Blood volume and hemoglobin oxygenation response following electrical stimulation of human cortex

Our understanding of perfusion-based human brain mapping techniques relies on a detailed knowledge of the relationship between neuronal activity and cerebrovascular hemodynamics. We performed optical imaging of intrinsic signals at wavelengths sensitive to total hemoglobin (Hbt; which correlate with cerebral blood volume (CBV)) and deoxygenated hemoglobin (Hbr) directly in humans during neurosurgical operations and investigated the optical signals associated with bipolar cortical stimulation at a range of amplitudes. Cortical stimulation elicited a rapid focal increase in Hbr (initial dip) in all subjects. An equally rapid increase in Hbt (<200 ms), with a slightly higher signal-to-noise ratio, was also highly localized for <2 s in spite of the non-columnar nature of the stimulus, after which the signal spread to adjacent gyri. A later decrease in Hbr (>3 s), which is relevant to the blood oxygen level dependent (BOLD) signal, was poorly localized. Increasing the stimulus amplitude elicited a linear increase in the area of the optical signal for Hbt and the initial dip but not the late decrease in Hbr, and a nonlinear increase in optical signal amplitude with a plateau effect for initial dip, Hbt and late decrease in Hbr.

[1]  R S Fisher,et al.  Motor and sensory cortex in humans: topography studied with chronic subdural stimulation. , 1992, Neurosurgery.

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

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

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

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

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

[7]  K Sartor,et al.  Extirpation of glioblastomas: MR and CT follow-up of residual tumor and regrowth patterns. , 1993, AJNR. American journal of neuroradiology.

[8]  N. Thakor,et al.  Determination of current density distributions generated by electrical stimulation of the human cerebral cortex. , 1993, Electroencephalography and clinical neurophysiology.

[9]  A. Grinvald,et al.  A tandem-lens epifluorescence macroscope: Hundred-fold brightness advantage for wide-field imaging , 1991, Journal of Neuroscience Methods.

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

[11]  T A Woolsey,et al.  Neuronal units linked to microvascular modules in cerebral cortex: response elements for imaging the brain. , 1996, Cerebral cortex.

[12]  M. Raichle,et al.  Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[13]  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.

[14]  Nader Pouratian,et al.  Spatial/temporal correlation of BOLD and optical intrinsic signals in humans , 2002, Magnetic resonance in medicine.

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

[16]  H. Scheich,et al.  New Insights into the Hemodynamic Blood Oxygenation Level-Dependent Response through Combination of Functional Magnetic Resonance Imaging and Optical Recording in Gerbil Barrel Cortex , 2000, The Journal of Neuroscience.

[17]  C. Rovainen,et al.  Journal of Cerebral Blood Flow and Metabolism Localized Dynamic Changes in Cortical Blood Flow with Whisker Stimulation Corresponds to Matched Vascular and Neuronal Architecture of Rat Barrels , 2022 .

[18]  G. Ojemann Cortical organization of language , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  J. B. Ranck,et al.  Which elements are excited in electrical stimulation of mammalian central nervous system: A review , 1975, Brain Research.

[20]  C Sato,et al.  Analysis of Optical Signals Evoked by Peripheral Nerve Stimulation in Rat Somatosensory Cortex: Dynamic Changes in Hemoglobin Concentration and Oxygenation , 1999, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[21]  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.

[22]  O D Creutzfeldt,et al.  Relations between EEG phenomena and potentials of single cortical cells. I. Evoked responses after thalamic and erpicortical stimulation. , 1966, Electroencephalography and clinical neurophysiology.

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

[24]  S. Ogawa,et al.  BOLD Based Functional MRI at 4 Tesla Includes a Capillary Bed Contribution: Echo‐Planar Imaging Correlates with Previous Optical Imaging Using Intrinsic Signals , 1995, Magnetic resonance in medicine.

[25]  J. Hennig,et al.  Observation of a fast response in functional MR , 1994, Magnetic resonance in medicine.

[26]  X. Hu,et al.  Evaluation of the early response in fMRI in individual subjects using short stimulus duration , 1997, Magnetic resonance in medicine.

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

[28]  G. Krüger,et al.  Temporal characteristics of oxygenation‐sensitive MRI responses to visual activation in humans , 1998, Magnetic resonance in medicine.

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

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

[31]  J. Mayhew,et al.  Cerebral Vasomotion: A 0.1-Hz Oscillation in Reflected Light Imaging of Neural Activity , 1996, NeuroImage.

[32]  N. Harel,et al.  Blood capillary distribution correlates with hemodynamic-based functional imaging in cerebral cortex. , 2002, Cerebral cortex.

[33]  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.

[34]  William B. Levy,et al.  Stimulation-dependent depression of neurotransmitter release in brain: [Ca2+]0 dependence , 1978, Brain Research.

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

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

[37]  O. Devinsky,et al.  Function‐Specific High‐Probability “Nodes” Identified in Posterior Language Cortex , 1999, Epilepsia.

[38]  Theodore H. Schwartz,et al.  In Vivo Intrinsic Optical Signal Imaging of Neocortical Epilepsy , 2005 .

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

[40]  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.

[41]  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.

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

[43]  Seong-Gi Kim,et al.  Early Temporal Characteristics of Cerebral Blood Flow and Deoxyhemoglobin Changes during Somatosensory Stimulation , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[44]  Thomas A Woolsey,et al.  Spatial Integration of Vascular Changes with Neural Activity in Mouse Cortex , 2002, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[45]  Patricia A. Broderick,et al.  Bioimaging in Neurodegeneration , 2005 .

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

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

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

[49]  R. Fisher,et al.  Motor and sensory cortex in humans: topography studied with chronic subdural stimulation. , 1992 .

[50]  B. Ances,et al.  Coupling of Changes in Cerebral Blood Flow with Neural Activity: What Must Initially Dip Must Come Back Up , 2004, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

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

[52]  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.

[53]  D. McCreery,et al.  Histological evaluation of neural damage from electrical stimulation: considerations for the selection of parameters for clinical application. , 1981, Neurosurgery.

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

[55]  A. Rodríguez-Baeza,et al.  Morphological characteristics and distribution pattern of the arterial vessels in human cerebral cortex: A scanning electron microscope study , 1998, The Anatomical record.

[56]  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.

[57]  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.

[58]  A. Dale,et al.  Coupling of Total Hemoglobin Concentration, Oxygenation, and Neural Activity in Rat Somatosensory Cortex , 2003, Neuron.

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

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

[61]  R. Freeman,et al.  High-resolution neurometabolic coupling revealed by focal activation of visual neurons , 2004, Nature Neuroscience.

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

[63]  B. Rosen,et al.  MRI measurement of the temporal evolution of relative CMRO2 during rat forepaw stimulation , 1999, Magnetic resonance in medicine.