Neurovascular coupling and energy metabolism in the developing brain

Progress in Brain Research

Volumn 225, Issue , 2016, Pages 213-242

  Kozberg, M ^a   Hillman, E ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Brain development; Brain metabolism; FMRI; Neurovascular coupling; Optical imaging

Indexed keywords

HEMOGLOBIN; OXYGEN;

ASTROCYTE; AUTOREGULATION; BLOOD VESSEL TONE; BOLD SIGNAL; BRAIN ARTERY; BRAIN CAPILLARY; BRAIN DEVELOPMENT; BRAIN NERVE CELL; BRAIN PERICYTE; ENERGY METABOLISM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMICS; HUMAN; MICROVASCULATURE; NERVE CELL NETWORK; NEUROVASCULAR COUPLING; POSTNATAL DEVELOPMENT; ANIMAL; BLOOD; BRAIN; CYTOLOGY; DIAGNOSTIC IMAGING; GROWTH, DEVELOPMENT AND AGING; IMAGE PROCESSING; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY;

ANIMALS; BRAIN; ENERGY METABOLISM; HEMODYNAMICS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; NEUROVASCULAR COUPLING; OXYGEN;

EID: 84962148628     PISSN: 00796123     EISSN: 18757855     Source Type: Book Series    
DOI: 10.1016/bs.pbr.2016.02.002     Document Type: Chapter

References (126)

1. Ackman J.B., Burbridge T.J., Crair M.C. Retinal waves coordinate patterned activity throughout the developing visual system. Nature 2012, 490:219-225.
2. Allievi A.G., Arichi T., Tusor N., Kimpton J., Arulkumaran S., Counsell S.J., Edwards A.D., Burdet E. Maturation of sensori-motor functional responses in the preterm brain. Cereb. Cortex 2016, 26(1):402-413.
3. Altman D.I., Perlman J.M., Volpe J.J., Powers W.J. Cerebral oxygen metabolism in newborns. Pediatrics 1993, 92:99-104.
4. Anderson A.W., Marois R., Colson E.R., Peterson B.S., Duncan C.C., Ehrenkranz R.A., Schneider K.C., Gore J.C., Ment L.R., et al. Neonatal auditory activation detected by functional magnetic resonance imaging. Magn. Reson. Imaging 2001, 19:1-5.
5. Andresen J., Shafi N.I., Bryan R.M. Endothelial influences on cerebrovascular tone. J. Appl. Physiol. 2005, 100:318-327.
6. Argandoña E.G., Lafuente J.V. Effects of dark-rearing on the vascularization of the developmental rat visual cortex. Brain Res. 1996, 732:43-51.
7. Arichi T., Moraux A., Melendez A., Doria V., Groppo M., Merchant N., Combs S., Burdet E., Larkman D.J., Counsell S.J., et al. Somatosensory cortical activation identified by functional MRI in preterm and term infants. Neuroimage 2010, 49:2063-2071.
8. Arichi T., Fagiolo G., Varela M., Melendez-calderon A., Allievi A., Merchant N., Tusor N., Counsell S.J., Burdet E., Beckmann C.F., et al. Development of BOLD signal hemodynamic responses in the human brain. Neuroimage 2012, 63:663-673.
9. Armulik A., Abramsson A., Betsholtz C. Endothelial/pericyte interactions. Circ. Res. 2005, 97:512-523.
10. Attwell D., Iadecola C. The neural basis of functional brain imaging signals. Trends Neurosci. 2002, 25:621-625.
11. Attwell D., Buchan A.M., Charpak S., Lauritzen M., Macvicar B.A., Newman E.A. Glial and neuronal control of brain blood flow. Nature 2010, 468:232-243.
12. Bekar L.K., Wei H.S., Nedergaard M. The locus coeruleus-norepinephrine network optimizes coupling of cerebral blood volume with oxygen demand. J. Cereb. Blood Flow Metab. 2012, 32:2135-2145.
13. Ben-Ari Y. Excitatory actions of gaba during development: the nature of the nurture. Nat. Rev. Neurosci. 2002, 3:728-739.
14. Bilger A., Nehlig A. Quantitative histochemical changes in enzymes involved in energy metabolism in the rat brain during postnatal development. I. Cytochrome oxidase and lactate dehydrogenase. Int. J. Dev. Neurosci. 1991, 9:545-553.
15. Binmöller F., Müller C. Postnatal development of dye-coupling among astrocytes in the visual cortex. Glia 1992, 6:127-137.
16. Black J., Sirevaag A., Greenough W. Complex experience promotes capillary formation in young rat visual cortex. Neurosci. Lett. 1987, 83:351-355.
17. Boas D., Jones S., Devor A., Huppart T., Dale A. A vascular anatomical network model of the spatio-temporal response to brain activation. Neuroimage 2008, 40:1116-1129.
18. Bonavita Vi, Ponte F., Amore G. Lactate dehydrogenase isozymes in the developing rat brain. Nature 1962, 196:576-577.
19. Booth R.F., Patel T.B., Clark J.B. The development of enzymes of energy metabolism in the brain of a precocial (guinea pig) and non-precocial (rat) species. J. Neurochem. 1980, 34:17-25.
20. Born P., Rostrup E., Leth H., Peitersen B., Lou H. Change of visually induced cortical activation patterns during development. Lancet 1996, 347:543.
21. Born P., Leth H., Miranda M.J., Rostrup E., Stensgaard A., Peitersen B., Larsson H.B.W., Lou H.C. Visual activation in infants and young children studied by functional magnetic resonance imaging. Pediatr. Res. 1998, 44:578-583.
22. Born A.P., Miranda M.J., Rostrup E., Toft P.B., Peitersen B., Larsson H.B.W., Lou H.C. Functional magnetic resonance imaging of the normal and abnormal visual system in early life. Neuropediatrics 2000, 31:24-32.
23. Born A.P., Rostrup E., Miranda M.J., Larsson H.B.W., Lou H.C. Visual cortex reactivity in sedated children examined with perfusion MRI (FAIR). Magn. Reson. Imaging 2002, 20:199-205.
24. Bustamante J., Czerniczyniec A., Cymeryng C., Lores-Arnaiz S. Age related changes from youth to adulthood in rat brain cortex: nitric oxide synthase and mitochondrial respiratory function. Neurochem. Res. 2008, 33:1216-1223.
25. Cahalane D.J., Clancy B., Kingsbury M.A., Graf E., Sporns O., Finlay B.L. Network structure implied by initial axon outgrowth in rodent cortex: empirical measurement and models. PLoS One 2011, 6:e16113.
26. Cauli B., Tong X., Rancillac A., Serluca N., Lambolez B., Rossier J., Hamel E. Cortical GABA interneurons in neurovascular coupling: relays for subcortical vasoactive pathways. J. Neurosci. 2004, 24:8940-8949.
27. Chen B.R., Bouchard M.B., Mccaslin A.F.H., Burgess S.A., Hillman E.M.C. High-speed vascular dynamics of the hemodynamic response. Neuroimage 2011, 54:1021-1030.
28. Chen B.R., Kozberg M.G., Bouchard M.B., Shaik M.A., Hillman E.M.C. A critical role for the vascular endothelium in functional neurovascular coupling in the brain. J. Am. Heart Assoc. 2014, 3:e000787.
29. Chiron C., Raynaud C., Mazière B., Zilbovicius M., Laflamme L., Masure M.C., Dulac O., Bourguignon M., Syrota A. Changes in regional cerebral blood flow during brain maturation in children and adolescents. J. Nucl. Med. 1992, 33:696-703.
30. Chugani H.T., Phelps M.E. Maturational changes in cerebral function in infants determined by 18FDG positron emission tomography. Science 1986, 231:840-843.
31. Church J., Peterson S., Schlagger B. The "Task B problem" and other considerations in developmental functional neuroimaging. Hum. Brain Mapp. 2010, 31:852-862.
32. Colonnese M.T., Phillips M.A., Constantine-paton M., Kaila K., Jasanoff A. Development of hemodynamic responses and functional connectivity in rat somatosensory cortex. Nat. Neurosci. 2008, 11:72-79.
33. Crook J.M., Kisvárday Z.F., Eysel U.T. Evidence for a contribution of lateral inhibition to orientation tuning and direction selectivity in cat visual cortex: reversible inactivation of functionally characterized sites combined with neuroanatomical tracing techniques. Eur. J. Neurosci. 1998, 10:2056-2075.
34. Culley D.J., Maze M., Crosby G. Reprogramming of the infant brain by surgery with general anesthesia. Mayo Clin. Proc. 2012, 87:110-113.
35. Cusack R., Wild C., Linke A.C., Arichi T., Lee D.S.C., Han V.K. Optimizing stimulation and analysis protocols for neonatal fMRI optimizing stimulation and analysis protocols for neonatal fMRI. PLoS One 2015, 10:e0120202.
36. Devor A., Hillman E.M.C., Tian P., Waeber C., Teng I.C., Ruvinskaya L., Shalinsky M.H., Zhu H., Haslinger R.H., Narayanan S.N., et al. Stimulus-induced changes in blood flow and 2-deoxyglucose uptake dissociate in ipsilateral somatosensory cortex. J. Neurosci. 2008, 28:14347-14357.
37. 2 is required to maintain baseline tissue oxygenation at locations distal to blood vessels. J. Neurosci. 2011, 31:13676-13681.
38. Doria V., Beckmann C.F., Arichi T., Merchant N., Groppo M., Turkheimer F.E., Counsell S.J., Murgasova M., Aljabar P., Nunes R.G., et al. Emergence of resting state networks in the preterm human brain. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:20015-20020.
39. Erberich S.G., Panigrahy A., Friedlich P., Seri I., Nelson M.D., Gilles F. Somatosensory lateralization in the newborn brain. Neuroimage 2006, 29:155-161.
40. Feller M.B. Spontaneous correlated activity in developing neural circuits. Neuron 1999, 22:653-656.
41. Ferradal S.L., Liao S.M., Eggebrecht A.T., Shimony J.S., Inder T.E., Culver J.P., Smyser C.D. Functional imaging of the developing brain at the bedside using diffuse optical tomography. Cereb. Cortex 2015, 1-11. Epub ahead of print.
42. Ferrazzi G., Kuklisova Murgasova M., Arichi T., Malamateniou C., Fox M.J., Makropoulos A., Allsop J., Rutherford M., Malik S., Aljabar P., et al. Resting state fMRI in the moving fetus: a robust framework for motion, bias field and spin history correction. Neuroimage 2014, 101:555-568.
43. Fox M.D., Raichle M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 2007, 8:700-711.
44. Fox P.T., Raichle M.E., Mintun M.A., Dence C., Focal D. Nonoxidative glucose consumption during focal physiologic neural activity. Science 1988, 241:462-464.
45. Fransson P., Aden U., Blennow M., Lagercrantz H. The functional architecture of the infant brain as revealed by resting-state fMRI. Cereb. Cortex 2011, 21:145-154.
46. Fujimoto K. Pericyte-endothelial gap junctions in developing rat cerebral capillaries: a fine structural study. Anat. Rec. 1995, 242:562-565.
47. Gao P., Postiglione M.P., Krieger T.G., Hernandez L., Wang C., Han Z., Streicher C., Papusheva E., Insolera R., Chugh K., et al. Article deterministic progenitor behavior and unitary production of neurons in the neocortex. Cell 2014, 159:775-788.
48. Gelfand M., Hong S., Gu C. Guidance from above: common cues direct distinct signaling outcomes in vascular and neural patterning. Trends Cell Biol. 2009, 19:1199-1216.
49. Goldman-Rakic P., Brown R. Postnatal development of monoamine content and synthesis in the cerebral cortex of rhesus monkeys. Brain Res. 1982, 256:339-349.
50. Graham A.M., Pfeifer J.H., Fisher P.A., Lin W., Gao W., Fair D.A. The potential of infant fMRI research and the study of early life stress as a promising exemplar. Dev. Cogn. Neurosci. 2014, 12:12-39.
51. Greisen G. To autoregulate or not to autoregulate-that is no longer the question. Semin. Pediatr. Neurol. 2009, 16:207-215.
52. Hall C.N., Reynell C., Gesslein B., Hamilton N.B., Mishra A., Sutherland B.A., O'Farrell F.M., Buchan A.M., Lauritzen M., Attwell D. Capillary pericytes regulate cerebral blood flow in health and disease. Nature 2014, 508:55-60.
53. Hamilton N.B., Attwell D., Hall C.N. Pericyte-mediated regulation of capillary diameter: a component of neurovascular coupling in health and disease. Front. Neuroenergetics 2010, 2:1-14.
54. Hand R., Polleux F. Neurogenin2 regulates the initial axon guidance of cortical pyramidal neurons projecting medially to the corpus callosum. Neural Dev. 2011, 6:30.
55. Harb R., Whiteus C., Freitas C., Grutzendler J. In vivo imaging of cerebral microvascular plasticity from birth to death. J. Cereb. Blood Flow Metab. 2013, 33:146-156.
56. Harris J.J., Reynell C., Attwell D. The physiology of developmental changes in BOLD functional imaging signals. Dev. Cogn. Neurosci. 2011, 1:199-216.
57. Heeger D.J., Ress D. What does fMRI tell us about neuronal activity?. Nat. Rev. Neurosci. 2002, 3:142-151.
58. Heep A., Scheef L., Jankowski J., Born M., Zimmermann N., Sival D., Bos A., Gieseke J., Bartmann P., Schild H., et al. Functional magnetic resonance imaging of the sensorimotor system in preterm infants. Pediatrics 2009, 123:294-300.
59. Hensch T.K. Critical period regulation. Annu. Rev. Neurosci. 2004, 27:549-579.
60. Herken R., Gotz W., Wattjes K.-H. Initial development of capillaries in the neuroepithelium of the mouse. J. Anat. 1989, 164:85-92.
61. Hill R.A., Tong L., Yuan P., Murikinati S., Gupta S., Grutzendler J. Regional blood flow in the normal and ischemic brain is controlled by arteriolar smooth muscle cell contractility and not by capillary pericytes. Neuron 2015, 87:95-110.
62. Hillman E.M.C. Coupling mechanism and significance of the BOLD signal: a status report. Annu. Rev. Neurosci. 2014, 37:161-181.
63. Hillman E.M.C., Kozberg M.G. What secrets can functional MRI reveal about the developing infant brain?. Imaging Med. 2013, 5:203-206.
64. Hoshi Y., Tamura M. Dynamic multichannel near-infrared optical imaging of human brain activity. J. Appl. Physiol. 1993, 75:1842-1846.
65. Hoshi Y., Kohri S., Matsumoto Y., Cho K., Matsuda T., Okajima S., Fujimoto S. Hemodynamic responses to photic stimulation in neonates. Pediatr. Neurol. 2000, 23:323-327.
66. Hubel D.H., Wiesel T.N. Receptive fields of cells in striate cortex of very young, visually inexperienced kittens. J. Neurophysiol. 1963, 26:994-1002.
67. Huttenlocher P., de Courten C., Garey L., van der Loos H. Synaptogenesis in human visual cortex-evidence for synapse elimination during normal development. Neurosci. Lett. 1982, 33:247-252.
68. Iadecola C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat. Rev. Neurosci. 2004, 5:347-360.
69. Iwahara S.-I., Abe Y., Okazaki T. Identification of five embryonic hemoglobins of rat and ontogeny of their constituent globins during fetal development. J. Biochem. 1996, 119:360-366.
70. Joeri P., Huisman T., Ekatodramis D., Loenneker T., Rumpel H., Martin E. Functional magnetic resonance imaging (fMRI) of the visual cortex in children. Pediatr. Res. 1996, 40:535.
71. Karen T., Morren G., Haensse D., Bauschatz A.S., Bucher H.U., Wolf M. Hemodynamic response to visual stimulation in newborn infants using functional near-infrared spectroscopy. Hum. Brain Mapp. 2008, 29:453-460.
72. Katz L.C., Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 1996, 274:1133-1138.
73. Keep R., Jones H. Cortical microvessels during brain development: a morphometric study in the rat. Microvasc. Res. 1990, 40:412-426.
74. Khwaja O., Volpe J.J. Pathogenesis of cerebral white matter injury of prematurity. Arch. Dis. Child. Fetal Neonatal Ed. 2008, 93:F153-F161.
75. Kozberg M.G., Chen B.R., Deleo S.E., Bouchard M.B., Hillman E.M.C. Resolving the transition from negative to positive blood oxygen level-dependent responses in the developing brain. Proc. Natl. Acad. Sci. 2013, 110:4380-4385.
76. Kozberg, M.G., Ma, Y., Kim, S.H., and Hillman, E.M.C. (under review). Rapid postnatal expansion of neural networks occurs in an environment of altered neurovascular and neurometabolic coupling.
77. Kusaka T., Kawada K., Okubo K., Nagano K., Namba M., Okada H., Imai T., Isobe K., Itoh S. Noninvasive optical imaging in the visual cortex in young infants. Hum. Brain Mapp. 2004, 22(2):122-132.
78. Lacoste B., Gu C. Control of cerebrovascular patterning by neural activity during postnatal development. Mech. Dev. 2015, 138:43-49.
79. Lacoste B., Comin C.H., Ben-Zvi A., Kaeser P.S., Xu X., Costa Lda F., Gu C. Sensory-related neural activity regulates the structure of vascular networks in the cerebral cortex. Neuron 2014, 83:1117-1130.
80. Le Magueresse C., Monyer H. GABAergic interneurons shape the functional maturation of the cortex. Neuron 2013, 77:388-405.
81. Lewis T.L., Courchet J., Polleux F. Cell biology in neuroscience: cellular and molecular mechanisms underlying axon formation, growth, and branching. J. Cell Biol. 2013, 202:837-848.
82. Liao S.M., Gregg N.M., White B.R., Zeff B.W., Bjerkaas K.A., Inder T.E., Culver J.P. Neonatal hemodynamic response to visual cortex activity: high-density near-infrared spectroscopy study. J. Biomed. Opt. 2010, 15:1-9.
83. Lind B.L., Brazhe A.R., Jessen S.J., Tan F.C.C., Lauritzen M.J. Rapid stimulus-evoked astrocyte Ca2+ elevations and hemodynamic responses in mouse somatosensory cortex in vivo. Proc. Natl. Acad. Sci. 2013, 110:E4678-E4687.
84. Lindauer U., Leithner C., Kaasch H., Rohrer B., Foddis M., Füchtemeier M., Offenhauser N., Steinbrink J., Royl G., Kohl-Bareis M., et al. Neurovascular coupling in rat brain operates independent of hemoglobin deoxygenation. J. Cereb. Blood Flow Metab. 2010, 30:757-768.
85. Lovick T.A., Brown L.A., Key B.J. Neurovascular relationships in hippocampal slices: physiological and anatomical studies of mechanisms underlying flow-metabolism coupling in intraparenchymal microvessels. Neuroscience 1999, 92:47-60.
86. Martin E., Joeri P., Loenneker T., Ekatodramis D., Vitacco D., Hennig J., Marcar V.L. Visual processing in infants and children studied using functional MRI. Pediatr. Res. 1999, 46:135-140.
87. McCandlish C.A., Li C.X., Waters R.S. Early development of the SI cortical barrel field representation in neonatal rats follows a lateral-to-medial gradient: an electrophysiological study. Exp. Brain Res. 1993, 92:369-374.
88. Meek J.H., Firbank M., Elwell C.E., Atkinson J., Braddick O., Wyatt J.S. Regional hemodynamic responses to visual stimulation in awake infants. Pediatr. Res. 1998, 43:840-843.
89. Muramoto S., Yamada H., Sadato N., Kimura H., Konishi Y., Kimura K., Tanaka M., Kochiyama T., Yonekura Y., Ito H. Age-dependent change in metabolic response to photic stimulation of the primary visual cortex in infants: functional magnetic resonance imaging study. J. Comput. Assist. Tomogr. 2002, 26:894-901.
90. Norman M.G. The growth and development of microvasculature in human cerebral cortex. J. Neuropathol. Exp. Neurol. 1986, 45:222-232.
91. Quinn R. Comparing rat's to human's age: how old is my rat in people years?. Nutrition 2005, 21:775-777.
92. Rey S., Semenza G.L. Hypoxia-inducible factor-1-dependent mechanisms of vascularization and vascular remodelling. Cardiovasc. Res. 2010, 86:236-242.
93. Riddle D.R., Gutierrez G., Zheng D., White L.E., Richards A., Purves D. Differential metabolic and electrical activity in the somatic sensory cortex of juvenile and adult rats. J. Neurosci. 1993, 13:4193-4213.
94. Risser L., Plouraboué F., Cloetens P., Fonta C. A 3D-investigation shows that angiogenesis in primate cerebral cortex mainly occurs at capillary level. Int. J. Dev. Neurosci. 2009, 27:185-196.
95. Rowan R.A., Maxwell D.S. Patterns of vascular sprouting in the postnatal development of the cerebral cortex of the rat. Am. J. Anat. 1981, 160:247-255.
96. Sakadžić S., Mandeville E.T., Gagnon L., Musacchia J.J., Yaseen M.A., Yucel M.A., Lefebvre J., Lesage F., Anders M., Eikermann-haerter K., et al. Large arteriolar component of oxygen delivery implies a safe margin of oxygen supply to cerebral tissue. Nat. Commun. 2014, 5:5734.
97. Sakatani K., Chen S., Lichty W., Zuo H., Wang Y.P. Cerebral blood oxygenation changes induced by auditory stimulation in newborn infants measured by near infrared spectroscopy. Early Hum. Dev. 1999, 55:229-236.
98. Saugstad O.D. Resuscitation of newborn infants: from oxygen to room air. Lancet 2010, 376:1970-1971.
99. Schmithorst V.J., Vannest J., Lee G., Hernandez-Garcia L., Plante E., Rajagopal A., Holland S.K. Evidence that neurovascular coupling underlying the BOLD effect increases with age during childhood. Hum. Brain Mapp. 2015, 36:1-15.
100. Seregi A., Keller M., Hertting G. Are cerebral prostanoids of astroglial origin? Studies on the prostanoid forming system in developing rat brain and primary cultures of rat astrocytes. Brain Res. 1987, 404:113-120.
101. Sie L., Rombouts S., Valk J., Hart A., Scheltens P., van der Knaap M. Functional MRI of visual cortex in infants with or without periventricular leukomalacia. Dev. Med. Child Neurol. 2001, 43:486-490.
102. Singer D. Neonatal tolerance to hypoxia: a comparative-physiological approach. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 1999, 123:221-234.
103. Smyser C.D., Inder T.E., Shimony J.S., Hill J.E., Degnan A.J., Snyder A.Z., Neil J.J. Longitudinal analysis of neural network development in preterm infants. Cereb. Cortex 2010, 20:2852-2862.
104. Stichel C.C., Müller C.M., Zilles K. Distribution of glial fibrillary acidic protein and vimentin immunoreactivity during rat visual cortex development. J. Neurocytol. 1991, 20:97-108.
105. Taga G., Asakawa K., Maki A., Konishi Y., Koizumi H. Brain imaging in awake infants by near-infrared optical topography. Proc. Natl. Acad. Sci. 2003, 100:107222-110727.
106. Takahashi T., Shirane R., Sato S., Yoshimoto T. Developmental changes of cerebral blood flow and oxygen metabolism in children. AJNR Am. J. Neuroradiol. 1999, 20:917-922.
107. Takano T., Tian G.-F., Peng W., Lou N., Libionka W., Han X., Nedergaard M. Astrocyte-mediated control of cerebral blood flow. Nat. Neurosci. 2006, 9:260-267.
108. Takata N., Nagai T., Ozawa K., Oe Y., Mikoshiba K., Hirase H. Cerebral blood flow modulation by basal forebrain or whisker stimulation can occur independently of large cytosolic Ca2+ signaling in astrocytes. PLoS One 2013, 8:e66525.
109. Thein S.L., Menzel S., Lathrop M., Garner C. Control of fetal hemoglobin: new insights emerging from genomics and clinical implications. Hum. Mol. Genet. 2009, 18:R216-R223.
110. Tian P., Teng I.C., May L.D., Kurz R., Lu K., Scadeng M., Hillman E.M.C., Crespigny A.J.De, Arceuil H.E.D., Mandeville J.B., et al. Cortical depth-specific microvascular dilation underlies laminar differences in blood oxygenation level-dependent functional MRI signal. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:15246-15251.
111. Ujiie H., Chaytor A.T., Bakker L.M., Griffith T.M. Essential role of Gap junctions in NO- and prostanoid-independent relaxations evoked by acetylcholine in rabbit intracerebral arteries. Stroke 2003, 34:544-550.
112. Uylings H.B., Van Eden C.G., Parnavelas J.G., Kalsbeek A. The prenatal and postnatal development of rat cerebral cortex. The Cerebral Cortex of the Rat 1990, 36-76. MIT Press, Cambridge, MA. B. Kolb, R.C. Tees (Eds.).
113. Volpe J.J. Brain injury in the premature infant-from pathogenesis to prevention. Brain Dev. 1997, 19:519-534.
114. Vovenko E. Distribution of oxygen tension on the surface of arterioles, capillaries and venules of brain cortex and in tissue in normoxia: an experimental study on rats. Pflugers Arch. 1999, 437:617-623.
115. Wang D.-B.B., Blocher N.C., Spence M.E., Rovainen C.M., Woolsey T.A. Development and remodeling of cerebral blood vessels and their flow in postnatal mice observed with in vivo videomicroscopy. J. Cereb. Blood Flow Metab. 1996, 12:935-946.
116. Wang C.-L., Zhang L., Zhou Y., Zhou J., Yang X.-J., Duan S., Xiong Z.-Q., Ding Y.-Q. Activity-dependent development of callosal projections in the somatosensory cortex. J. Neurosci. 2007, 27:11334-11342.
117. Watanabe H., Homae F., Nakano T., Taga G. Functional activation in diverse regions of the developing brain of human infants. Neuroimage 2008, 43:346-357.
118. Weber B., Keller A.L., Reichold J., Logothetis N.K. The microvascular system of the striate and extrastriate visual cortex of the macaque. Cereb. Cortex 2008, 18:2318-2330.
119. Wheatley C.M., Dickinson J.L., Mackey D.A., Craig J.E., Sale M.M. Retinopathy of prematurity: recent advances in our understanding. Arch. Dis. Child. Fetal Neonatal Ed. 2002, 87:F78-F82.
120. Whiteus C., Freitas C., Grutzendler J. Perturbed neural activity disrupts cerebral angiogenesis during a postnatal critical period. Nature 2014, 505:407-411.
121. Wolf T., Lindauer U., Villringer A., Dirnagl U. Excessive oxygen or glucose supply does not alter the blood flow response to somatosensory stimulation or spreading depression in rats. Brain Res. 1997, 761:290-299.
122. Yamada H., Sadato N., Konishi Y., Kimura K., Tanaka M., Yonekura Y., Ishii Y. A rapid brain metabolic change in infants detected by fMRI. Neuroreport 1997, 8:3775-3778.
123. Zaramella P., Freato F., Amigoni A., Salvadori S., Marangoni P., Suppjei A., Schiavo B., Chiandetti L. Brain auditory activation measured by near-infrared spectroscopy (NIRS) in neonates. Pediatr. Res. 2001, 49:213-219.
124. Zehendner C.M., Tsohataridis S., Luhmann H.J., Yang J.-W. Developmental switch in neurovascular coupling in the immature rodent barrel cortex. PLoS One 2013, 8:e80749.
125. Zijlstra W.G., Buursma A., Meeuwsen-van der Roest W.P. Absorption spectra of human fetal and adult oxyhemoglobin, de-oxyhemoglobin, carboxyhemoglobin, and methemoglobin. Clin. Chem. 1991, 37:1633-1638.
126. Zuckerman S.L., Armstead W., Hsu P., Shibata M., Leffler C. Age dependence of cerebrovascular response mechanisms in domestic pigs. Am. J. Physiol. Heart Circ. Physiol. 1996, 271:H535-H540.