Cerebral Cortex 1996; 6:647-660
© Oxford University Press 1996
research-article |
Neuronal Units Linked to Microvascular Modules in Cerebral Cortex: Response Elements for Imaging the Brain
1Department of Neurology and Neurological Surgery, Washington University School of Medicine St Louis, MO 63110, 2Department of Cell Biology and Physiology, Washington University School of Medicine St Louis, MO 63110, 3Sechenov Institute of Evolutionary Physiology and Biochemistry, Academy of Sciences of Russia St Petersburg, 194223 Russia
Address correspondence to Dr Thomas A. Woolsey, Department of Neurological Surgery, Box 8057, Washington University School of Medicine, 660 South Euclid Avenue, St Louis, MO 63110, USA
How neuronal activity changes cerebral blood flow is of biological and practical importance. The rodent whisker-barrel system has special merits as a model for studies of changes in local cerebral blood flow (LCBF). Stimulus-evoked changes in neural firing and intrinsic signals recorded through a cranial window were used to define regions of interest for repeated flow measurements. Whisker-activated changes in flow were measured with intravascular markers at the pia. LCBF changes were always prompt and localized over the appropriate barrel. Stimulus-related changes in parenchymal flow monitored continuously with H2 electrodes recorded short latency flow changes initiated in middle cortical layers. Activation that increased flow to particular barrels often led to reduced flow to adjacent cortex. Dye was injected into single penetrating arterioles from the pia of the fixed brain and injected into arterioles in slices of cortex where barrels were evident without stains. Arteriolar and venular domains at the surface were not directly related to underlying barrels. Capillary tufts in layer IV were mainly coincident with barrels. The matching between a capillary plexus (a vascular module) and a barrel (a functional neuronal unit) is a spatial organization of neurons and blood vessels that optimizes local interactions between the two. The paths of communication probably include: neurons to neurons, neurons to glia, neurons to vessels, glia to vessels, vessels to vessels and vessels to brain. Matching a functional grouping of neurons with a vascular module is an elegant means of reducing the risk of embarrassment for energy-expensive neuronal activity (ion pumping) while minimizing energy spent for delivery of the energy (cardiac output). For imaging studies this organization sets biological limits to spatial, temporal and magnitude resolution. Reduced flow to nearby inactive cortex enhances local differences.
![]()
CiteULike
Connotea
Del.icio.us What's this?
This article has been cited by other articles:
![]() |
G. Tomasi, P. Edison, A. Bertoldo, F. Roncaroli, P. Singh, A. Gerhard, C. Cobelli, D. J. Brooks, and F. E. Turkheimer Novel Reference Region Model Reveals Increased Microglial and Reduced Vascular Binding of 11C-(R)-PK11195 in Patients with Alzheimer's Disease J. Nucl. Med., August 1, 2008; 49(8): 1249 - 1256. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. de Celis Alonso, A. S. Lowe, J. P. Dear, K. C. Lee, S. C. R. Williams, and G. T. Finnerty Sensory Inputs from Whisking Movements Modify Cortical Whisker Maps Visualized with Functional Magnetic Resonance Imaging Cereb Cortex, June 1, 2008; 18(6): 1314 - 1325. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. Houades, A. Koulakoff, P. Ezan, I. Seif, and C. Giaume Gap Junction-Mediated Astrocytic Networks in the Mouse Barrel Cortex J. Neurosci., May 14, 2008; 28(20): 5207 - 5217. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. I. Moore and R. Cao The Hemo-Neural Hypothesis: On The Role of Blood Flow in Information Processing J Neurophysiol, May 1, 2008; 99(5): 2035 - 2047. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Weber, A. L. Keller, J. Reichold, and N. K. Logothetis The Microvascular System of the Striate and Extrastriate Visual Cortex of the Macaque Cereb Cortex, February 10, 2008; (2008) bhm259v3. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Masamoto, J. Kershaw, M. Ureshi, N. Takizawa, H. Kobayashi, K. Tanishita, and I. Kanno Apparent diffusion time of oxygen from blood to tissue in rat cerebral cortex: implication for tissue oxygen dynamics during brain functions J Appl Physiol, October 1, 2007; 103(4): 1352 - 1358. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. M. Siegel, J.-R. Duann, T.-P. Jung, and T. Sejnowski Spatiotemporal Dynamics of the Functional Architecture for Gain Fields in Inferior Parietal Lobule of Behaving Monkey Cereb Cortex, February 1, 2007; 17(2): 378 - 390. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. Nishimura, C. B. Schaffer, B. Friedman, P. D. Lyden, and D. Kleinfeld Penetrating arterioles are a bottleneck in the perfusion of neocortex PNAS, January 2, 2007; 104(1): 365 - 370. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Geuze, H. G. M. Westenberg, A. Jochims, C. S. de Kloet, M. Bohus, E. Vermetten, and C. Schmahl Altered Pain Processing in Veterans With Posttraumatic Stress Disorder Arch Gen Psychiatry, January 1, 2007; 64(1): 76 - 85. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Cauli, X.-K. Tong, A. Rancillac, N. Serluca, B. Lambolez, J. Rossier, and E. Hamel Cortical GABA Interneurons in Neurovascular Coupling: Relays for Subcortical Vasoactive Pathways J. Neurosci., October 13, 2004; 24(41): 8940 - 8949. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Nemoto, S. Sheth, M. Guiou, N. Pouratian, J. W. Y. Chen, and A. W. Toga Functional Signal- and Paradigm-Dependent Linear Relationships between Synaptic Activity and Hemodynamic Responses in Rat Somatosensory Cortex J. Neurosci., April 14, 2004; 24(15): 3850 - 3861. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. A. Sheth, M. Nemoto, M. Guiou, M. Walker, N. Pouratian, N. Hageman, and A. W. Toga Columnar Specificity of Microvascular Oxygenation and Volume Responses: Implications for Functional Brain Mapping J. Neurosci., January 21, 2004; 24(3): 634 - 641. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. M. Shepherd The single capillary and the active brain PNAS, October 28, 2003; 100(22): 12535 - 12536. [Full Text] [PDF] |
||||
![]() |
J. Lubke, A. Roth, D. Feldmeyer, and B. Sakmann Morphometric Analysis of the Columnar Innervation Domain of Neurons Connecting Layer 4 and Layer 2/3 of Juvenile Rat Barrel Cortex Cereb Cortex, October 1, 2003; 13(10): 1051 - 1063. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Zenger-Landolt and D. J. Heeger Response Suppression in V1 Agrees with Psychophysics of Surround Masking J. Neurosci., July 30, 2003; 23(17): 6884 - 6893. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. C. Silva and A. P. Koretsky Laminar specificity of functional MRI onset times during somatosensory stimulation in rat PNAS, November 12, 2002; 99(23): 15182 - 15187. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. J. Blood, N. Pouratian, and A. W. Toga Temporally Staggered Forelimb Stimulation Modulates Barrel Cortex Optical Intrinsic Signal Responses to Whisker Stimulation J Neurophysiol, July 1, 2002; 88(1): 422 - 437. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Iadecola CC COMMENTARY: Intrinsic Signals and Functional Brain Mapping: Caution, Blood Vessels at Work Cereb Cortex, March 1, 2002; 12(3): 223 - 224. [Full Text] [PDF] |
||||
![]() |
R. V. Harrison, N. Harel, J. Panesar, and R. J. Mount Blood Capillary Distribution Correlates with Hemodynamic-based Functional Imaging in Cerebral Cortex Cereb Cortex, March 1, 2002; 12(3): 225 - 233. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Fonta and M. Imbert Vascularization in the Primate Visual Cortex during Development Cereb Cortex, February 1, 2002; 12(2): 199 - 211. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. W. Spitzer, M. B. Calford, J. C. Clarey, J. D. Pettigrew, and A. W. Roe Spontaneous and Stimulus-Evoked Intrinsic Optical Signals in Primary Auditory Cortex of the Cat J Neurophysiol, March 1, 2001; 85(3): 1283 - 1298. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. I. Schubotz and D. Y. von Cramon Interval and Ordinal Properties of Sequences Are Associated with Distinct Premotor Areas Cereb Cortex, March 1, 2001; 11(3): 210 - 222. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. Yang, J. M. T. Huard, A. J. Beitz, M. E. Ross, and C. Iadecola Stellate Neurons Mediate Functional Hyperemia in the Cerebellar Molecular Layer J. Neurosci., September 15, 2000; 20(18): 6968 - 6973. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Niwa, L. Younkin, C. Ebeling, S. K. Turner, D. Westaway, S. Younkin, K. H. Ashe, G. A. Carlson, and C. Iadecola Abeta 1-40-related reduction in functional hyperemia in mouse neocortex during somatosensory activation PNAS, August 15, 2000; 97(17): 9735 - 9740. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. Niwa, E. Araki, S. G. Morham, M. E. Ross, and C. Iadecola Cyclooxygenase-2 Contributes to Functional Hyperemia in Whisker-Barrel Cortex J. Neurosci., January 15, 2000; 20(2): 763 - 770. [Abstract] [Full Text] [PDF] |
||||
![]() |
G. Yang, G. Chen, T. J. Ebner, and C. Iadecola Nitric oxide is the predominant mediator of cerebellar hyperemia during somatosensory activation in rats Am J Physiol Regulatory Integrative Comp Physiol, December 1, 1999; 277(6): R1760 - R1770. [Abstract] [Full Text] [PDF] |
||||
![]() |
I. Toni, N. D. Schluter, O. Josephs, K. Friston, and R. E. Passingham Signal-, Set- and Movement-related Activity in the Human Brain: An Event-related fMRI Study Cereb Cortex, January 1, 1999; 9(1): 35 - 49. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. Kleinfeld, P. P. Mitra, F. Helmchen, and W. Denk Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex PNAS, December 22, 1998; 95(26): 15741 - 15746. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. G. Hudetz, H. Shen, and J. P. Kampine Nitric oxide from neuronal NOS plays critical role in cerebral capillary flow response to hypoxia Am J Physiol Heart Circ Physiol, March 1, 1998; 274(3): H982 - H989. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. L. Davis, K. K. Kwong, R. M. Weisskoff, and B. R. Rosen Calibrated functional MRI: Mapping the dynamics of oxidative metabolism PNAS, February 17, 1998; 95(4): 1834 - 1839. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. E. Raichle Behind the scenes of functional brain imaging: A historical and physiological perspective PNAS, February 3, 1998; 95(3): 765 - 772. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. R. Rosen, R. L. Buckner, and A. M. Dale Event-related functional MRI: Past, present, and future PNAS, February 3, 1998; 95(3): 773 - 780. [Abstract] [Full Text] [PDF] |
||||








