramm,et al.  Somatosensory evoked potential phase reversal and direct motor cortex stimulation during surgery in and around the central region. , 1996, Neurosurgery.

[8]  R. Sahjpaul.  Awake Craniotomy: Controversies, Indications and Techniques in the Surgical Treatment of Temporal Lobe Epilepsy , 2000, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[9]  M. Steriade.  Grouping of brain rhythms in corticothalamic systems , 2006, Neuroscience.

[10]  Mitchel S. Berger,et al.  Low grade gliomas: Functional mapping resection strategies, extent of resection, and outcome , 1997, Journal of Neuro-Oncology.

[11]  Theodoros Kombos,et al.  Neurophysiological basis of direct cortical stimulation and applied neuroanatomy of the motor cortex: a review. , 2009, Neurosurgical focus.

[12]  H. Duffau,et al.  Intraoperative electrical stimulation in awake craniotomy: methodological aspects of current practice. , 2010, Neurosurgical focus.

[13]  J. V. Van Buren,et al.  Mechanism and localization of speech in the parietotemporal cortex. , 1978, Neurosurgery.

[14]  W. Penfield,et al.  SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION , 1937 .

[15]  W. Blume,et al.  Properties of after-discharges from cortical electrical stimulation in focal epilepsies , 2004, Clinical Neurophysiology.

[16]  R. Duckrow,et al.  Local spatial effect of 50 Hz cortical stimulation in humans , 2008, Epilepsia.

[17]  Tomas Sauer,et al.  Conventional and wavelet coherence applied to sensory-evoked electrical brain activity , 2006, IEEE Transactions on Biomedical Engineering.

[18]  K R Hess,et al.  Neurosurgical outcomes in a modern series of 400 craniotomies for treatment of parenchymal tumors. , 1998, Neurosurgery.

[19]  F. Sala,et al.  Subcortical stimulation (mapping) of the corticospinal tract , 2011, Clinical Neurophysiology.

[20]  A. Gorman,et al.  Differential patterns of activation of the pyramidal system elicited by surface anodal and cathodal cortical stimulation. , 1966, Journal of neurophysiology.

[21]  C. G. Phillips,et al.  Selective excitation of corticofugal neurones by surface‐anodal stimulation of the baboon's motor cortex , 1962, The Journal of physiology.

[22]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. , 1998, Brain : a journal of neurology.

[23]  S. Goldring,et al.  Localization of function in the excision of lesions from the sensorimotor region. , 1984, Journal of neurosurgery.

[24]  M. Berger,et al.  Functional mapping-guided resection of low-grade gliomas. , 1995, Clinical neurosurgery.

[25]  Mitchel S. Berger,et al.  Brain Mapping Techniques to Maximize Resection, Safety, and Seizure Control in Children with Brain Tumors , 1989 .

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

[27]  M. Bernstein.  Outpatient Craniotomy for Brain Tumor: A Pilot Feasibility Study in 46 Patients , 2001, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[28]  C. Crainiceanu,et al.  Electrocorticographic high gamma activity versus electrical cortical stimulation mapping of naming. , 2005, Brain : a journal of neurology.

[29]  MARC JOBERT,et al.  Wavelets—a new tool in sleep biosignal analysis , 1994, Journal of sleep research.

[30]  B. O'neill,et al.  Awake craniotomy for aggressive resection of primary gliomas located in eloquent brain. , 2001, Mayo Clinic proceedings.

[31]  M M Haglund,et al.  Resection of intrinsic tumors from nondominant face motor cortex using stimulation mapping: report of two cases. , 1991, Surgical neurology.

[32]  R. Irizarry,et al.  Electrocorticographic gamma activity during word production in spoken and sign language , 2001, Neurology.

[33]  S. Mallat.  A wavelet tour of signal processing , 1998 .

[34]  Gert Pfurtscheller,et al.  Event-related desynchronization. Handbook of Electroencephalography and Clinical Neurophysiology. Revised Series, Volume 6 , 1999 .

[35]  M. Bernstein,et al.  Awake craniotomy with brain mapping as the routine surgical approach to treating patients with supratentorial intraaxial tumors: a prospective trial of 200 cases. , 1999, Journal of neurosurgery.

[36]  R. Warnick,et al.  Neurosurgical Outcomes in a Modern Series of 400 Craniotomies for Treatment of Parenchymal Tumors , 1998 .

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

[38]  C. Ajmone‐Marsan.  Depth electrography and electrocorticography , 1980 .

[39]  J. Marshall,et al.  Functional anatomy of the human brain , 2004 .

[40]  V. Deletis.  What does intraoperative monitoring of motor evoked potentials bring to the neurosurgeon? , 2005, Acta Neurochirurgica.

[41]  Gert Pfurtscheller,et al.  Basic concepts on EEG synchronization and desynchronization , 1999 .

[42]  Ashwini Sharan,et al.  The effectiveness of low‐frequency stimulation for mapping cortical function , 2008, Epilepsia.

[43]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. , 1998, Brain : a journal of neurology.

[44]  R. Lesser,et al.  Short-term variations in response distribution to cortical stimulation , 2008, Brain : a journal of neurology.

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

[46]  Vernon L. Towle,et al.  Intra-operative localization of sensorimotor cortex by cortical somatosensory evoked potentials: From analysis of waveforms to dipole source modeling , 2005, Acta Neurochirurgica.

[47]  V. Seifert,et al.  Transcranial and direct cortical stimulation for motor evoked potential monitoring in intracerebral aneurysm surgery , 2007, Neurophysiologie Clinique/Clinical Neurophysiology.

[48]  O. Suess,et al.  Comparison Between Monopolar and Bipolar Electrical Stimulation of the Motor Cortex , 1999, Acta Neurochirurgica.

[49]  Lotfi Senhadji,et al.  Epileptic transient detection: wavelets and time-frequency approaches , 2002, Neurophysiologie Clinique/Clinical Neurophysiology.

[50]  G Pfurtscheller,et al.  Event-related desynchronization during motor behavior and visual information processing. , 1991, Electroencephalography and clinical neurophysiology. Supplement.

[51]  Osvaldo A. Rosso,et al.  Wavelet analysis of generalized tonic-clonic epileptic seizures , 2003, Signal Process..

[52]  U. D. Schmid,et al.  Safe surgery of lesions near the motor cortex using intra-operative mapping techniques: a report on 50 patients , 2005, Acta Neurochirurgica.

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

[54]  G Pfurtscheller,et al.  Mu‐rhythm changes in brisk and slow self‐paced finger movements , 1996, Neuroreport.

[55]  A. Szelényi,et al.  Motor evoked potentials. , 2019, Journal of neurosurgery.

[56]  J. Sobesky,et al.  Surgery of intrinsic cerebral neoplasms in eloquent areas under local anesthesia. , 2000, Neurochirurgia.

[57]  P. Lanteri,et al.  Surgical treatment of high-grade gliomas in motor areas. The impact of different supportive technologies: a 171-patient series , 2010, Journal of Neuro-Oncology.

[58]  R P Lesser,et al.  Cortical Afterdischarge and Functional Response Thresholds: Results of Extraoperative Testing , 1984, Epilepsia.

[59]  V. Seifert,et al.  Intra-operative subcortical electrical stimulation: A comparison of two methods , 2011, Clinical Neurophysiology.