Emergence of a hierarchical brain during infancy reflected by stepwise functional connectivity

Human Brain Mapping

Volumn 38, Issue 5, 2017, Pages 2666-2682

  Pendl, Suzanne L ^a   Salzwedel, Andrew P ^a   Goldman, Barbara D ^b   Barrett, Lisa F ^c,d   Lin, Weili ^e   Gilmore, John H ^e   Gao, Wei ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b University of North Carolina at Chapel Hill   (United States)

^c NORTHEASTERN UNIVERSITY   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

early brain development; hierarchical brain organization; predictive coding; sensory integration; stepwise functional connectivity

Indexed keywords

ADULT; AMYGDALA; ARTICLE; BASAL GANGLION; BLOOD OXYGENATION; BRAIN; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN REGION; CHILD DEVELOPMENT; COGNITIVE DEVELOPMENT; CORPUS STRIATUM; DORSAL ANTERIOR CINGULATE CORTEX; DORSOMEDIAL PREFRONTAL CORTEX; FEMALE; FRONTAL LOBE; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HIPPOCAMPUS; HUMAN; IMAGE ANALYSIS; INFANT; INSULA; LEARNING; MAJOR CLINICAL STUDY; MALE; MIDDLE FRONTAL GYRUS; NEUROPSYCHOLOGICAL TEST; PARAHIPPOCAMPAL GYRUS; POSTERIOR CINGULATE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PUTAMEN; RESTING STATE NETWORK; SENSORIMOTOR CORTEX; SENSORY CORTEX; SUPERIOR PARIETAL LOBULE; SUPERIOR TEMPORAL SULCUS; SUPPLEMENTARY MOTOR AREA; TEMPORAL LOBE; THALAMUS; VISUAL CORTEX; ADOLESCENT; AGE; BLOOD; BRAIN MAPPING; COGNITION; DIAGNOSTIC IMAGING; GROWTH, DEVELOPMENT AND AGING; IMAGE PROCESSING; LONGITUDINAL STUDY; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PRESCHOOL CHILD; SENSATION; YOUNG ADULT;

OXYGEN;

ADOLESCENT; ADULT; AGE FACTORS; BRAIN; BRAIN MAPPING; CHILD, PRESCHOOL; COGNITION; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INFANT; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; OXYGEN; SENSATION; YOUNG ADULT;

EID: 85014481201     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.23552     Document Type: Article

References (95)

1. Alcauter S, Lin W, Smith JK, Gilmore JH, Gao W (2013): Consistent anterior–posterior segregation of the insula during the first 2 years of life. Cereb Cortex 25:1176–1187.
2. Alcauter S, Lin W, Smith JK, Short SJ, Goldman BD, Reznick JS, Gilmore JH, Gao W (2014): Development of thalamocortical connectivity during infancy and its cognitive correlations. J Neurosci 34:9067–9075.
3. Allen EA, Erhardt EB, Damaraju E, Gruner W, Segall JM, Silva RF, Havlicek M, Rachakonda S, Fries J, Kalyanam R, Michael AM, Caprihan A, Turner JA, Eichele T, Adelsheim S, Bryan AD, Bustillo J, Clark VP, Feldstein Ewing SW, Filbey F, Ford CC, Hutchison K, Jung RE, Kiehl KA, Kodituwakku P, Komesu YM, Mayer AR, Pearlson GD, Phillips JP, Sadek JR, Stevens M, Teuscher U, Thoma RJ, Calhoun VD (2011): A baseline for the multivariate comparison of resting-state networks. Front Syst Neurosci 5:2.
4. Amiez C, Petrides M (2009): Anatomical organization of the eye fields in the human and non-human primate frontal cortex. Prog Neurobiol 89:220–230.
5. Bahrick LE, Lickliter R (2000): Intersensory redundancy guides attentional selectivity and perceptual learning in infancy. Dev Psychol 36:190.
6. Barrett LF, Simmons WK (2015): Interoceptive predictions in the brain. Nat Rev Neurosci 16:419–429.
7. Beauchamp MS, Nath AR, Pasalar S (2010): fMRI-Guided transcranial magnetic stimulation reveals that the superior temporal sulcus is a cortical locus of the McGurk effect. J Neurosci 30:2414–2417.
8. Benedict H (1979): Early lexical development: Comprehension and production. J Child Lang 6:183–200.
9. Benjamini Y, Yekutieli D (2001): The control of the false discovery rate in multilpe testing under dependency. Ann Statist 29:1165–1188.
10. Binder JR, Desai RH, Graves WW, Conant LL (2009): Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb Cortex 19:2767–2796.
11. Binkofski F, Buccino G, Posse S, Seitz RJ, Rizzolatti G, Freund HJ (1999): A fronto-parietal circuit for object manipulation in man: Evidence from an fMRI-study. Eur J Neurosci 11:3276–3286.
12. Biswal B, Zerrin Yetkin F, Haughton VM, Hyde JS (1995): Functional connectivity in the motor cortex of resting human brain using echo-planar mri. Magn Reson Med 34:537–541.
13. Blank H, Anwander A, von Kriegstein K (2011): Direct structural connections between voice-and face-recognition areas. J Neurosci 31:12906–12915.
14. Brauer J, Anwander A, Perani D, Friederici AD (2013): Dorsal and ventral pathways in language development. Brain Lang 127:289–295.
15. Bullmore E, Sporns O (2012): The economy of brain network organization. Nat Rev Neurosci 13:336–349.
16. Burr D, Gori M (2012): Multisensory integration develops late in humans. In: Murray MM, Wallace MT, editors. The Neural Bases of Multisensory Processes. Boca Raton (FL): CRC Press/Taylor & Francis.
17. Cai Q, Paulignan Y, Brysbaert M, Ibarrola D, Nazir TA (2010): The left ventral occipito-temporal response to words depends on language lateralization but not on visual familiarity. Cereb Cortex 20:1153–1163.
18. Chanes L, Barrett LF (2016): Redefining the role of limbic areas in cortical processing. Trends Cogn Sci 20:96–106.
19. Chang C, Glover GH (2009): Effects of model-based physiological noise correction on default mode network anti-correlations and correlations. Neuroimage 47:1448–1459.
20. Cole MW, Reynolds JR, Power JD, Repovs G, Anticevic A, Braver TS (2013): Multi-task connectivity reveals flexible hubs for adaptive task control. Nat Neurosci 16:1348–1355.
21. Conant LL, Liebenthal E, Desai A, Binder JR (2014): FMRI of phonemic perception and its relationship to reading development in elementary-to middle-school-age children. Neuroimage 89:192–202.
22. Connolly JD, Andersen RA, Goodale MA (2003): FMRI evidence for a'parietal reach region'in the human brain. Exp Brain Res 153:140–145.
23. Corbetta M, Shulman GL (2002): Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201–215.
24. Corbetta M, Patel G, Shulman GL (2008): The reorienting system of the human brain: From environment to theory of mind. Neuron 58:306–324.
25. Culham JC, Danckert SL, De Souza JF, Gati JS, Menon RS, Goodale MA (2003): Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas. Exp Brain Res 153:180–189.
26. Cunnington R, Windischberger C, Deecke L, Moser E (2003): The preparation and readiness for voluntary movement: A high-field event-related fMRI study of the Bereitschafts-BOLD response. Neuroimage 20:404–412.
27. Damasio AR (1989): Time-locked multiregional retroactivation: A systems-level proposal for the neural substrates of recall and recognition. Cognition 33:25–62.
28. Deak GO, Krasno AM, Triesch J, Lewis J, Sepeta L (2014): Watch the hands: Infants can learn to follow gaze by seeing adults manipulate objects. Dev Sci 17:270–281.
29. Driver J, Noesselt T (2008): Multisensory interplay reveals crossmodal influences on ‘sensory-specific'brain regions, neural responses, and judgments. Neuron 57:11–23.
30. Fenson L, Dale PS, Reznick JS, Bates E, Thal DJ, Pethick SJ, Tomasello M, Mervis CB, Stiles J (1994): Variability in early communicative development. Monogr Soc Res Child Dev 59:1–173.
31. Fernandino L, Binder JR, Desai RH, Pendl SL, Humphries CJ, Gross WL, Conant LL, Seidenberg MS (2016): Concept representation reflects multimodal abstraction: A framework for embodied semantics. Cereb Cortex 26:2018–2034.
32. Foxe JJ, Wylie GR, Martinez A, Schroeder CE, Javitt DC, Guilfoyle D, Ritter W, Murray MM (2002): Auditory-somatosensory multisensory processing in auditory association cortex: An fMRI study. J Neurophysiol 88:540–543.
33. Fransson P, Aden U, Blennow M, Lagercrantz H (2011): The functional architecture of the infant brain as revealed by resting-state fMRI. Cereb Cortex 21:145–154.
34. Fried I, Katz A, McCarthy G, Sass KJ, Williamson P, Spencer SS, Spencer DD (1991): Functional organization of human supplementary motor cortex studied by electrical stimulation. J Neurosci 11:3656–3666.
35. Gao W, Lin W (2012): Frontal parietal control network regulates the anti-correlated default and dorsal attention networks. Hum Brain Mapp 33:192–202.
36. Gao W, Lin W, Chen Y, Gerig G, Smith JK, Jewells V, Gilmore JH (2009a): Temporal and spatial development of axonal maturation and myelination of white matter in the developing brain. AJNR Am J Neuroradiol 30:290–296.
37. Gao W, Zhu H, Giovanello KS, Smith JK, Shen D, Gilmore JH, Lin W (2009b): Evidence on the emergence of the brain's default network from 2-week-old to 2-year-old healthy pediatric subjects. Proc Natl Acad Sci U S A 106:6790–6795.
38. Gao W, Gilmore JH, Shen D, Smith JK, Zhu H, Lin W (2013): The synchronization within and interaction between the default and dorsal attention networks in early infancy. Cereb Cortex 23:594–603.
39. Gao W, Alcauter S, Elton A, Hernandez-Castillo CR, Smith JK, Ramirez J, Lin W (2014a): Functional network development during the first year: Relative sequence and socioeconomic correlations. Cereb Cortex 25:2919–2928.
40. Gao W, Alcauter S, Smith J, Gilmore J, Lin W (2014b): Development of human brain cortical network architecture during infancy. Brain Struct Funct 220:1173–1186.
41. Gao W, Lin W, Grewen K, Gilmore JH (2016): Functional connectivity of the infant human brain: Plastic and modifiable. Neuroscientist. pii: 1073858416635986. [Epub ahead of print]
42. Gilmore JH, Shi F, Woolson SL, Knickmeyer RC, Short SJ, Lin W, Zhu H, Hamer RM, Styner M, Shen D (2012): Longitudinal development of cortical and subcortical gray matter from birth to 2 years. Cereb Cortex 22:2478–2485.
43. Girard N, Raybaud C, du Lac P (1991): MRI study of brain myelination. J Neuroradiol 18:291–307.
44. Goldfield BA, Reznick JS (1990): Early lexical acquisition: Rate, content, and the vocabulary spurt. J Child Lang 17:171–183.
45. Grefkes C, Fink GR (2005): REVIEW: The functional organization of the intraparietal sulcus in humans and monkeys. J Anat 207:3–17.
46. Hashimoto R, Sakai KL (2004): Learning letters in adulthood: Direct visualization of cortical plasticity for forming a new link between orthography and phonology. Neuron 42:311–322.
47. Hepper PG, Shahidullah BS (1994): Development of fetal hearing. Arch Dis Child 71:F81–F87.
48. Hickok G, Okada K, Serences JT (2009): Area Spt in the human planum temporale supports sensory-motor integration for speech processing. J Neurophysiol 101:2725–2732.
49. Hickok G, Houde J, Rong F (2011): Sensorimotor integration in speech processing: Computational basis and neural organization. Neuron 69:407–422.
50. Jasso H, Triesch J, Deak G (2008): A reinforcement learning model of social referencing. In: 7th IEEE International Conference on Development and Learning. pp 286–291.
51. Johnson-Frey SH, Vinton D, Norlund R, Grafton ST (2005): Cortical topography of human anterior intraparietal cortex active during visually guided grasping. Cogn Brain Res 23:397–405.
52. Karnath H-O, Perenin M-T (2005): Cortical control of visually guided reaching: Evidence from patients with optic ataxia. Cereb Cortex 15:1561–1569.
53. Kimmerle M, Ferre CL, Kotwica KA, Michel GF (2010): Development of role-differentiated bimanual manipulation during the infant's first year. Dev Psychobiol 52:168–180.
54. Kravitz DJ, Saleem KS, Baker CI, Mishkin M (2011): A new neural framework for visuospatial processing. Nat Rev Neurosci 12:217–230.
55. Langner R, Kellermann T, Eickhoff SB, Boers F, Chatterjee A, Willmes K, Sturm W (2012): Staying responsive to the world: Modality-specific and-nonspecific contributions to speeded auditory, tactile, and visual stimulus detection. Hum Brain Mapp 33:398–418.
56. Liebenthal E, Sabri M, Beardsley SA, Mangalathu-Arumana J, Desai A (2013): Neural dynamics of phonological processing in the dorsal auditory stream. J Neurosci 33:15414–15424.
57. Macaluso E (2010): Orienting of spatial attention and the interplay between the senses. Cortex 46:282–297.
58. Man K, Kaplan J, Damasio H, Damasio A (2013): Neural convergence and divergence in the mammalian cerebral cortex: From experimental neuroanatomy to functional neuroimaging. J Comp Neurol 521:4097–4111.
59. Mano QR, Humphries C, Desai RH, Seidenberg MS, Osmon DC, Stengel BC, Binder JR (2013): The role of left occipitotemporal cortex in reading: Reconciling stimulus, task, and lexicality effects. Cereb Cortex 23:988–1001.
60. Mesulam MM (1998): From sensation to cognition. Brain 121:1013–1052.
61. Miller LM, D'Esposito M (2005): Perceptual fusion and stimulus coincidence in the cross-modal integration of speech. J Neurosci 25:5884–5893.
62. Mullen EM (1995): Mullen Scales of Early Learning. Circle Pines, MN: AGS.
63. Munson B (2001): Phonological pattern frequency and speech production in adults and children. J Speech Lang Hear Res 44:778–792.
64. Murphy K, Birn RM, Handwerker DA, Jones TB, Bandettini PA (2009): The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced?. Neuroimage 44:893–905.
65. Nelson EL, Campbell JM, Michel GF (2013): Unimanual to bimanual: Tracking the development of handedness from 6 to 24 months. Infant Behav Dev 36:181–188.
66. Newman R, Ratner NB, Jusczyk AM, Jusczyk PW, Dow KA (2006): Infants' early ability to segment the conversational speech signal predicts later language development: A retrospective analysis. Dev Psychol 42:643.
67. Nigam S, Shimono M, Ito S, Yeh F-C, Timme N, Myroshnychenko M, Lapish CC, Tosi Z, Hottowy P, Smith WC, Masmanidis SC, Litke AM, Sporns O, Beggs JM (2016): Rich-club organization in effective connectivity among cortical neurons. J Neurosci 36:670–684.
68. Okada K, Hickok G (2006): Left posterior auditory-related cortices participate both in speech perception and speech production: Neural overlap revealed by fMRI. Brain Lang 98:112–117.
69. Oztop E, Bradley NS, Arbib MA (2004): Infant grasp learning: A computational model. Exp Brain Res 158:480–503.
70. Perani D, Saccuman MC, Scifo P, Anwander A, Spada D, Baldoli C, Poloniato A, Lohmann G, Friederici AD (2011): Neural language networks at birth. Proc Natl Acad Sci 108:16056–16061.
71. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012): Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142–2154.
72. Price CJ, Devlin JT (2011): The interactive account of ventral occipitotemporal contributions to reading. Trends Cogn Sci 15:246–253.
73. Ptak R (2012): The frontoparietal attention network of the human brain action, saliency, and a priority map of the environment. Neuroscientist 18:502–515.
74. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001): A default mode of brain function. Proc Natl Acad Sci U S A 98:676–682.
75. Ramsay DS, Weber SL (1986): Infants' hand preference in a task involving complementary roles for the two hands. Child Dev 300–307.
76. Rushworth M, Behrens T, Johansen-Berg H (2006): Connection patterns distinguish 3 regions of human parietal cortex. Cereb Cortex 16:1418–1430.
77. Schipke CS, Kauschke C (2010): Early word formation in German language acquisition: A study on word formation growth during the second and third years. First Lang 14:195–211.
78. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD (2007): Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349–2356.
79. Sepulcre J (2014): Integration of visual and motor functional streams in the human brain. Neurosci Lett 567:68–73.
80. Sepulcre J (2015): An OP4 functional stream in the language-related neuroarchitecture. Cereb Cortex 25:658–666.
81. Sepulcre J, Sabuncu MR, Yeo TB, Liu H, Johnson KA (2012): Stepwise connectivity of the modal cortex reveals the multimodal organization of the human brain. J Neurosci 32:10649–10661.
82. Shaw KE, Bortfeld H (2015): Sources of confusion in infant audiovisual speech perception research. Front Psychol 6:1844.
83. Shi F, Yap P-T, Wu G, Jia H, Gilmore JH, Lin W, Shen D (2011): Infant brain atlases from neonates to 1-and 2-year-olds. PloS One 6:e18746.
84. Short SJ, Elison JT, Goldman BD, Styner M, Gu H, Connelly M, Maltbie E, Woolson S, Lin W, Gerig G (2013): Associations between white matter microstructure and infants' working memory. Neuroimage 64:156–166.
85. Spreng RN, Stevens WD, Chamberlain JP, Gilmore AW, Schacter DL (2010): Default network activity, coupled with the frontoparietal control network, supports goal-directed cognition. Neuroimage 53:303–317.
86. Thelen E, Corbetta D, Kamm K, Spencer JP, Schneider K, Zernicke RF (1993): The transition to reaching: Mapping intention and intrinsic dynamics. Child Dev 64:1058–1098.
87. Van Den Heuvel MP, Sporns O (2011): Rich-club organization of the human connectome. J Neurosci 31:15775–15786.
88. Von Hofsten C (1991): Structuring of early reaching movements: A longitudinal study. J Motor Behav 23:280–292.
89. Von Kriegstein K, Giraud A-L (2004): Distinct functional substrates along the right superior temporal sulcus for the processing of voices. Neuroimage 22:948–955.
90. Von Kriegstein K, Kleinschmidt A, Sterzer P, Giraud AL (2005): Interaction of face and voice areas during speaker recognition. J Cogn Neurosci 17:367–376.
91. Von Kriegstein K, Kleinschmidt A, Giraud AL (2006): Voice recognition and cross-modal responses to familiar speakers' voices in prosopagnosia. Cereb Cortex 16:1314–1322.
92. Vouloumanos A, Hauser MD, Werker JF, Martin A (2010): The tuning of human neonates' preference for speech. Child Dev 81:517–527.
93. Warlaumont AS, Westermann G, Buder EH, Oller DK (2013): Prespeech motor learning in a neural network using reinforcement. Neural Netw 38:64–75.
94. Yan CG, Craddock RC, Zuo XN, Zang YF, Milham MP (2013): Standardizing the intrinsic brain: Towards robust measurement of inter-individual variation in 1000 functional connectomes. Neuroimage 80:246–262.
95. Zamuner TS, Gerken L, Hammond M (2004): Phonotactic probabilities in young children's speech production. J Child Lang 31:515–536.