Development of BOLD signal hemodynamic responses in the human brain

NeuroImage

Volumn 63, Issue 2, 2012, Pages 663-673

  Arichi, Tomoki ^a   Fagiolo, Gianlorenzo ^a   Varela, Marta ^a   Melendez Calderon, Alejandro ^b   Allievi, Alessandro ^b   Merchant, Nazakat ^a   Tusor, Nora ^a   Counsell, Serena J ^a   Burdet, Etienne ^b   Beckmann, Christian F ^c,d   Edwards, A David ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^d UNIVERSITY OF TWENTE   (Netherlands)

Author keywords

Brain development; Functional MRI; Hemodynamic response function; Neonate

Indexed keywords

ADULT; AGE; ARTICLE; BOLD SIGNAL; BRAIN FUNCTION; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; EVENT RELATED POTENTIAL; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMIC RESPONSE FUNCTION; HEMODYNAMICS; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; IMAGE DISPLAY; INFANT; MALE; NEUROIMAGING; PREGNANCY; PREMATURITY; PRIORITY JOURNAL; SOMATOSENSORY STIMULATION;

ADULT; BRAIN; FEMALE; HEMODYNAMICS; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; INFANT; INFANT, NEWBORN; INFANT, PREMATURE; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; OXYGEN; YOUNG ADULT;

EID: 84865461274     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.06.054     Document Type: Article

References (95)

1. Aguirre G.K., Zarahn E., D'Esposito M. The variability of human, BOLD hemodynamic responses. NeuroImage 1998, 8:360-369.
2. Altman D.I., et al. Cerebral blood flow requirement for brain viability in newborn infants is lower than in adults. Ann. Neurol. 1988, 24:218-226.
3. Arichi T., et al. Somatosensory cortical activation identified by functional MRI in preterm and term infants. NeuroImage 2010, 49(3):2063-2071.
4. Avlonitou E., Balatsouras D.G., Margaritis E., et al. Use of chloral hydrate as a sedative for auditory brainstem response testing in a pediatric population. Int. J. Pediatr. Otorhinolaryngol. 2011, 75(6):760-763.
5. Bandettini P.A., Cox R.W. Event-related fMRI contrast when using constant interstimulus interval: theory and experiment. Magn. Reson. Med. 2000, 43(4):540-548.
6. Beckmann C.F., Smith S.M. Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans. Med. Imaging 2004, 23(2):137-152.
7. Blankenship A.G., Feller M.B. Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat. Rev. Neurosci. 2010, 11:18-29.
8. Born A.P., et al. Functional magnetic resonance imaging of the normal and abnormal visual system in early life. Neuropediatrics 2000, 31(1):24-32.
9. Boyton G., Engel S., Glover G., Heeger D. Linear systems analysis of functional magnetic resonance imaging in human V1. J. Neurosci. 1996, 16:4207-4221.
10. Buijs P.C., et al. Effect of age on cerebral blood flow: measurement with ungated two-dimensional phase-contrast MR angiography in 250 adults. Radiology 1998, 209:667-674.
11. Buxton R.B., Wong E.C., Frank L.R. Dynamics of blood flow and oxygenation changes during brain activation: the balloon model. Magn. Reson. Med. 1998, 39:855-864.
12. Buxton R.B., Uludag K., Dubowitz D., Liu T.T. Modeling the hemodynamic response to brain activation. NeuroImage 2004, 23:s220-s233.
13. Cauli B., Hamel E. Revisiting the role of neurons in neurovascular coupling. Front. Neuroenergetics 2010, 2:1-8.
14. Chan K.C., Xing K., Cheung M.M., Zhou I.Y., Wu E.X. Functional MRI of postnatal visual development in normal and hypoxic-ischemic-injured superior colliculi. NeuroImage 2010, 49(3):2013-2020.
15. Chen Y., Parrish T.B. Caffeine dose effect on activation-induced BOLD and CBF responses. NeuroImage 2009, 46(3):577-583.
16. Chen J., Pike G.B. BOLD-specific cerebral blood volume and blood flow changes during neuronal activation in humans. NMR Biomed. 2009, 22:1054-1062.
17. Chen J., Pike G.B. Origins of the BOLD post-stimulus undershoot. NeuroImage 2009, 46:559-568.
18. Chen J., Pike G.B. Global cerebral oxidative metabolism during hypercapnia and hypocapnia in humans: implications for BOLD MRI. J. Cereb. Blood Flow Metab. 2010, 30(6):1094-1099.
19. Chen J., Pike G.B. MRI measurement of the BOLD-specific flow-volume relationship during hypercapnia and hypocapnia in humans. NeuroImage 2010, 53(2):383-391.
20. Chugani H.T., Phelps M.E. Maturational changes in cerebral function in infants determined by 18FDG positron emission tomography. Science 1986, 231(4740):840-843.
21. Cohen E.R., Ugurbil K., Kim S.G. Effect of basal conditions on the magnitude and dynamics of the blood oxygenation level-dependent fMRI response. J. Cereb. Blood Flow Metab. 2002, 22(9):1042-1053.
22. Colonnese M.T., Philips M.A., Constanine-Paton M., Kaila K., Jasanoff A. Development of hemodynamic responses and functional connectivity in rat somatosensory cortex. Nat. Neurosci. 2008, 11(1):72-79.
23. Corlew R., Bosma M.M., Moody W.J. Spontaneous, synchronous electrical activity in neonatal mouse cortical neurones. J. Physiol. 2004, 560:377-390.
24. Dale A.M., Buckner R.L. Selective averaging of rapidly presented individual trials using fMRI. Hum. Brain Mapp. 1997, 5(5):329-340.
25. de Graaf-Peters V.B., Hadders-Algra M. Ontogeny of the human central nervous system: what is happening when?. Early Hum. Dev. 2006, 82:257-266.
26. Dechent P., Schutze G., Helms G., Merboldt K.D., Frahm J. Basal cerebral blood volume during the poststimulation undershoot in BOLD MRI of the human brain. J. Cereb. Blood Flow Metab. 2011, 31:82-89.
27. Delpy D.T., et al. Cerebral monitoring in newborn infants by magnetic resonance and near infrared spectroscopy. Scand. J. Clin. Lab. Invest. Suppl. 1987, 188:9-17.
28. Doria V., et al. Emergence of resting state networks in the preterm human brain. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(46):20015-20020.
29. Edwards A.D., et al. Cotside measurement of cerebral blood flow in ill newborn infants by near infrared sprectroscopy. Lancet 1988, 2(8614):770-771.
30. Elwell C.E., Cope M., Delpy D.T. An analytical model for determining cerebrovascular transit time using near infrared spectroscopy. Adv. Exp. Med. Biol. 1997, 428:561-568.
31. Erberich S.G., et al. Somatosensory lateralization in the newborn brain. NeuroImage 2006, 29(1):155-161.
32. Felleman D.J., Van Essen D.C. Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1991, 1:1-47.
33. Franceschini M.A., et al. Assessment of infant brain development with frequency-domain near-infrared spectroscopy. Pediatr. Res. 2007, 61:546-551.
34. Friston K.J., et al. Event-related fMRI: characterizing differential responses. NeuroImage 1998, 9:30-40.
35. Gaillard W.D., Grandon C.B., Xu B. Developmental aspects of pediatric fMRI: considerations for image acquisition, analysis, and interpretation. NeuroImage 2001, 13:239-249.
36. Gassert R., Burdet E., Chinzei K. MRI-compatible robotics. IEEE Eng. Med. Biol. Mag. 2008, 27(3):12-14.
37. Glover G.H. Deconvolution of impulse response in event-related BOLD fMRI. NeuroImage 1999, 9:416-429.
38. Greisen G. Cerebral blood flow in preterm infants during the first few weeks of life. Acta Paediatr. Scand. 1986, 75(1):43-51.
39. Grubb R.L., Raichle M.E., Eichling J.O., Ter-Pogossian M.M. The effects of changes in PaCO2 on cerebral blood volume, blood flow, and vascular mean transit time. Stroke 1974, 5:630-639.
40. Gu H., Stein E.A., Yang Y. Nonlinear responses of cerebral blood volume, blood flow and blood oxygenation during visual stimulation. Magn. Reson. Imaging 2005, 23(9):921-928.
41. Handwerker D.A., Ollinger J.M., D'Esposito M.D. Variation of BOLD hemodynamic responses across subjects and brain regions and their effects on statistical analyses. NeuroImage 2004, 21:1639-1651.
42. Harris J.J., Reynell C., Attwell D. The physiology of developmental changes in BOLD functional imaging signals. Dev. Cogn. Neurosci. 2011, 1:199-216.
43. Heep A., et al. Functional magnetic resonance imaging of the sensorimotor system in preterm infants. Pediatrics 2009, 123(1):294-300.
44. Hillman E.M., et al. Depth-resolved optical imaging and microscopy of vascular compartment dynamics during somatosensory stimulation. NeuroImage 2007, 35(1):89-104.
45. Hirano Y., Stefanovic B., Silva A.C. Spatiotemporal evolution of the functional magnetic resonance imaging response to ultrashort stimuli. J. Neurosci. 2011, 31(4):1440-1447.
46. Hua J., Stevens R.D., Huang A.J., Pekar J.J., van Zijl P.C. Physiological origin for the BOLD poststimulus undershoot in human brain: vascular compliance versus oxygen metabolism. J. Cereb. Blood Flow Metab. 2011, 31(7):1599-1611.
47. Huttunen J.K., Grohn O., Penttonen M. Coupling between simultaneously recorded BOLD response and neuronal activity in the rat somatosensory cortex. NeuroImage 2008, 39(2):775-785.
48. Jenkinson M., Bannister P., Brady M., Smith S.M. Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage 2002, 17(2):825-841.
49. Kamei A., Houdou S., Mito T., Konomi H., Takashima S. Developmental change in type VI collagen in human cerebral vessels. Pediatr. Neurol. 1992, 8(3):183-186.
50. Kaur C., Ling E.A., Wong W.C. Development of the various glial cell types in the cerebral cortex of postnatal rats. Acta Anat. 1989, 136:204-210.
51. Kuban K., Gilles F.H. Human telencephalic angiogenesis. Ann. Neurol. 1985, 17(6):539-548.
52. Kuklisova-Murgasova M., et al. A dynamic 4D probabilistic atlas of the developing brain. NeuroImage 2011, 54(4):2750-2763.
53. Kusaka T., et al. Functional lateralization of sensorimotor cortex in infants measured using multichannel near-infrared spectroscopy. Pediatr. Res. 2011, 69(5):430-435.
54. Kwong K.K., et al. Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc. Natl. Acad. Sci. U. S. A. 1992, 89(12):5675-5679.
55. Lindauer U., Villringer A., Dirnagel U. Characterisation of CBF response to somatosensory stimulation: model and influence of anesthetics. Am. J. Physiol. 1993, 264(4 Pt 2):H1223-H1228.
56. Lindquist M.A., Loh J.M., Atlas L.Y., Wager T.D. Modeling the hemodynamic response function in fMRI: efficiency, bias and mis-modeling. NeuroImage 2009, 45:S187-S198.
57. Liu T.T., et al. Caffeine alters the temporal dynamics of the visual BOLD response. NeuroImage 2004, 23:1402-1413.
58. Marcar V.L., et al. How depth of anesthesia influences the blood oxygen level-dependent signal from the visual cortex of children. AJNR Am. J. Neuroradiol. 2006, 27(4):799-805.
59. Matsuura T., Fujita H., Kashikura K., Kanno I. Evoked local cerebral blood flow induced by somatosensory stimulation is proportional to the baseline flow. Neurosci. Res. 2000, 38(4):341-348.
60. McCaslin A.F.H., Chen B.R., Radosevich A.J., Cauli B., Hillman E.M.C. In vivo 3D morphology of astrocyte-vasculature interactions in the somatosensory cortex: implications for neurovascular coupling. J. Cereb. Blood Flow Metab. 2011, 31(3):795-806.
61. McClure K.D., McClure S.M., Richter M.C., Richter W. The kinetics of the BOLD response depend on inter-stimulus time. NeuroImage 2005, 27:817-823.
62. Meier P., Zierler L.L. On the theory of the indicator-dilution method for measurement of blood flow and volume. J. Appl. Physiol. 1954, 6:731-744.
63. Merchant N., et al. A patient care system for early 3.0Tesla magnetic resonance imaging of very low birth weight infants. Early Hum. Dev. 2009, 85(12):779-783.
64. Mercuri E., Ricci D., Pane M., Baranello G. The neurological examination of the newborn baby. Early Hum. Dev. 2005, 81(12):947-956.
65. Miezin F.M., Maccotta L., Ollinger J.M., Peterson S.E., Buckner R.L. Characterizing the hemodynamic response: effects of presentation rate, sampling procedure, and the possibility of ordering brain activity based on relative timing. NeuroImage 2000, 11:735-759.
66. Miranda M.J., Olofsson K., Sidaros K. Noninvasive measurements of regional perfusion in preterm and term neonates by magnetic resonance arterial spin labelling. Pediatr. Res. 2006, 60(3):359-363.
67. Monti M.M. Statistical analysis of fMRI time-series: a critical review of the GLM approach. Front. Hum. Neurosci. 2011, 5(28):1-13.
68. Murphy K., Bodurka J., Bandettini P.A. How long to scan? The relationship between fMRI temporal signal to noise ratio and necessary scan duration. NeuroImage 2007, 34:565-574.
69. Norman M.G., O'Klusky J.R. The growth and development of microvasculature in human cerebral cortex. J. Neuropathol. Exp. Neurol. 1986, 45(3):222-233.
70. Ogawa S., et al. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc. Natl. Acad. Sci. U. S. A. 1992, 89(13):5951-5955.
71. Parelkar N.K., et al. 2,2,2-Trichloroethanol activates a nonclassical potassium channel in cerebrovascular smooth muscle and dilates the middle cerebral artery. J. Pharmacol. Exp. Ther. 2010, 332(3):803-810.
72. Perthen J.E., et al. Caffeine-induced uncoupling of cerebral blood flow and oxygen metabolism: a calibrated BOLD fMRI study. NeuroImage 2008, 40(1):237-247.
73. Power J.D., Barnes K.A., Snyder A.Z., Schlaggar B.L., Peterson S.E. Spurious but systematic correlations in functional connectivity networks arise from subject motion. NeuroImage 2012, 59(3):2142-2154.
74. Risser L., Plouraboue 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.
75. Rivkin M.J., et al. Prolonged T2* values in newborn versus adult brain: implications for fMRI studies of newborns. Magn. Reson. Med. 2004, 51:1287-1291.
76. Roche-Labarbe, et al. Near-infrared spectroscopy assessment of cerebral oxygen metabolism in the developing premature brain. J. Cereb. Blood Blow Metab. 2011, 32(3):481-488.
77. Rueckert D., et al. Non-rigid registration using free-form deformations: applications to breast images. IEEE Trans. Med. Imaging 1999, 18(8):712-721.
78. Rutherford M.A. MRI of the Neonatal Brain 2001, W.B. Saunders, Philadelphia, PA, (http://www.mrineonatalbrain.com). 1st edition.
79. Satterthwaite T.D., Wolf D.H., Loughead J., et al. Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. NeuroImage 2012, 60(1):623-632.
80. Seghier M.L., et al. Combination of event-related fMRI and diffusion tensor imaging in an infant with perinatal stroke. NeuroImage 2004, 21(1):463-472.
81. Seghier M.L., Lazeyras, Huppi P.S. Functional MRI of the newborn. Semin. Fetal Neonatal. Med. 2006, 11:479-488.
82. Sisson D.F., Siegel J. Chloral hydrate anesthesia: EEG power spectrum analysis and effects on VEPs in the rat. Neurotoxicol. Teratol. 1989, 11(1):51-56.
83. Smith S.M., et al. Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 2004, 23(supp 1):s208-s219.
84. Steffener J., Tabert M., Reuben A., Stern Y. Investigating hemodynamic response variability using basis functions. NeuroImage 2010, 49:2113-2122.
85. Uematsu M., Takasawa M., Hosoi R., Inoue O. Uncoupling of flow and metabolism by chloral hydrate: a rat in-vivo autoradiographic study. Neuroreport 2009, 20:219-222.
86. Van Dijk K.R., Sabuncu M.R., Buckner R.L. The influence of head motion on intrinsic functional connectivity MRI. NeuroImage 2012, 59(1):431-438.
87. Vanhatalo S., Lauronen L. Neonatal SEP-back to bedside with basic science. Semin. Fetal Neonatal. Med. 2006, 11:464-470.
88. Varela M., Groves A.G., Arichi T., Hajnal J.V. Mean cerebral blood flow measurements using phase contrast MRI in the first year of life. NMR Biomed. 2012, (Electronic publication ahead of print). http://dx.doi.org/10.1002/nbm.2771.
89. Volpe J.J. Brain injury in premature infants: a complex amalgram of destructive and developmental disturbances. Lancet Neurol. 2009, 8(1):110-124.
90. Woolrich M.W., Ripley B.D., Brady J.M., Smith S.M. Temporal autocorrelation in univariate modelling of fMRI data. NeuroImage 2001, 14(6):1370-1386.
91. Woolrich M.W., Behrens T.E., Smith S.M. Constrained linear basis sets for HRF modelling using variational Bayes. NeuroImage 2004, 221:1748-1761.
92. Wyatt J.S., et al. Quantitation of cerebral blood volume in human infants by near-infrared spectroscopy. J. Appl. Physiol. 1990, 68(3):1086-1091.
93. Yamada H., et al. A milestone for normal development of the infantile brain detected by functional MRI. Neurology 2000, 55(2):218-223.
94. Yesilyurt B., Whittingstall K., Ugurbil K., Logethetis N.K., Uludag K. Relationship of the BOLD signal with VEP for ultrashort duration visual stimuli (0.1 to 5ms) in humans. J. Cereb. Blood Flow Metab. 2010, 30(2):449-458.
95. Zhang Y., Brady M., Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans. Med. Imaging 2001, 20(1):45-57.