Fetal functional imaging portrays heterogeneous development of emerging human brain networks

Frontiers in Human Neuroscience

Volumn 8, Issue OCT, 2014, Pages

  Jakab, András ^a   Schwartz, Ernst ^a   Kasprian, Gregor ^a   Gruber, Gerlinde M ^b   Prayer, Daniela ^a   Schöpf, Veronika ^a   Langs, Georg ^a,c  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b Medical University of Vienna   (Austria)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Connectome; Fetal brain connectivity; Fetal brain development; Fetal functional MRI; Prenatal development

Indexed keywords

ARTICLE; BRAIN; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN REGION; COGNITION; CROSS-SECTIONAL STUDY; DATA ANALYSIS; FEMALE; FETUS; FETUS (ANATOMY); FETUS BRAIN; FRONTAL CORTEX; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; GESTATIONAL AGE; HUMAN; IMAGE PROCESSOR; IN VIVO STUDY; MALE; PARIETAL CORTEX; SENSORIMOTOR CORTEX; SUBCORTEX;

EID: 84933671771     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00852     Document Type: Article

References (94)

1. Achard, S., Salvador, R., Whitcher, B., Suckling, J., and Bullmore, E. (2006). A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J. Neurosci. 26, 63-72. doi: 10.1523/JNEUROSCI.3874-05.2006
2. Behzadi, Y., Restom, K., Liau, J., and Liu, T. T. (2007). A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 37, 90-101. doi: 10.1016/j.neuroimage.2007.04.042
3. Birn, R. M., Murphy, K., and Bandettini, P. A. (2008). The effect of respiration variations on independent component analysis results of resting state functional connectivity. Hum. Brain Mapp. 29, 740-750. doi: 10.1002/hbm.20577
4. Buckner, R. L., and Krienen, F. M. (2013). The evolution of distributed association networks in the human brain. Trends Cogn. Sci. (Regul. Ed.) 17, 648-665. doi: 10.1016/j.tics.2013.09.017
5. Buckner, R. L., Krienen, F. M., and Yeo, B. T. T. (2013). Opportunities and limitations of intrinsic functional connectivity MRI. Nat. Neurosci. 16, 832-837. doi: 10.1038/nn.3423
6. Bullmore, E., and Sporns, O. (2009). Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Rev. Neurosci. 10, 186-198. doi: 10.1038/nrn2575
7. Bystron, I., Blakemore, C., and Rakic, P. (2008). Development of the human cerebral cortex: boulder committee revisited. Nat. Rev. Neurosci. 9, 110-122. doi: 10.1038/nrn2252
8. Chung, H. W., Chen, C. Y., Zimmerman, R. A., Lee, K. W., Lee, C. C., and Chin, S. C. (2000). T2-Weighted fast MR imaging with true FISP versus HASTE: comparative efficacy in the evaluation of normal fetal brain maturation. AJR Am. J. Roentgenol. 175, 1375-1380. doi: 10.2214/ajr.175.5.1751375
9. Clancy, B., Darlington, R. B., and Finlay, B. L. (2001). Translating developmental time across mammalian species. Neuroscience 105, 7-17. doi: 10.1016/S0306-4522(01)00171-3
10. Colonnese, M., and Khazipov, R. (2012). Spontaneous activity in developing sensory circuits: implications for resting state fMRI. Neuroimage 62, 2212-2221. doi: 10.1016/j.neuroimage.2012.02.046
11. Craddock, R. C., James, G. A., Holtzheimer, P. E. III, Hu, X. P., and Mayberg, H. S. (2012). A whole brain fMRI atlas generated via spatially constrained spectral clustering. Hum. Brain Mapp. 33, 1914-1928. doi: 10.1002/hbm.21333
12. Damaraju, E., Phillips, J. R., Lowe, J. R., Ohls, R., Calhoun, V. D., and Caprihan, A. (2010). Resting-state functional connectivity differences in premature children. Front. Syst. Neurosci. 4:23. doi: 10.3389/fnsys.2010.00023
13. D'Elia, A., Pighetti, M., Moccia, G., and Santangelo, N. (2001). Spontaneous motor activity in normal fetuses. Early Hum. Dev. 65, 139-147. doi: 10.1016/S0378-3782(01)00224-9
14. Dennis, E. L., Jahanshad, N., McMahon, K. L., de Zubicaray, G. I., Martin, N. G., Hickie, I. B.,et al. (2013). Development of brain structural connectivity between ages 12 and 30: a 4-tesla diffusion imaging study in 439 adolescents and adults. Neuroimage 64, 671-684. doi: 10.1016/j.neuroimage.2012.09.004
15. Desikan, R. S., Ségonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D.,et al. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31, 968-980. doi: 10.1016/j.neuroimage.2006.01.021
16. Doria, V., Beckmann, C. F., Arichi, T., Merchant, N., Groppo, M., Turkheimer, F. E.,et al. (2010). Emergence of resting state networks in the preterm human brain. Proc. Natl. Acad. Sci. U.S.A. 107, 20015-20020. doi: 10.1073/pnas.1007921107
17. Dubois, J., Dehaene-Lambertz, G., Perrin, M., Mangin, J. F., Cointepas, Y., Duchesnay, E.,et al. (2008). Asynchrony of the early maturation of white matter bundles in healthy infants: quantitative landmarks revealed noninvasively by diffusion tensor imaging. Hum. Brain Mapp. 29, 14-27. doi: 10.1002/hbm.20363
18. Fjell, A. M., Westlye, L. T., Amlien, I., Tamnes, C. K., Grydeland, H., Engvig, A.,et al. (2013). High-expanding cortical regions in human development and evolution are related to higher intellectual abilities. Cereb. Cortex doi: 10.1093/cercor/bht201 [Epub ahead of print].
19. Flechsig, P. E. (1920). Anatomie des Menschlichen Gehirns und Rückenmarks auf Myelogenetischer Grundlage. Leipzig: G. Thieme.
20. Fransson, P. (2005). Spontaneous low-frequency BOLD signal fluctuations: an fMRI investigation of the resting-state default mode of brain function hypothesis. Hum. Brain Mapp. 26, 15-29. doi: 10.1002/hbm.20113
21. Geschwind, N. (1964). "The development of the brain and the evolution of language," in Monograph Series on Language and Linguistics, ed. C. I. J. M. Stuart (Washington, DC: Georgetown University Press).
22. Glenn, O. A., and Barkovich, A. J. (2006). Magnetic resonance imaging of the fetal brain and spine: an increasingly important tool in prenatal diagnosis, part 1. AJNR Am. J. Neuroradiol. 27, 1604-1611.
23. Gowland, P., and Fulford, J. (2004). Initial experiences of performing fetal fMRI. Exp. Neurol. 190(Suppl. 1), 22-27. doi: 10.1016/j.expneurol.2004.06.022
24. Greicius, M. (2008). Resting-state functional connectivity in neuropsychiatric disorders. Curr. Opin. Neurol. 21, 424-430. doi: 10.1097/WCO.0b013e328306f2c5
25. Greicius, M. D., Krasnow, B., Reiss, A. L., and Menon, V. (2003). Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. U.S.A. 100, 253-258. doi: 10.1073/pnas.0135058100
26. Hill, J., Inder, T., Neil, J., Dierker, D., Harwell, J., and Van Essen, D. (2010). Similar patterns of cortical expansion during human development and evolution. Proc. Natl. Acad. Sci. U.S.A. 107, 13135-13140. doi: 10.1073/pnas.1001229107
27. Holst, M., Eswaran, H., Lowery, C., Murphy, P., Norton, J., and Preissl, H. (2005). Development of auditory evoked fields in human fetuses and newborns: a longitudinal MEG study. Clin. Neurophysiol. 116, 1949-1955. doi: 10.1016/j.clinph.2005.04.008
28. Honey, C. J., Sporns, O., Cammoun, L., Gigandet, X., Thiran, J. P., Meuli, R.,et al. (2009). Predicting human resting-state functional connectivity from structural connectivity. Proc. Natl. Acad. Sci. U.S.A. 106, 2035-2040. doi: 10.1073/pnas.0811168106
29. Huang, H., Xue, R., Zhang, J., Ren, T., Richards, L. J., Yarowsky, P.,et al. (2009). Anatomical characterization of human fetal brain development with diffusion tensor magnetic resonance imaging. J. Neurosci. 29, 4263-4273. doi: 10.1523/JNEUROSCI.2769-08.2009
30. Jakob, H., and Beckmann, H. (1986). Prenatal developmental disturbances in the limbic allocortex in schizophrenics. J. Neural Transm. 65, 303-326. doi: 10.1007/BF01249090
31. Jardri, R., Houfflin-Debarge, V., Delion, P., Pruvo, J. P., Thomas, P., and Pins, D. (2012). Assessing fetal response to maternal speech using a noninvasive functional brain imaging technique. Int. J. Dev. Neurosci. 30, 159-161. doi: 10.1016/j.ijdevneu.2011.11.002
32. Jardri, R., Pins, D., Houfflin-Debarge, V., Chaffiotte, C., Rocourt, N., Pruvo, J. P.,et al. (2008). Fetal cortical activation to sound at 33 weeks of gestation: a functional MRI study. Neuroimage 42, 10-18. doi: 10.1016/j.neuroimage.2008.04.247
33. Jenkinson, M., Beckmann, C. F., Behrens, T. E., Woolrich, M. W., and Smith, S. M. (2012). FSL. Neuroimage 62, 782-790. doi: 10.1016/j.neuroimage.2011.09.015
34. Johansen-Berg, H., and Rushworth, M. F. S. (2009). Using diffusion imaging to study human connectional anatomy. Annu. Rev. Neurosci. 32, 75-94. doi: 10.1146/annurev.neuro.051508.135735
35. Johnson, M. H. (2001). Functional brain development in humans. Nat. Rev. Neurosci. 2, 475-483. doi: 10.1038/35081509
36. Jokhi, R. P., and Whitby, E. H. (2011). Magnetic resonance imaging of the fetus. Dev. Med. Child Neurol. 53, 18-28. doi: 10.1111/j.1469-8749.2010.03813.x
37. Joseph, R. (2000). Fetal brain behavior and cognitive development. Dev. Rev. 20, 81-98. doi: 10.1006/drev.1999.0486
38. Judas, M., Sedmak, G., and Kostovic, I. (2013). The significance of the subplate for evolution and developmental plasticity of the human brain. Front. Hum. Neurosci. 7:423. doi: 10.3389/fnhum.2013.00423
39. Kanold, P. O. (2009). Subplate neurons: crucial regulators of cortical development and plasticity. Front. Neuroanat. 3:16. doi: 10.3389/neuro.05.016.2009
40. Kasprian, G., Brugger, P. C., Weber, M., Krssák, M., Krampl, E., Herold, C.,et al. (2008). In utero tractography of fetal white matter development. Neuroimage 43, 213-224. doi: 10.1016/j.neuroimage.2008.07.026
41. Kelly, C., Biswal, B. B., Craddock, R. C., Castellanos, F. X., and Milham, M. P. (2012). Characterizing variation in the functional connectome: promise and pitfalls. Trends Cogn. Sci. (Regul. Ed.) 16, 181-188. doi: 10.1016/j.tics.2012.02.001
42. Khazipov, R., and Luhmann, H. J. (2006). Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci. 29, 414-418. doi: 10.1016/j.tins.2006.05.007
43. Kinney, H. C., Brody, B. A., Kloman, A. S., and Gilles, F. H. (1988). Sequence of central nervous system myelination in human infancy. II. Patterns of myelination in autopsied infants. J. Neuropathol. Exp. Neurol. 47, 217-234. doi: 10.1097/00005072-198805000-00003
44. Kok, R. D., de Vries, M. M., Heerschap, A., and van den Berg, P. P. (2004). Absence of harmful effects of magnetic resonance exposure at 1.5 T in utero during the third trimester of pregnancy: a follow-up study. Magn. Reson. Imaging 22, 851-854. doi: 10.1016/j.mri.2004.01.047
45. Kok, R. D., van den Bergh, A. J., Heerschap, A., Nijland, R., and van den Berg, P. P. (2001). Metabolic information from the human fetal brain obtained with proton magnetic resonance spectroscopy. Am. J. Obstet. Gynecol. 185, 1011-1015. doi: 10.1067/mob.2001.117677
46. Kostovic, I., and Judas, M. (2010). The development of the subplate and thalamocortical connections in the human foetal brain. Acta Paediatr. 99, 1119-1127. doi: 10.1111/j.1651-2227.2010.01811.x
47. Kostovic, I., Judas, M., Rados, M., and Hrabac, P. (2002). Laminar organization of the human fetal cerebrum revealed by histochemical markers and magnetic resonance imaging. Cereb. Cortex 12, 536-544. doi: 10.1093/cercor/12.5.536
48. Kostovic, I., and Molliver, M. (1974). New interpretation of laminar development of cerebral-cortex-synaptogenesis in different layers of neopallium in human fetus. Anat. Rec. 178:395.
49. Lauritzen, M. (2005). Reading vascular changes in brain imaging: is dendritic calcium the key? Nat. Rev. Neurosci. 6, 77-85. doi: 10.1038/nrn1589
50. Lee, W., Morgan, B. R., Shroff, M. M., Sled, J. G., and Taylor, M. J. (2013). The development of regional functional connectivity in preterm infants into early childhood. Neuroradiology 55(Suppl. 2), 105-111. doi: 10.1007/s00234-013-1232-z
51. Logothetis, N. K., and Wandell, B. A. (2004). Interpreting the BOLD signal. Annu. Rev. Physiol. 66, 735-769. doi: 10.1146/annurev.physiol.66.082602.092845
52. Lopez-Bendito, G., and Molnar, Z. (2003). Thalamocortical development: how are we going to get there? Nat. Rev. Neurosci. 4, 276-289. doi: 10.1038/nrn1075
53. Lowe, M., Mock, B., and Sorenson, J. (1998). Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage 7, 119-132. doi: 10.1006/nimg.1997.0315
54. Luhmann, H. J., Kilb, W., and Hanganu-Opatz, I. L. (2009). Subplate cells: amplifiers of neuronal activity in the developing cerebral cortex. Front. Neuroanat. 3:19. doi: 10.3389/neuro.05.019.2009
55. Maas, L. C., Mukherjee, P., Carballido-Gamio, J., Veeraraghavan, S., Miller, S. P., Partridge, S. C.,et al. (2004). Early laminar organization of the human cerebrum demonstrated with diffusion tensor imaging in extremely premature infants. Neuroimage 22, 1134-1140. doi: 10.1016/j.neuroimage.2004.02.035
56. Mailath-Pokorny, M., Kasprian, G., Mitter, C., Schöpf, V., Nemec, U., and Prayer, D. (2012). Magnetic resonance methods in fetal neurology. Semin. Fetal Neonatal Med. 17, 278-284. doi: 10.1016/j.siny.2012.06.002
57. Mantini, D., Corbetta, M., Romani, G. L., Orban, G. A., and Vanduffel, W. (2013). Evolutionarily novel functional networks in the human brain? J. Neurosci. 33, 3259-3275. doi: 10.1523/JNEUROSCI.4392-12.2013
58. Molnár, Z., Métin, C., Stoykova, A., Tarabykin, V., Price, D. J., Francis, F.,et al. (2006). Comparative aspects of cerebral cortical development. Eur. J. Neurosci. 23, 921-934. doi: 10.1111/j.1460-9568.2006.04611.x
59. Moore, A. R., Filipovic, R., Mo, Z., Rasband, M. N., Zecevic, N., and Antic, S. D. (2009). Electrical excitability of early neurons in the human cerebral cortex during the second trimester of gestation. Cereb. Cortex 19, 1795-1805. doi: 10.1093/cercor/bhn206
60. Morokuma, S., Fukushima, K., Otera, Y., Yumoto, Y., Tsukimori, K., Ochiai, M.,et al. (2013). Ultrasound evaluation of fetal brain dysfunction based on behavioral patterns. Brain Dev. 35, 61-67. doi: 10.1016/j.braindev.2012.01.007
61. Mueller, S., Wang, D., Fox, M. D., Yeo, B. T., Sepulcre, J., Sabuncu, M. R.,et al. (2013). Individual variability in functional connectivity architecture of the human brain. Neuron 77, 586-595. doi: 10.1016/j.neuron.2012.12.028
62. Neubert, F., Mars, R., Thomas, A., Sallet, J., and Rushworth, M. S. (2014). Comparison of Human ventral frontal cortex areas for cognitive control and language with areas in monkey frontal cortex. Neuron 81, 700-713. doi: 10.1016/j.neuron.2013.11.012
63. Nooner, K. B., Colcombe, S., Tobe, R., Mennes, M., Benedict, M., Moreno, A.,et al. (2012). The NKI-Rockland sample: a model for accelerating the pace of discovery science in psychiatry. Front. Neurosci. 6:152. doi: 10.3389/fnins.2012.00152
64. Oakes, T., Johnstone, T., Ores Walsh, K., Greischar, L., Alexander, A., Fox, A.,et al. (2005). Comparison of fMRI motion correction software tools. Neuroimage 28, 529-543. doi: 10.1016/j.neuroimage.2005.05.058
65. Partanen, E., Kujala, T., Naatanen, R., Liitola, A., Sambeth, A., and Huotilainen, M. (2013a). Learning-induced neural plasticity of speech processing before birth. Proc. Natl. Acad. Sci. U.S.A. 110, 15145-15150. doi: 10.1073/pnas.1302159110
66. Partanen, E., Kujala, T., Tervaniemi, M., and Huotilainen, M. (2013b). Prenatal music exposure induces long-term neural effects. PLoS ONE 8:e78946. doi: 10.1371/journal.pone.0078946
67. Paul, L. K., Brown, W. S., Adolphs, R., Tyszka, J. M., Richards, L. J., Mukherjee, P.,et al. (2007). Agenesis of the corpus callosum: genetic, developmental and functional aspects of connectivity. Nat. Rev. Neurosci. 8, 287-299. doi: 10.1038/nrn2107
68. Penn, A. A., and Shatz, C. J. (1999). Brain waves and brain wiring: the role of endogenous and sensory-driven neural activity in development. Pediatr. Res. 45, 447-458. doi: 10.1203/00006450-199904010-00001
69. Power, J. D., Barnes, K. A., Snyder, A. Z., Schlaggar, B. L., and Petersen, S. E. (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59, 2142-2154. doi: 10.1016/j.neuroimage.2011.10.018
70. Prayer, D., Kasprian, G., Krampl, E., Ulm, B., Witzani, L., Prayer, L.,et al. (2006). MRI of normal fetal brain development. Eur. J. Radiol. 57, 199-216. doi: 10.1016/j.ejrad.2005.11.020
71. Preuss, T. M. (2009). "The cognitive neuroscience of human uniqueness," in, The Cognitive Neurosciences, ed. M. S. Gazzaniga (Cambridge, MA: MIT Press), 49-64.
72. Price, D. J., Kennedy, H., Dehay, C., Zhou, L., Mercier, M., Jossin, Y.,et al. (2006). The development of cortical connections. Eur. J. Neurosci. 23, 910-920. doi: 10.1111/j.1460-9568.2006.04620.x
73. Pugash, D., Brugger, P. C., Bettelheim, D., and Prayer, D. (2008). Prenatal ultrasound and fetal MRI: the comparative value of each modality in prenatal diagnosis. Eur. J. Radiol. 68, 214-226. doi: 10.1016/j.ejrad.2008.06.031
74. Rakic, P. (2009). Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 10, 724-735. doi: 10.1038/nrn2719
75. Rice, D., and Barone, S. (2000). Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ. Health Perspect. 108(Suppl. 3), 511-533. doi: 10.1289/ehp.00108s3511
76. Rilling, J. K. (2014). Comparative primate neuroimaging: insights into human brain evolution. Trends Cogn. Sci. (Regul. Ed.) 18, 46-55. doi: 10.1016/j.tics.2013.09.013
77. Rubinov, M., and Sporns, O. (2010). Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52, 1059-1069. doi: 10.1016/j.neuroimage.2009.10.003
78. Rueckert, D. (2012). A Multi-channel 4D Probabilistic Atlas of the Developing Fetal Brain. Available at:http://biomedic.doc.ic.ac.uk/brain-development/index.php?n=Main.Fetal-(accessed November 1, 2013).
79. Schlotz, W., and Phillips, D. I. W. (2009). Fetal origins of mental health: evidence and mechanisms. Brain Behav. Immun. 23, 905-916. doi: 10.1016/j.bbi.2009.02.001
80. Schöpf, V., Kasprian, G., Brugger, P. C., and Prayer, D. (2012). Watching the fetal brain at "rest." Int. J. Dev. Neurosci. 30, 11-17. doi: 10.1016/j.ijdevneu.2011.10.006
81. Serag, A., Aljabar, P., Ball, G., Counsell, S. J., Boardman, J. P., Rutherford, M. A.,et al. (2012). Construction of a consistent high-definition spatio-temporal atlas of the developing brain using adaptive kernel regression. Neuroimage 59, 2255-2265. doi: 10.1016/j.neuroimage.2011.09.062
82. Shmueli, K., van Gelderen, P., de Zwart, J. A., Horovitz, S. G., Fukunaga, M., Jansma, J. M.,et al. (2007). Low-frequency fluctuations in the cardiac rate as a source of variance in the resting-state fMRI BOLD signal. Neuroimage 38, 306-320. doi: 10.1016/j.neuroimage.2007.07.037
83. Smyser, C. D., Inder, T. E., Shimony, J. S., Hill, J. E., Degnan, A. J., Snyder, A. Z.,et al. (2010). Longitudinal analysis of neural network development in preterm infants. Cereb. Cortex 20, 2852-2862. doi: 10.1093/cercor/bhq035
84. Thomason, M. E., Dassanayake, M. T., Shen, S., Katkuri, Y., Alexis, M., Anderson, A. L.,et al. (2013). Cross-hemispheric functional connectivity in the human fetal brain. Sci. Transl. Med. 5:173ra24.
85. Trivedi, R., Gupta, R. K., Husain, N., Rathore, R. K., Saksena, S., Srivastava, S.,et al. (2009). Region-specific maturation of cerebral cortex in human fetal brain: diffusion tensor imaging and histology. Neuroradiology 51, 567-576. doi: 10.1007/s00234-009-0533-8
86. Uğurbil, K., Xu, J., Auerbach, E. J., Moeller, S., Vu, A. T., Duarte-Carvajalino, J. M.,et al. (2013). Pushing spatial and temporal resolution for functional and diffusion MRI in the human connectome project. Neuroimage 80, 80-104. doi: 10.1016/j.neuroimage.2013.05.012
87. van den Heuvel, M. P., Stam, C. J., Kahn, R. S., and Hulshoff Pol, H. E. (2009). Efficiency of functional brain networks and intellectual performance. J. Neurosci. 29, 7619-7624. doi: 10.1523/JNEUROSCI.1443-09.2009
88. Vanhatalo, S., and Kaila, K. (2006). Development of neonatal EEG activity: from phenomenology to physiology. Semin. Fetal Neonatal Med. 11, 471-478. doi: 10.1016/j.siny.2006.07.008
89. Weissenbacher, A., Kasess, C., Gerstl, F., Lanzenberger, R., Moser, E., and Windischberger, C. (2009). Correlations and anticorrelations in resting-state functional connectivity MRI: a quantitative comparison of preprocessing strategies. Neuroimage 47, 1408-1416. doi: 10.1016/j.neuroimage.2009.05.005
90. Yakovlev, P. I., and Lecours, A. (1967). "The myelogenetic cycles of regional maturation of the brain," in Regional Development of the Brain in Early Life, ed. A. Minkowski (Oxford: Blackwell), 3-70.
91. Yan, C., Craddock, R. C., Zuo, X., Zang, Y., and Milham, M. P. (2013). Standardizing the intrinsic brain: towards robust measurement of inter-individual variation in 1000 functional connectomes. Neuroimage 80, 246-262. doi: 10.1016/j.neuroimage.2013.04.081
92. Yoshida, S., Oishi, K., Faria, A., and Mori, S. (2013). Diffusion tensor imaging of normal brain development. Pediatr. Radiol. 43, 15-27. doi: 10.1007/s00247-012-2496-x
93. Zalesky, A., Fornito, A., and Bullmore, E. T. (2010). Network-based statistic: identifying differences in brain networks. Neuroimage 53, 1197-1207. doi: 10.1016/j.neuroimage.2010.06.041
94. Zhang, L. I., and Poo, M. M. (2001). Electrical activity and development of neural circuits. Nat. Neurosci. 4(Suppl.), 1207-1214. doi: 10.1038/nn753