Evidence that cerebral blood volume can provide brain activation maps with better spatial resolution than deoxygenated hemoglobin

With the aim of evaluating the relative performance of hemodynamic contrasts for mapping brain activity, the spatio-temporal response of oxy-, deoxy-, and total-hemoglobin concentrations were imaged with diffuse optical tomography during electrical stimulation of the rat somatosensory cortex. For both 6-s and 30-s stimulus durations, total hemoglobin images provided smaller activation areas than oxy- or deoxy-hemoglobin images. In addition, analysis of regions of interest near the sagittal sinus vein show significantly greater contrast in both oxy- and deoxy-relative to total hemoglobin, suggesting that oximetric contrasts have larger draining vein contributions compared to total hemoglobin contrasts under the given stimulus conditions. These results indicate that total hemoglobin and cerebral blood volume may have advantages as hemodynamic mapping contrasts, particularly for large amplitude, longer duration stimulus paradigms.

[1]  E. Gratton,et al.  Near-infrared study of fluctuations in cerebral hemodynamics during rest and motor stimulation: temporal analysis and spatial mapping. , 2000, Medical physics.

[2]  Takashi Kusaka,et al.  Noninvasive optical imaging in the visual cortex in young infants , 2004, Human brain mapping.

[3]  Thomas T. Liu,et al.  Discrepancies between BOLD and flow dynamics in primary and supplementary motor areas: application of the balloon model to the interpretation of BOLD transients , 2004, NeuroImage.

[4]  Seong-Gi Kim,et al.  Relative changes of cerebral arterial and venous blood volumes during increased cerebral blood flow: Implications for BOLD fMRI , 2001, Magnetic resonance in medicine.

[5]  R. Koehler,et al.  Dependency of Cortical Functional Hyperemia to Forepaw Stimulation on Epoxygenase and Nitric Oxide Synthase Activities in Rats , 2004, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[6]  B. Rosen,et al.  Dynamic functional imaging of relative cerebral blood volume during rat forepaw stimulation , 1998, Magnetic resonance in medicine.

[7]  B. Rosen,et al.  Regional sensitivity and coupling of BOLD and CBV changes during stimulation of rat brain , 2001, Magnetic resonance in medicine.

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

[9]  K. Sakatani,et al.  Cerebral blood oxygenation changes induced by auditory stimulation in newborn infants measured by near infrared spectroscopy. , 1999, Early human development.

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

[11]  D. Boas,et al.  Functional Imaging with Diffusing Light , 2003 .

[12]  D. Boas,et al.  Experimental images of heterogeneous turbid media by frequency-domain diffusing-photon tomography. , 1995, Optics letters.

[13]  Seong-Gi Kim,et al.  Comparison of diffusion‐weighted high‐resolution CBF and spin‐echo BOLD fMRI at 9.4 T , 2002, Magnetic resonance in medicine.

[14]  Takashi Kusaka,et al.  Estimation of Regional Cerebral Blood Flow Distribution in Infants by Near-Infrared Topography Using Indocyanine Green , 2001, NeuroImage.

[15]  C. Iadecola.  Neurovascular regulation in the normal brain and in Alzheimer's disease , 2004, Nature Reviews Neuroscience.

[16]  K. Kubota,et al.  Cortical Mapping of Gait in Humans: A Near-Infrared Spectroscopic Topography Study , 2001, NeuroImage.

[17]  Dae-Shik Kim,et al.  Localized cerebral blood flow response at submillimeter columnar resolution , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[18]  A Villringer,et al.  Separation of changes in light scattering and chromophore concentrations during cortical spreading depression in rats. , 1998, Optics letters.

[19]  P. Zaramella,et al.  Brain Auditory Activation Measured by Near-Infrared Spectroscopy (NIRS) in Neonates , 2001, Pediatric Research.

[20]  S. Tomura,et al.  Cerebral blood volume and oxygenation among poststroke hemiplegic patients: effects of 13 rehabilitation tasks measured by near-infrared spectroscopy. , 2000, Archives of physical medicine and rehabilitation.

[21]  K. Sakatani,et al.  Auditory-evoked cerebral oxygenation changes in hypoxic-ischemic encephalopathy of newborn infants monitored by near infrared spectroscopy. , 2002, Early human development.

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

[23]  Hideaki Koizumi,et al.  Prefrontal cortical activation associated with working memory in adults and preschool children: an event-related optical topography study. , 2004, Cerebral cortex.

[24]  A. Maki,et al.  Activation of the visual cortex imaged by 24-channel near-infrared spectroscopy. , 2000, Journal of biomedical optics.

[25]  J. R. Baker,et al.  The intravascular contribution to fmri signal change: monte carlo modeling and diffusion‐weighted studies in vivo , 1995, Magnetic resonance in medicine.

[26]  Takashi Kusaka,et al.  Functional imaging of the brain in sedated newborn infants using near infrared topography during passive knee movement , 2001, Neuroscience Letters.

[27]  A. Yodh,et al.  Diffuse Optical Tomography of Cerebral Blood Flow, Oxygenation, and Metabolism in Rat during Focal Ischemia , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[28]  M. Malkoff,et al.  Near infrared spectroscopy (NIRS) distinguishes seizure types , 2000, Seizure.

[29]  L. O. Svaasand,et al.  Boundary conditions for the diffusion equation in radiative transfer. , 1994, Journal of the Optical Society of America. A, Optics, image science, and vision.

[30]  G. Orban,et al.  Visual Motion Processing Investigated Using Contrast Agent-Enhanced fMRI in Awake Behaving Monkeys , 2001, Neuron.

[31]  David A Boas,et al.  Temporal comparison of functional brain imaging with diffuse optical tomography and fMRI during rat forepaw stimulation , 2003, Physics in medicine and biology.

[32]  J. Hebden.  Advances in optical imaging of the newborn infant brain. , 2003, Psychophysiology.

[33]  Seong-Gi Kim,et al.  Simultaneous Blood Oxygenation Level-Dependent and Cerebral Blood Flow Functional Magnetic Resonance Imaging during Forepaw Stimulation in the Rat , 1999, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[34]  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.

[35]  M. C. Angulo,et al.  Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation , 2003, Nature Neuroscience.

[36]  D. Boas,et al.  Volumetric diffuse optical tomography of brain activity. , 2003, Optics letters.

[37]  K. Uğurbil,et al.  High‐resolution, spin‐echo BOLD, and CBF fMRI at 4 and 7 T , 2002, Magnetic resonance in medicine.

[38]  G. Taga,et al.  Brain imaging in awake infants by near-infrared optical topography , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[39]  J P Culver,et al.  Optimization of optode arrangements for diffuse optical tomography: A singular-value analysis. , 2001, Optics letters.

[40]  A H Hielscher,et al.  Three-dimensional optical tomographic brain imaging in small animals, part 1: hypercapnia. , 2004, Journal of biomedical optics.

[41]  R. Alfano,et al.  Intracerebral hemodynamics probed by near infrared spectroscopy in the transition between wakefulness and sleep , 2000, Brain Research.

[42]  Himender Makker,et al.  Measurement of changes in cytochrome oxidase redox state during obstructive sleep apnea using near-infrared spectroscopy. , 2003, Sleep.

[43]  D. Delpy,et al.  Characterization of the near infrared absorption spectra of cytochrome aa3 and haemoglobin for the non-invasive monitoring of cerebral oxygenation. , 1988, Biochimica et biophysica acta.

[44]  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.

[45]  K. Kubota,et al.  Longitudinal Optical Imaging Study for Locomotor Recovery After Stroke , 2003, Stroke.

[46]  J. Detre,et al.  Dynamic Changes in Cerebral Blood Flow, O2 Tension, and Calculated Cerebral Metabolic Rate of O2 during Functional Activation Using Oxygen Phosphorescence Quenching , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[47]  Danilo P. Mandic,et al.  Signal nonlinearity in fMRI: a comparison between BOLD and MION , 2003, IEEE Transactions on Medical Imaging.

[48]  Anders M. Dale,et al.  Repeated fMRI Using Iron Oxide Contrast Agent in Awake, Behaving Macaques at 3 Tesla , 2002, NeuroImage.

[49]  B. Rosen,et al.  Evidence of a Cerebrovascular Postarteriole Windkessel with Delayed Compliance , 1999, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[50]  A. Villringer,et al.  Non-invasive optical spectroscopy and imaging of human brain function , 1997, Trends in Neurosciences.

[51]  J. Detre,et al.  Spatiotemporal Quantification of Cerebral Blood Flow during Functional Activation in Rat Somatosensory Cortex using Laser-Speckle Flowmetry , 2004, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[52]  Avinash C. Kak,et al.  Principles of computerized tomographic imaging , 2001, Classics in applied mathematics.

[53]  R. Poldrack,et al.  Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy? , 2003, Physics in medicine and biology.

[54]  J. Detre,et al.  Diffuse optical measurement of blood flow, blood oxygenation, and metabolism in a human brain during sensorimotor cortex activation. , 2004, Optics letters.

[55]  A. Villringer,et al.  Cerebral haemoglobin oxygenation during sustained visual stimulation--a near-infrared spectroscopy study. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[57]  W Hacke,et al.  Bedside monitoring of cerebral blood flow in patients with acute hemispheric stroke , 2000, Critical care medicine.

[58]  David A Boas,et al.  Optode positional calibration in diffuse optical tomography. , 2003, Applied optics.

[59]  Turgut Durduran,et al.  Diffuse optical measurement of hemoglobin and cerebral blood flow in rat brain during hypercapnia, hypoxia and cardiac arrest. , 2003, Advances in experimental medicine and biology.

[60]  A. Dale,et al.  Simultaneous imaging of total cerebral hemoglobin concentration, oxygenation, and blood flow during functional activation. , 2003, Optics letters.

[61]  R. Buxton,et al.  A Model for the Coupling between Cerebral Blood Flow and Oxygen Metabolism during Neural Stimulation , 1997, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

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

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

[64]  A. Villringer,et al.  Cerebral oxygenation changes in response to motor stimulation. , 1996, Journal of applied physiology.

[65]  F. Hyder,et al.  Dynamic Magnetic Resonance Imaging of the Rat Brain during Forepaw Stimulation , 1994, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[66]  A. Yodh,et al.  Frequency-domain multiplexing system for in vivo diffuse light measurements of rapid cerebral hemodynamics. , 2003, Applied optics.

[67]  Janette Atkinson,et al.  Regional Hemodynamic Responses to Visual Stimulation in Awake Infants , 1998, Pediatric Research.

[68]  R. Frostig.  In Vivo Optical Imaging of Brain Function , 2002 .

[69]  V. Ntziachristos,et al.  Three-dimensional diffuse optical tomography in the parallel plane transmission geometry: evaluation of a hybrid frequency domain/continuous wave clinical system for breast imaging. , 2003, Medical physics.

[70]  A. Villringer,et al.  Physical model for the spectroscopic analysis of cortical intrinsic optical signals. , 2000, Physics in medicine and biology.

[71]  B. Chance,et al.  Cognition-activated low-frequency modulation of light absorption in human brain. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[72]  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.

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

[74]  Seong-Gi Kim,et al.  High-resolution functional magnetic resonance imaging of the animal brain. , 2003, Methods.

[75]  T. Wiesel,et al.  Functional architecture of cortex revealed by optical imaging of intrinsic signals , 1986, Nature.

[76]  A H Hielscher,et al.  Three-dimensional optical tomographic brain imaging in small animals, part 2: unilateral carotid occlusion. , 2004, Journal of biomedical optics.

[77]  J. Mandeville,et al.  Vascular filters of functional MRI: Spatial localization using BOLD and CBV contrast , 1999, Magnetic resonance in medicine.

[78]  D. Boas,et al.  Hemodynamic evoked response of the sensorimotor cortex measured noninvasively with near-infrared optical imaging. , 2003, Psychophysiology.

[79]  D. Benaron,et al.  Bedside Imaging of Intracranial Hemorrhage in the Neonate Using Light: Comparison with Ultrasound, Computed Tomography, and Magnetic Resonance Imaging , 1999, Pediatric Research.

[80]  A. Fallgatter,et al.  Frontal brain activation during the Wisconsin Card Sorting Test assessed with two-channel near-infrared spectroscopy , 1998, European Archives of Psychiatry and Clinical Neuroscience.

[81]  D. Boas,et al.  Improving the diffuse optical imaging spatial resolution of the cerebral hemodynamic response to brain activation in humans. , 2004, Optics letters.

[82]  A. Kleinschmidt,et al.  Brain or veinoxygenation or flow? On signal physiology in functional MRI of human brain activation , 1994, NMR in biomedicine.