Neurovascular coupling and oximetry during epileptic events

Epilepsy is an abnormal brain state in which a large population of neurons is synchronously active, causing an enormous increase in metabolic demand. Recent investigations using high-resolution imaging techniques, such as optical recording of intrinsic signals and voltagesensitive dyes, as well as measurements with oxygen-sensitive electrodes have elucidated the spatiotemporal relationship between neuronal activity, cerebral blood volume, and oximetry in vivo. A focal decrease in tissue oxygenation and a focal increase in deoxygenated hemoglobin occurs following both interictal and ictal events. This “epileptic dip” in oxygenation can persist for the duration of an ictal event, suggesting that cerebral blood flow is inadequate to meet metabolic demand. A rapid focal increase in cerebral blood flow and cerebral blood volume also accompanies epileptic events; however, this increase in perfusion soon (>2 s) spreads to a larger area of the cortex than the excitatory change in membrane potential. Investigations in humans during neurosurgical operations have confirmed the laboratory data derived from animal studies. These data not only have clinical implications for the interpretation of noninvasive imaging studies such as positron emission tomography, single-photon emission tomography, and functional magnetic resonance imaging but also provide a mechanism for the cognitive decline in patients with chronic epilepsy.

[1]  R. Buxton The Elusive Initial Dip , 2001, NeuroImage.

[2]  G. Hagemann,et al.  Brain Hypometabolism in a Model of Chronic Focal Epilepsy in Rat Neocortex , 1998, Epilepsia.

[3]  C. Sherrington,et al.  On the Regulation of the Blood‐supply of the Brain , 1890, The Journal of physiology.

[4]  R. Yuste,et al.  The neocortical local circuit--a research workshop held in Sde-Boker, Israel, May 4-8, 1997. , 1997, Somatosensory & motor research.

[5]  Jeffrey R Tenney,et al.  fMRI of Brain Activation in a Genetic Rat Model of Absence Seizures , 2004, Epilepsia.

[6]  Arthur W. Toga,et al.  Evaluation of coupling between optical intrinsic signals and neuronal activity in rat somatosensory cortex , 2003, NeuroImage.

[7]  U. Lindauer,et al.  Neuronal activity-induced changes of local cerebral microvascular blood oxygenation in the rat: effect of systemic hyperoxia or hypoxia , 2003, Brain Research.

[8]  M Ingvar,et al.  Metabolic Changes in Cerebral Cortex, Hippocampus, and Cerebellum During Sustained Bicuculline‐Induced Seizures , 1981, Journal of neurochemistry.

[9]  J. London,et al.  Optical recordings of the cortical response to whisker stimulation before and after the addition of an epileptogenic agent , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  Arthur W. Toga,et al.  Shedding light on brain mapping: advances in human optical imaging , 2003, Trends in Neurosciences.

[11]  N. Logothetis,et al.  Functional imaging of the monkey brain , 1999, Nature Neuroscience.

[12]  A. Villringer,et al.  No Evidence for Early Decrease in Blood Oxygenation in Rat Whisker Cortex in Response to Functional Activation , 2001, NeuroImage.

[13]  Louis Lemieux,et al.  Comparison of Spike-Triggered Functional MRI BOLD Activation and EEG Dipole Model Localization , 2001, NeuroImage.

[14]  R. Keynes,et al.  Opacity changes in stimulated nerve , 1949, The Journal of physiology.

[15]  Arthur W. Toga,et al.  Temporal spatial differences observed by functional MRI and human intraoperative optical imaging. , 2001 .

[16]  Arthur W. Toga,et al.  Functional Signal- and Paradigm-Dependent Linear Relationships between Synaptic Activity and Hemodynamic Responses in Rat Somatosensory Cortex , 2004, The Journal of Neuroscience.

[17]  Astrid Nehlig,et al.  Local Cerebral Blood Flow during Lithium–Pilocarpine Seizures in the Developing and Adult Rat: Role of Coupling between Blood Flow and Metabolism in the Genesis of Neuronal Damage , 2002, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[18]  J. Mayhew,et al.  Spectroscopic Analysis of Neural Activity in Brain: Increased Oxygen Consumption Following Activation of Barrel Cortex , 2000, NeuroImage.

[19]  Mamoru Tamura,et al.  Reassessment of activity-related optical signals in somatosensory cortex by an algorithm with wavelength-dependent path length. , 2002, The Japanese journal of physiology.

[20]  A W Toga,et al.  Optical intrinsic signal imaging in a rodent seizure model , 2000, Neurology.

[21]  L. Guan,et al.  Epileptiform activity can be initiated in various neocortical layers: an optical imaging study. , 1999, Journal of neurophysiology.

[22]  M M Haglund,et al.  Intraoperative hippocampal electrocorticography to predict the extent of hippocampal resection in temporal lobe epilepsy surgery. , 2000, Journal of neurosurgery.

[23]  R. Kajiwara,et al.  Voltage-sensitive dye versus intrinsic signal optical imaging: comparison of optically determined functional maps from rat barrel cortex , 2001, Neuroreport.

[24]  Martin Ingvar,et al.  Cerebral Blood Flow and Metabolic Rate during Seizures a , 1986 .

[25]  N. Kreisman,et al.  Relative Hypoperfusion in Rat Cerebral Cortex during Recurrent Seizures , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[26]  Amiram Grinvald,et al.  Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns , 1991, Nature.

[27]  S. Bahar,et al.  Intrinsic optical signal imaging of neocortical seizures: the ‘epileptic dip’ , 2006, Neuroreport.

[28]  M. Haglund,et al.  Optical Imaging of Epileptiform Activity in Human Neocortex , 2004, Epilepsia.

[29]  Theodore H Schwartz,et al.  The Application of Optical Recording of Intrinsic Signals to Simultaneously Acquire Functional, Pathological and Localizing Information and Its Potential Role in Neurosurgery , 2005, Stereotactic and Functional Neurosurgery.

[30]  R. Frostig,et al.  Optical imaging of neuronal activity. , 1988, Physiological reviews.

[31]  A W Toga,et al.  Topographical and temporal specificity of human intraoperative optical intrinsic signals , 1998, Neuroreport.

[32]  Jean Gotman,et al.  The BOLD Response to Interictal Epileptiform Discharges , 2002, NeuroImage.

[33]  Ying Zheng,et al.  Spectroscopic Analysis of Changes in Remitted Illumination: The Response to Increased Neural Activity in Brain , 1999, NeuroImage.

[34]  A. Grinvald,et al.  Increased cortical oxidative metabolism due to sensory stimulation: implications for functional brain imaging. , 1999, Science.

[35]  P. Schwartzkroin,et al.  Dissociation of Synchronization and Excitability in Furosemide Blockade of Epileptiform Activity , 1995, Science.

[36]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[37]  Fahmeed Hyder,et al.  Dynamic fMRI and EEG Recordings during Spike-Wave Seizures and Generalized Tonic-Clonic Seizures in WAG/Rij Rats , 2004, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[38]  J. Hablitz,et al.  Spread of epileptiform activity in the immature rat neocortex studied with voltage-sensitive dyes and laser scanning microscopy. , 1994, Journal of neurophysiology.

[39]  R. Freeman,et al.  Single-Neuron Activity and Tissue Oxygenation in the Cerebral Cortex , 2003, Science.

[40]  Y Tsau,et al.  Initiation of spontaneous epileptiform activity in the neocortical slice. , 1998, Journal of neurophysiology.

[41]  Astrid Nehlig,et al.  Dynamic Variations of Local Cerebral Blood Flow in Maximal Electroshock Seizures in the Rat , 2002, Epilepsia.

[42]  Amiram Grinvald,et al.  Evidence and Lack of Evidence for the Initial Dip in the Anesthetized Rat: Implications for Human Functional Brain Imaging , 2001, NeuroImage.

[43]  C. Gilbert,et al.  Long-range horizontal connections and their role in cortical reorganization revealed by optical recording of cat primary visual cortex , 1995, Nature.

[44]  Theodore H. Schwartz,et al.  In vivo optical mapping of epileptic foci and surround inhibition in ferret cerebral cortex , 2001, Nature Medicine.

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

[46]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Nathan S. Hageman,et al.  Columnar Specificity of Microvascular Oxygenation and Volume Responses: Implications for Functional Brain Mapping , 2004, The Journal of Neuroscience.

[48]  G. Ojemann,et al.  Optical imaging of epileptiform and functional activity in human cerebral cortex , 1992, Nature.

[49]  B. MacVicar,et al.  Mapping patterns of neuronal activity and seizure propagation by imaging intrinsic optical signals in the isolated whole brain of the guinea-pig , 1994, Neuroscience.

[50]  Dae-Shik Kim,et al.  High-resolution mapping of iso-orientation columns by fMRI , 2000, Nature Neuroscience.

[51]  A. Grinvald,et al.  Compartment-Resolved Imaging of Activity-Dependent Dynamics of Cortical Blood Volume and Oximetry , 2005, The Journal of Neuroscience.

[52]  S. Bahar,et al.  Temporal Dependence in Uncoupling of Blood Volume and Oxygenation during Interictal Epileptiform Events in Rat Neocortex , 2005, The Journal of Neuroscience.

[53]  Reinhold Ludwig,et al.  Corticothalamic Modulation during Absence Seizures in Rats: A Functional MRI Assessment , 2003, Epilepsia.

[54]  D. Treiman,et al.  Interical spiking increases 2‐deoxy[14C]glucose uptake and c‐fos—like reacitivity , 1994, Annals of neurology.

[55]  R. Buxton,et al.  Dynamics of blood flow and oxygenation changes during brain activation: The balloon model , 1998, Magnetic resonance in medicine.

[56]  U. Kuhnt,et al.  Epileptiform Activity in the Guinea‐pig Neocortical Slice Spreads Preferentially along Supragranular Layers—Recordings with Voltage‐sensitive Dyes , 1995, The European journal of neuroscience.

[57]  A. Grinvald,et al.  The Cortical Representation of the Hand in Macaque and Human Area S-I: High Resolution Optical Imaging , 2001, The Journal of Neuroscience.

[58]  Jian-Young Wu,et al.  Initiation of spontaneous epileptiform events in the rat neocortex in vivo. , 2004, Journal of neurophysiology.

[59]  Theodore H Schwartz,et al.  Intraoperative optical imaging of human face cortical topography: a case study , 2004, Neuroreport.

[60]  A. Grinvald,et al.  Columnar Resolution of Blood Volume and Oximetry Functional Maps in the Behaving Monkey Implications for fMRI , 2004, Neuron.

[61]  Theodore H Schwartz,et al.  Optical imaging of epileptiform events in visual cortex in response to patterned photic stimulation. , 2003, Cerebral cortex.

[62]  A. Toga,et al.  Temporal spatial differences observed by functional MRI and human intraoperative optical imaging , 2001, NeuroImage.

[63]  U. Kuhnt,et al.  Optical recording of epileptiform voltage changes in the neocortical slice , 2004, Experimental Brain Research.

[64]  M. Mintun,et al.  Nonoxidative glucose consumption during focal physiologic neural activity. , 1988, Science.

[65]  J. Detre,et al.  Temporal dynamics of the partial pressure of brain tissue oxygen during functional forepaw stimulation in rats , 2001, Neuroscience Letters.

[66]  Theodore H. Schwartz,et al.  Blood volume and hemoglobin oxygenation response following electrical stimulation of human cortex , 2006, NeuroImage.

[67]  D. Ts'o,et al.  Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[68]  C. Schwarz,et al.  Spatiotemporal effects of microstimulation in rat neocortex: a parametric study using multielectrode recordings. , 2003, Journal of neurophysiology.

[69]  A. Grinvald,et al.  Interactions Between Electrical Activity and Cortical Microcirculation Revealed by Imaging Spectroscopy: Implications for Functional Brain Mapping , 1996, Science.

[70]  J. Mayhew,et al.  Concurrent Optical Imaging Spectroscopy and Laser-Doppler Flowmetry: The Relationship between Blood Flow, Oxygenation, and Volume in Rodent Barrel Cortex , 2001, NeuroImage.

[71]  K. Sako,et al.  Uncoupling of local blood flow and metabolism in the hippocampal CA3 in kainic acid-induced limbic seizure status , 1990, Neuroscience.

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

[73]  Tadashi Nariai,et al.  Intraoperative intrinsic optical imaging of neuronal activity from subdivisions of the human primary somatosensory cortex. , 2002, Cerebral cortex.

[74]  A. Toga,et al.  Linear and Nonlinear Relationships between Neuronal Activity, Oxygen Metabolism, and Hemodynamic Responses , 2004, Neuron.

[75]  M. Ingvar Cerebral blood flow and metabolic rate during seizures. Relationship to epileptic brain damage. , 1986, Annals of the New York Academy of Sciences.