Longitudinal study of the emerging functional connectivity asymmetry of primary language regions during infancy

Journal of Neuroscience

Volumn 36, Issue 42, 2016, Pages 10883-10892

  Emerson, Robert W ^a   Gao, Wei ^a,b   Lin, Weili ^a  

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

^b CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

Cognitive development; Functional asymmetry; Functional connectivity; Infancy; Language network

Indexed keywords

AGE; ALGORITHM; ARTICLE; BRAIN ASYMMETRY; CONTROLLED STUDY; DORSOLATERAL PREFRONTAL CORTEX; FEMALE; HUMAN; HUMAN EXPERIMENT; INFANCY; INFANT; INFERIOR FRONTAL GYRUS; INTRAPARIETAL SULCUS; LANGUAGE; MALE; NERVE CELL NETWORK; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; SCORING SYSTEM; STATISTICAL MODEL; SUPERIOR TEMPORAL GYRUS; WHITE MATTER; WORKING MEMORY; CHILD DEVELOPMENT; COGNITION; GROWTH, DEVELOPMENT AND AGING; HEMISPHERIC DOMINANCE; IMAGE PROCESSING; LANGUAGE DEVELOPMENT; LONGITUDINAL STUDY; NERVE TRACT; NEWBORN; PHYSIOLOGY; PREFRONTAL CORTEX; SOMATOSENSORY CORTEX; TEMPORAL LOBE; VISUAL CORTEX;

CHILD DEVELOPMENT; COGNITION; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INFANT; INFANT, NEWBORN; LANGUAGE DEVELOPMENT; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; NEURAL PATHWAYS; PREFRONTAL CORTEX; SOMATOSENSORY CORTEX; TEMPORAL LOBE; VISUAL CORTEX;

EID: 84991764815     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3980-15.2016     Document Type: Article

References (61)

1. 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.
2. Barbey AK, Koenigs M, Grafman J (2013) Dorsolateral prefrontal contributions to human working memory. Cortex 49:1195–1205.
3. Binder JR, Frost JA, Hammeke TA, Bellgowan PS, Springer JA, Kaufman JN, Possing ET (2000) Human temporal lobe activation by speech and nonspeech sounds. Cereb Cortex 10:512–528.
4. Brauer J, Anwander A, Friederici AD (2011) Neuroanatomical prerequisites for language functions in the maturing brain. Cereb Cortex 21:459–466.
5. Brody BA, Kinney HC, Kloman AS, Gilles FH (1987) Sequence of central nervous system myelination in human infancy. I. An autopsy study of myelination. J Neuropathol Exp Neurol 46:283–301.
6. Burkhalter A (1993) Development of forward and feedback connections between areas V1 and V2 of human visual cortex. Cereb Cortex 3:476–487.
7. Crow TJ, Ball J, Bloom SR, Brown R, Bruton CJ, Colter N, Frith CD, John-stone EC, Owens DG, Roberts GW (1989) Schizophrenia as an anomaly of development of cerebral asymmetry: a postmortem study and a proposal concerning the genetic basis of the disease. Arch Gen Psychiatry 46:1145–1150.
8. Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A 103:13848–13853.
9. deAzevedo LC, Hedin-Pereira C, Lent R (1997) Callosal neurons in the cin-gulate cortical plate and subplate of human fetuses. J Comp Neurol 386: 60–70.
10. Dehaene-Lambertz G, Dehaene S, Hertz-Pannier L (2002) Functional neuroimaging of speech perception in infants. Science 298:2013–2015.
11. Dehaene-Lambertz G, Montavont A, Jobert A, Allirol L, Dubois J, Hertz-Pannier L, Dehaene S (2010) Language or music, mother or Mozart? Structural and environmental influences on infants’ language networks. Brain Lang 114:53–65.
12. Doria V, Beckmann CF, Arichi T, Merchant N, Groppo M, Turkheimer FE, Counsell SJ, Murgasova M, Aljabar P, Nunes RG, Larkman DJ, Rees G, Edwards AD (2010) Emergence of resting state networks in the preterm human brain. Proc Natl Acad Sci U S A 107:20015–20020.
13. Dubois J, Benders M, Lazeyras F, Borradori-Tolsa C, Leuchter RH, Mangin JF, Hüppi PS (2010) Structural asymmetries of perisylvian regions in the preterm newborn. Neuroimage 52:32–42.
14. Emerson RW, Cantlon JF (2012) Early math achievement and functional connectivity in the fronto-parietal network. Dev Cogn Neurosci 2:S139– S151.
15. Fransson P, Skiöld B, Engström M, Hallberg B, Mosskin M, Aden U, Lager-crantz H, Blennow M (2009) Spontaneous brain activity in the newborn brain during natural sleep—an fMRI study in infants born at full term. Pediatr Res 66:301–305.
16. Friederici AD (2009) Pathways to language: fiber tracts in the human brain. Trends Cogn Sci 13:175–181.
17. Friederici AD, Alter K (2004) Lateralization of auditory language functions: a dynamic dual pathway model. Brain Lang 89:267–276.
18. 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.
19. 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.
20. Gao W, Gilmore JH, Giovanello KS, Smith JK, Shen D, Zhu H, Lin W (2011) Temporal and spatial evolution of brain network topology during the first two years of life. PloS One 6:e25278.
21. 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.
22. Gao W, Alcauter S, Smith JK, Gilmore JH, Lin W (2015a) Development of human brain cortical network architecture during infancy. Brain Struct Funct 220:1173–1186.
23. Gao W, Alcauter S, Elton A, Hernandez-Castillo CR, Smith JK, Ramirez J, Lin W (2015b) Functional network development during the first year: relative sequence and socioeconomic correlations. Cereb Cortex 25:2919– 2928.
24. Gao W, Lin W, Grewen K, Gilmore JH (2016) Functional connectivity of the infant human brain: plastic and modifiable. Neuroscientist pii: 1073858416635986.
25. Geng X, Gouttard S, Sharma A, Gu H, Styner M, Lin W, Gerig G, Gilmore JH (2012) Quantitative tract-based white matter development from birth to age 2 years. Neuroimage 61:542–557.
26. Hallquist MN, Hwang K, Luna B (2013) The nuisance of nuisance regression: spectral misspecification in a common approach to resting-state fMRI preprocessing reintroduces noise and obscures functional connectivity. Neuroimage 82:208–225.
27. Herbert MR, Harris GJ, Adrien KT, Ziegler DA, Makris N, Kennedy DN, Lange NT, Chabris CF, Bakardjiev A, Hodgson J, Takeoka M, Tager-Flusberg H, Caviness VS Jr (2002) Abnormal asymmetry in language association cortex in autism. Ann Neurol 52:588–596.
28. Hevner RF (2000) Development of connections in the human visual system during fetal mid-gestation: a DiItracing study. J Neuropathol Exp Neurol 59:385–392.
29. Jo HJ, Gotts SJ, Reynolds RC, Bandettini PA, Martin A, Cox RW, Saad ZS (2013) Effective preprocessing procedures virtually eliminate distance-dependent motion artifacts in resting state fMRI. J Appl Math 2013.
30. Johnson PC (2014) Extension of Nakagawa and Schielzeth’s R2GLMM to random slopes models. Methods Ecol Evol 5:944–946.
31. Kinney HC, Brody BA, Kloman AS, Gilles FH (1988) Sequence of central nervous system myelination in human infancy. II. Patterns of myelination in autopsied infants. J Neuropathol Exp Neurol 47:217–234.
32. Kleinhans NM, Müller RA, Cohen DN, Courchesne E (2008) Atypical functional lateralization of language in autism spectrum. Brain Res 1221:115– 125.
33. Kostović I, Judas M, Petanjek Z, Simić G (1995) Ontogenesis of goal-directed behavior: anatomo-functional considerations. Int J Psychophysiol 19:85–102.
34. Li G, Nie J, Wang L, Shi F, Lyall AE, Lin W, Gilmore JH, Shen D (2014) Mapping longitudinal hemispheric structural asymmetries of the human cerebral cortex from birth to 2 years of age. Cereb Cortex 24:1289–1300.
35. Lohmann G, Hoehl S, Brauer J, Danielmeier C, Bornkessel-Schlesewsky I, Bahlmann J, Turner R, Friederici A (2010) Setting the frame: the human brain activates a basic low-frequency network for language processing. Cereb Cortex 20:1286–1292.
36. May L, Byers-Heinlein K, Gervain J, Werker JF (2011) Language and the newborn brain: does prenatal language experience shape the neonate neural response to speech? Front Psychol 2:222.
37. Minagawa-Kawai Y, van der Lely H, Ramus F, Sato Y, Mazuka R, Dupoux E (2011) Optical brain imaging reveals general auditory and language-specific processing in early infant development. Cereb Cortex 21:254– 261.
38. Mullen EM (1995) Mullen scales of early learning. Circle Pines, MN: AGS.
39. Muschelli J, Nebel MB, Caffo BS, Barber AD, Pekar JJ, Mostofsky SH (2014) Reduction of motion-related artifacts in resting state fMRI using aComp-Cor. Neuroimage 96:22–35.
40. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142.
41. Nielsen JA, Zielinski BA, Ferguson MA, Lainhart JE, Anderson JS (2013) An evaluation of the left-brain vs. right-brain hypothesis with resting state functional connectivity magnetic resonance imaging. PloS One 8:e71275.
42. Patel AX, Kundu P, Rubinov M, Jones PS, Vértes PE, Ersche KD, Suckling J, Bullmore ET (2014) A wavelet method for modeling and despiking motion artifacts from resting-state fMRI time series. Neuroimage 95:287– 304.
43. Peña M, Maki A, Kovacić D, Dehaene-Lambertz G, Koizumi H, Bouquet F, Mehler J (2003) Sounds and silence: an optical topography study of language recognition at birth. Proc Natl Acad Sci U S A 100:11702–11705.
44. Perani D, Saccuman MC, Scifo P, Anwander A, Awander A, Spada D, Baldoli C, Poloniato A, Lohmann G, Friederici AD (2011) Neural language networks at birth. Proc Natl Acad Sci U S A 108:16056–16061.
45. Pinheiro J, Bates D, DebRoy S, Sarkar D (2007) Linear and nonlinear mixed effects models. R package version 3:57.
46. 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.
47. Power JD, Mitra A, Laumann TO, Snyder AZ, Schlaggar BL, Petersen SE (2014) Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage 84:320–341.
48. Power JD, Schlaggar BL, Petersen SE (2015) Recent progress and outstanding issues in motion correction in resting state fMRI. Neuroimage 105: 536–551.
49. Sato H, Hirabayashi Y, Tsubokura H, Kanai M, Ashida T, Konishi I, Uchida-Ota M, Konishi Y, Maki A (2012) Cerebral hemodynamics in newborn infants exposed to speech sounds: a whole-head optical topography study. Hum Brain Mapp 33:2092–2103.
50. Shen D, Davatzikos C (2002) HAMMER: hierarchical attribute matching mechanism for elastic registration. IEEE Trans Med Imaging 21:1421– 1439.
51. Shen D, Davatzikos C (2004) Measuring temporal morphological changes robustly in brain MR images via 4-dimensional template warping. Neuroimage 21:1508–1517.
52. Shultz S, Vouloumanos A, Bennett RH, Pelphrey K (2014) Neural specialization for speech in the first months of life. Dev Sci 17:766–774.
53. Slater R, Cantarella A, Gallella S, Worley A, Boyd S, Meek J, Fitzgerald M (2006) Cortical pain responses in human infants. J Neurosci 26:3662– 3666.
54. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:S208–S219.
55. Sommer IE, Ramsey NF, Kahn RS (2001) Language lateralization in schizophrenia, an fMRI study. Schizophr Res 52:57–67.
56. Stark DE, Margulies DS, Shehzad ZE, Reiss P, Kelly AM, Uddin LQ, Gee DG, Roy AK, Banich MT, Castellanos FX, Milham MP (2008) Regional vari- ation in interhemispheric coordination of intrinsic hemodynamic fluctuations. J Neurosci 28:13754–13764.
57. Thomason ME, Dassanayake MT, Shen S, Katkuri Y, Alexis M, Anderson AL, Yeo L, Mody S, Hernandez-Andrade E, Hassan SS, Studholme C, Jeong JW, Romero R (2013) Cross-hemispheric functional connectivity in the human fetal brain. Sci Transl Med 5:173ra24.
58. Toga AW, Thompson PM (2003) Mapping brain asymmetry. Nat Rev Neurosci 4:37–48.
59. van den Heuvel M, Mandl R, Hulshoff Pol H (2008) Normalized cut group clustering of resting-state FMRI data. PloS One 3:e2001.
60. van den Heuvel MP, Kersbergen KJ, de Reus MA, Keunen K, Kahn RS, Groenendaal F, de Vries LS, Benders MJ (2015) The neonatal connec-tome during preterm brain development. Cereb Cortex 25:3000–3013.
61. Zuo XN, Kelly C, Di Martino A, Mennes M, Margulies DS, Bangaru S, Grzadzinski R, Evans AC, Zang YF, Castellanos FX, Milham MP (2010) Growing together and growing apart: regional and sex differences in the lifespan developmental trajectories of functional homotopy. J Neurosci 30:15034–15043.