Neonatal White Matter Maturation Is Associated With Infant Language Development

Georgina M Sket, Judith Overfeld, Martin Styner, John H Gilmore, Sonja Entringer, Pathik D Wadhwa, Jerod M Rasmussen, Claudia Buss, Georgina M Sket, Judith Overfeld, Martin Styner, John H Gilmore, Sonja Entringer, Pathik D Wadhwa, Jerod M Rasmussen, Claudia Buss

Abstract

Background: While neonates have no sophisticated language skills, the neural basis for acquiring this function is assumed to already be present at birth. Receptive language is measurable by 6 months of age and meaningful speech production by 10-18 months of age. Fiber tracts supporting language processing include the corpus callosum (CC), which plays a key role in the hemispheric lateralization of language; the left arcuate fasciculus (AF), which is associated with syntactic processing; and the right AF, which plays a role in prosody and semantics. We examined if neonatal maturation of these fiber tracts is associated with receptive language development at 12 months of age.

Methods: Diffusion-weighted imaging (DWI) was performed in 86 infants at 26.6 ± 12.2 days post-birth. Receptive language was assessed via the MacArthur-Bates Communicative Development Inventory at 12 months of age. Tract-based fractional anisotropy (FA) was determined using the NA-MIC atlas-based fiber analysis toolkit. Associations between neonatal regional FA, adjusted for gestational age at birth and age at scan, and language development at 12 months of age were tested using ANOVA models.

Results: After multiple comparisons correction, higher neonatal FA was positively associated with receptive language at 12 months of age within the genu (p < 0.001), rostrum (p < 0.001), and tapetum (p < 0.001) of the CC and the left fronto-parietal AF (p = 0.008). No significant clusters were found in the right AF.

Conclusion: Microstructural development of the CC and the AF in the newborn is associated with receptive language at 12 months of age, demonstrating that interindividual variation in white matter microstructure is relevant for later language development, and indicating that the neural foundation for language processing is laid well ahead of the majority of language acquisition. This suggests that some origins of impaired language development may lie in the intrauterine and potentially neonatal period of life. Understanding how interindividual differences in neonatal brain maturity relate to the acquisition of function, particularly during early development when the brain is in an unparalleled window of plasticity, is key to identifying opportunities for harnessing neuroplasticity in health and disease.

Keywords: diffusion tensor imaging; infant language development; neonatal neuroimaging; receptive language development; white matter development.

Copyright © 2019 Sket, Overfeld, Styner, Gilmore, Entringer, Wadhwa, Rasmussen and Buss.

Figures

FIGURE 1
FIGURE 1
(A) Clusters within the genu, rostrum, and tapetum of the corpus callosum associated with MacArthur-Bates Communicative Development Inventory (MCDI)-Phrases Understood (PU) at 12 months of age controlling for gestational age at birth and age at scan, and PU at 12 months of age plotted against fractional anisotropy (FA) values (scalar values between 0 and 1, with 1 representing unidirectional movement) of the point with the highest p-value within clusters in the rostrum (B), tapetum (C), and genu (D) of the corpus callosum (CC) controlling for gestational age at birth and age at scan.
FIGURE 2
FIGURE 2
Cluster within the fronto-parietal region of the left arcuate fasciculus (AF) associated with MacArthur-Bates Communicative Development Inventory (MCDI)-PU at 12 months of age controlling for gestational age at birth and age at scan (A) and PU at 12 months of age plotted against neonatal FA values (scalar values between 0 and 1, with 1 representing unidirectional movement) of most significantly associated points within the cluster in the AF (B) controlling for gestational age at birth and age at scan.

References

    1. Alaghband-Rad J., McKenna K., Gordon C. T., Albus K. E., Hamburger S. D., Rumsey J. M., et al. (1995). Childhood-onset schizophrenia: the severity of premorbid course. J. Am. Acad. Child Adolesc. Psychiatr. 34 1273–1283. 10.1097/00004583-199510000-00012
    1. Arck P. C., Schepanski S., Buss C., Hanganu-Opatz I. (2018). Prenatal immune and endocrine modulators of offspring’s brain development and cognitive functions later in life. Front. Immunol. 9:2186.
    1. Astington J. W., Jenkins J. M. (1999). A longitudinal study of the relation between language and theory-of-mind development. Dev. Psychol. 35:1311. 10.1037/0012-1649.35.5.1311
    1. Azak S. (2012). Maternal depression and sex differences shape the infants’ trajectories of cognitive development. Infant Behav. Dev. 35 803–814. 10.1016/j.infbeh.2012.07.017
    1. Benasich A. A., Curtiss S., Tallal P. (1993). Language, learning, and behavioral disturbances in childhood: a longitudinal perspective. J. Am. Acad. Child Adolesc. Psychiatr. 32 585–594. 10.1097/00004583-199305000-00015
    1. Bloom J. S., Hynd G. W. (2005). The role of the corpus callosum in interhemispheric transfer of information: excitation or inhibition? Neuropsychol. Rev. 15 59–71. 10.1007/s11065-005-6252-y
    1. Brody B. A., Kinney H. C., Kloman A. S., Gilles F. H. (1987). Sequence of central nervous system myelination in human infancy. I. An autopsy study of myelination. J. Neuropathol. Exp. Neurol. 46 283–301. 10.1097/00005072-198705000-00005
    1. Caldwell B. M., Bradley R. H. (1984). Home Observation for Measurement of the Environment. Little Rock: University of Arkansas at Little Rock.
    1. Catani M., De Schotten M. T. (2008). A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44 1105–1132. 10.1016/j.cortex.2008.05.004
    1. Charman T., Drew A., Baird C., Baird G. (2003). Measuring early language development in preschool children with autism spectrum disorder using the MacArthur communicative development inventory (Infant Form). J. Child Lang. 30 213–236. 10.1017/s0305000902005482
    1. Cheng Q., Halgren E., Mayberry R. (2018). “Effects of early language deprivation: Mapping between brain and behavioral outcomes,” in Proceedings of the 42nd Annual Boston University Conference on Language Development, (Somerville, MA: Cascadilla Press; ).
    1. Crump K. S., Kjellström T., Shipp A. M., Silvers A., Stewart A. (1998). Influence of prenatal mercury exposure upon scholastic and psychological test performance: benchmark analysis of a New Zealand cohort. Risk Analysis 18 701–713. 10.1023/b:rian.0000005917.52151.e6
    1. Donahue M. (1986). Linguistic and communicative development in learning disabled children. Handb. Cogn. Soc. Neuropsychol. Aspects Learn. Disabil. 1 263–289.
    1. Douet V., Chang L. (2015). Fornix as an imaging marker for episodic memory deficits in healthy aging and in various neurological disorders. Front. Aging Neurosci. 6:343. 10.3389/fnagi.2014.00343
    1. Dubois J., Dehaene-Lambertz G., Kulikova S., Poupon C., Hüppi P. S., Hertz-Pannier L. (2014). The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience 276 48–71. 10.1016/j.neuroscience.2013.12.044
    1. 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. 10.1002/hbm.20363
    1. Fenson L., Marchman V. A., Thal D., Dale P. S., Reznick J. S. (2007). The MacArthur–Bates Communicative Development Inventories: User’s Guide and Technical Manual. Baltimore, MD: Brooks.
    1. Geng X., Gouttard S., Sharma A., Gu H., Styner M., Lin W., et al. (2012). Quantitative tract-based white matter development from birth to age 2years. Neuroimage 61 542–557. 10.1016/j.neuroimage.2012.03.057
    1. Girault J. B., Cornea E., Goldman B. D., Knickmeyer R. C., Styner M., Gilmore J. H. (2019). White matter microstructural development and cognitive ability in the first 2 years of life. Hum. Brain Mapp. 40 1195–1210. 10.1002/hbm.24439
    1. Graham A. M., Rasmussen J. M., Rudolph M. D., Heim C. M., Gilmore J. H., Styner M., et al. (2018). Maternal systemic interleukin-6 during pregnancy is associated with newborn amygdala phenotypes and subsequent behavior a1t 2 years of age. Biol. Psychiatry 83 109–119. 10.1016/j.biopsych.2017.05.027
    1. Greene T., Emhart C. B., Martier S., Sokol R., Ager J. (1990). Prenatal alcohol exposure and language development. Alcohol Clin. Exp. Res. 14 937–945. 10.1111/j.1530-0277.1990.tb01842.x
    1. Joshi S., Davis B., Jomier M., Gerig G. (2004). Unbiased diffeomorphic atlas construction for computational anatomy. Neuroimage 23 S151–S160.
    1. Lebel C., Beaulieu C. (2009). Lateralization of the arcuate fasciculus from childhood to adulthood and its relation to cognitive abilities in children. Hum. Brain Mapp. 30 3563–3573. 10.1002/hbm.20779
    1. Liu Z., Wang Y., Gerig G., Gouttard S., Tao R., Fletcher T., et al. (2010). Quality control of diffusion weighted images. Proc. SPIE Int. Soc. Opt. Eng. 7628:76280J. 10.1117/12.844748
    1. Locke J. L. (1997). A theory of neurolinguistic development. Brain Lang. 58 265–326. 10.1006/brln.1997.1791
    1. Fensen L., Dale P., Reznick S. (1993). MacArthur-Bates Communicative Development Inventory. Baltimore, MD: Paul H.
    1. Heim C., Entringer S., Buss C. (2018). Translating basic research knowledge on the biological embedding of early-life stress into novel approaches for the developmental programming of lifelong health. Psychoneuroendocrinology 105 123–137. 10.1016/j.psyneuen.2018.12.011
    1. Hinkley L. B., Marco E. J., Brown E. G., Bukshpun P., Gold J., Hill S., et al. (2016). The contribution of the corpus callosum to language lateralization. J. Neurosci. 36 4522–4533. 10.1523/JNEUROSCI.3850-14.2016
    1. Huttenlocher J., Haight W., Bryk A., Seltzer M., Lyons T. (1991). Early vocabulary growth: relation to language input and gender. Dev. Psychol. 27:236. 10.1044/1092-4388(2010/09-0216)
    1. Kaplan P. S., Danko C. M., Everhart K. D., Diaz A., Asherin R. M., Vogeli J. M., et al. (2014). Maternal depression and expressive communication in one-year-old infants. Infant Behav. Dev. 37 398–405. 10.1016/j.infbeh.2014.05.008
    1. Kuhl P. K., Conboy B. T., Padden D., Nelson T., Pruitt J. (2005). Early speech perception and later language development: implications for the critical period. Lang. Learn. Dev. 1 237–264. 10.1080/15475441.2005.9671948
    1. Langer N., Peysakhovich B., Zuk J., Drottar M., Sliva D. D., Smith S., et al. (2017). White matter alterations in infants at risk for developmental dyslexia. Cereb. Cortex 27 1027–1036. 10.1093/cercor/bhv281
    1. Laplante D. P., Barr R. G., Brunet A., Du Fort G. G., Meaney M. L., Saucier J. F., et al. (2004). Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatr. Res. 56:400. 10.1203/01.pdr.0000136281.34035.44
    1. Lewis B. A., Minnes S., Short E. J., Weishampel P., Satayathum S., Min M. O., et al. (2011). The effects of prenatal cocaine on language development at 10 years of age. Neurotoxicol. Teratol. 33 17–24.
    1. Luders E., Thompson P. M., Toga A. W. (2010). The development of the corpus callosum in the healthy human brain. J. Neurosci. 30 10985–10990. 10.1523/JNEUROSCI.5122-09.2010
    1. Mahmoudzadeh M., Dehaene-Lambertz G., Fournier M., Kongolo G., Goudjil S., Dubois J., et al. (2013). Syllabic discrimination in premature human infants prior to complete formation of cortical layers. Proc. Natl. Acad. Sci. U.S.A. 110 4846–4851. 10.1073/pnas.1212220110
    1. Matthews M., Fair D. A. (2015). Research review: functional brain connectivity and child psychopathology–overview and methodological considerations for investigators new to the field. J. Child Psychol. Psychiatr. 56 400–414. 10.1111/jcpp.12335
    1. McGrath J. M., Records K., Rice M. (2008). Maternal depression and infant temperament characteristics. Infant Behav. Dev. 31 71–80. 10.1016/j.infbeh.2007.07.001
    1. Mitchell S., Brian J., Zwaigenbaum L., Roberts W., Szatmari P., Smith I., et al. (2006). Early language and communication development of infants later diagnosed with autism spectrum disorder. J. Dev. Behav. Pediatr. 27 S69–S78.
    1. Moog N. K., Entringer S., Heim C., Wadhwa P. D., Kathmann N., Buss C. (2017). Influence of maternal thyroid hormones during gestation on fetal brain development. Neuroscience 342 68–100. 10.1016/j.neuroscience.2015.09.070
    1. Morrow C. E., Bandstra E. S., Anthony J. C., Ofir A. Y., Xue L., Reyes M. B. (2003). Influence of prenatal cocaine exposure on early language development: longitudinal findings from four months to three years of age. J. Dev. Behav. Pediatr. 24 39–50. 10.1097/00004703-200302000-00009
    1. Oguz I., Farzinfar M., Matsui J., Budin F., Liu Z., Gerig G., et al. (2014). DTIPrep: quality control of diffusion-weighted images. Front. Neuroinform. 2014:4.
    1. O’Muircheartaigh J., Dean D. C., Dirks H., Waskiewicz N., Lehman K., Jerskey B. A., et al. (2013). Interactions between white matter asymmetry and language during neurodevelopment. J. Neurosci. 33 16170–16177. 10.1523/JNEUROSCI.1463-13.2013
    1. Peters B. D., Ikuta T., DeRosse P., John M., Burdick K. E., Gruner P., et al. (2014). Age-related differences in white matter tract microstructure are associated with cognitive performance from childhood to adulthood. Biol. Psychiatry 75 248–256. 10.1016/j.biopsych.2013.05.020
    1. Pineda R. G., Neil J., Dierker D., Smyser C. D., Wallendorf M., Kidokoro H., et al. (2014). Alterations in brain structure and neurodevelopmental outcome in preterm infants hospitalized in different neonatal intensive care unit environments. J. Pediatr. 164 52–60. 10.1016/j.jpeds.2013.08.047
    1. Pujol J., Soriano-Mas C., Ortiz H., Sebastian-Galles N., Losilla J. M., Deus J. (2006). Myelination of language-related areas in the developing brain. Neurology 66 339–343. 10.1212/01.wnl.0000201049.66073.8d
    1. Qiu A., Mori S., Miller M. I. (2015). Diffusion tensor imaging for understanding brain development in early life. Annu. Rev. Psychol. 66 853–876. 10.1146/annurev-psych-010814-015340
    1. Radloff L. S. (1977). The CES-D scale: a self-report depression scale for research in the general population. Appl. Psychol. Meas. 1 385–401. 10.1177/014662167700100306
    1. Rasmussen J. M., Graham A. M., Entringer S., Gilmore J. H., Styner M., Fair D. A., et al. (2018). Maternal interleukin-6 concentration during pregnancy is associated with variation in frontolimbic white matter and cognitive development in early life. Neuroimage 185 825–835. 10.1016/j.neuroimage.2018.04.020
    1. Rasmussen J. M., Kruggel F., Gilmore J. H., Styner M., Entringer S., Consing K. N., et al. (2017). A novel maturation index based on neonatal diffusion tensor imaging reflects typical perinatal white matter development in humans. Int. J. Dev. Neurosci. 56 42–51. 10.1016/j.ijdevneu.2016.12.004
    1. Rose J., Butler E. E., Lamont L. E., Barnes P. D., Atlas S. W., Stevenson D. K. (2009). Neonatal brain structure on MRI and diffusion tensor imaging, sex, and neurodevelopment in very-low-birthweight preterm children. Dev. Med. Child Neurol. 51 526–535. 10.1111/j.1469-8749.2008.03231.x
    1. Rudolph M. D., Graham A. M., Feczko E., Miranda-Dominguez O., Rasmussen J. M., Nardos R., et al. (2018). Maternal IL-6 during pregnancy can be estimated from newborn brain connectivity and predicts future working memory in offspring. Nat. Neurosci. 21 765–772. 10.1038/s41593-018-0128-y
    1. Shapiro B. K., Palmer F. B., Antell S., Bilker S., Ross A., Capute A. J. (1990). Precursors of reading delay: neurodevelopmental milestones. Pediatrics 85 416–420.
    1. Short S. J., Elison J. T., Goldman B. D., Styner M., Gu H., Connelly M., et al. (2013). Associations between white matter microstructure and infants’ working memory. Neuroimage 64 156–166. 10.1016/j.neuroimage.2012.09.021
    1. Skeide M. A., Brauer J., Friederici A. D. (2015). Brain functional and structural predictors of language performance. Cereb. Cortex 26 2127–2139. 10.1093/cercor/bhv042
    1. Stjerna S., Sairanen V., Gröhn R., Andersson S., Metsäranta M., Lano A., et al. (2015). Visual fixation in human newborns correlates with extensive white matter networks and predicts long-term neurocognitive development. J. Neurosci. 35 4824–4829. 10.1523/JNEUROSCI.5162-14.2015
    1. Stoel-Gammon C. (1992). “Research on phonological development: recent advances,” in Phonological Development: Models, Research, Implications, eds Ferguson C., Menn L., Stoel-Gammon C. (Timonium, MD: York Press; ), 273–281.
    1. Szeszko P. R., Vogel J., Ashtari M., Malhotra A. K., Bates J., Kane J. M., et al. (2003). Sex differences in frontal lobe white matter microstructure: a DTI study. Neuroreport 14 2469–2473. 10.1097/00001756-200312190-00035
    1. Thomason M. E., Thompson P. M. (2011). Diffusion imaging, white matter, and psychopathology. Clin. Psychol. 7:63. 10.1146/annurev-clinpsy-032210-104507
    1. Torppa M., Lyytinen P., Erskine J., Eklund K., Lyytinen H. (2010). Language development, literacy skills, and predictive connections to reading in finnish children with and without familial risk for dyslexia. J. Learn. Disabil. 43 308–321. 10.1177/0022219410369096
    1. Totsika V., Sylva K. (2004). The home observation for measurement of the environment revisited. Child Adolesc. Ment. Health 9 25–35. 10.1046/j.1475-357x.2003.00073.x
    1. Tsao F. M., Liu H. M., Kuhl P. K. (2004). Speech perception in infancy predicts language development in the second year of life: a longitudinal study. Child Dev. 75 1067–1084. 10.1111/j.1467-8624.2004.00726.x
    1. van Kooij B. J., de Vries L. S., Ball G., van Haastert I. C., Benders M. J., Groenendaal F., et al. (2012). Neonatal tract-based spatial statistics findings and outcome in preterm infants. Am. J. Neuroradiol. 33 188–194. 10.3174/ajnr.a2723
    1. Verde A. R., Budin F., Berger J. B., Gupta A., Farzinfar M., Kaiser A., et al. (2014). UNC-Utah NA-MIC framework for DTI fiber tract analysis. Front. Neuroinform. 7:51. 10.3389/fninf.2013.00051
    1. Wechsler D. (1955). Wechsler adult intelligence scale (WAIS). J. Consult. Psychol. 19 319–320. 10.1037/h0039221
    1. Westerhausen R., Kreuder F., Sequeira S. D. S., Walter C., Woerner W., Wittling R. A., et al. (2004). Effects of handedness and gender on macro- and microstructure of the corpus callosum and its subregions: a combined high-resolution and diffusion-tensor MRI study. Cogn. Brain Res. 21 418–426. 10.1016/j.cogbrainres.2004.07.002
    1. Wolff J. J., Gu H., Gerig G., Elison J. T., Styner M., Gouttard S., et al. (2012). Differences in white matter fiber tract development present from 6 to 24 months in infants with autism. Am. J. Psychiatr. 169 589–600. 10.1176/appi.ajp.2011.11091447
    1. Wong H. S., Edwards P. (2013). Nature or nurture: a systematic review of the effect of socio-economic status on the developmental and cognitive outcomes of children born preterm. Matern. Child Health J. 17 1689–1700. 10.1007/s10995-012-1183-8
    1. Yakovlev P. I., Lecours A. R. (1967). “The myelogenetic cycles of regional maturation of the brain,” in Regional Development of the Brain in Early Life, ed. Minkowski A. (Oxford: Blackwell; ), 3–70.

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