Longitudinal growth of the basal ganglia and thalamus in very preterm children
- 43 Downloads
The impact of very preterm (VP) birth on the development of individual basal ganglia nuclei and the thalamus during childhood remains unclear. We first aimed to compare (1a) the volumes of individual basal ganglia nuclei (nucleus accumbens, caudate nucleus, pallidum, putamen) and the thalamus at age 7 years, and (1b) their volumetric change from infancy to 7 years, in VP children with term-born children. Secondly, we aimed to (2a) determine whether basal ganglia and thalamic volumes at 7 years, or (2b) basal ganglia and thalamic growth rates from infancy to 7 years were associated with neurodevelopmental outcomes at 7 years, and whether these associations differed between the VP and term-born children. One hundred and fifty-four VP (<30 weeks’ gestational age or birth weight < 1250 g) and 35 term-born children had useable magnetic resonance imaging (MRI) scans that could be analyzed at 7 years. Of these, 149 VP and 30 term-born infants also had useable MRI scans at term-equivalent age. Volumes of the individual basal ganglia nuclei and the thalamus were automatically generated from the MRI scans. Compared with the term-born group, the VP group had smaller basal ganglia and thalamic volumes at 7 years and slower growth rates from birth to 7 years. After controlling for overall brain size, VP children still had smaller thalamic volumes but the deep grey matter volume growth rates from birth to 7 years were similar between groups. Reduced basal ganglia and thalamic volumes and slower growth rates in the VP group were associated with poorer cognition, academic achievement and motor function at 7 years. After controlling for overall brain size, the nucleus accumbens and pallidum were the deep grey matter structures most strongly associated with 7-year neurodevelopmental outcomes. In conclusion, basal ganglia and thalamic growth is delayed during early childhood in VP children, with delayed development contributing to poorer functional outcomes.
KeywordsVery preterm Basal ganglia Thalamus Neurodevelopment
Caudate nucleus/Nucleus accumbens complex
Movement Assessment Battery for Children-2
Morphologically Adaptive Neonatal Tissue Segmentation
Magnetic Resonance Imaging
Pediatric Subcortical Segmentation Technique
Strengths and Difficulties Questionnaire
Total Brain Volume
Victorian Infant Brain Studies
We are grateful for the help and support of the Victorian Infant Brain Studies (VIBeS) and Developmental Imaging groups, as well as the Melbourne Children’s MRI Centre at the Murdoch Childrens Research institute. We also thank the families and children who participated in this study.
This study was supported by Australia’s National Health & Medical Research Council: Centre for Clinical Research Excellence 546519 (L.W.D. and P.J.A.); Centre for Research Excellence 1060733 (L.W.D., P.J.A., J.L.Y.C., D.K.T., A.J.S. and W.Y.L.); Project Grant 491209 (P.J.A., L.W.D., T.E.I. and J.L.Y.C.; Senior Research Fellowship 628371 & 1081288 (P.J.A.); Career Development Fellowships 1108714 (A.J.S.), 1085754 (D.K.T.), 1053609 to (K.J.L.); Early Career Fellowship 1053787 (J.L.Y.C.). This study was also supported by the National Institutes of Health (HD058056), the Victorian Government’s Operational Infrastructure Support Program, and The Royal Children’s Hospital Foundation.
Compliance with ethical standards
Conflict of interest
Wai Yen Loh, Peter J Anderson, Jeanie LY Cheong, Alicia J Spittle, Jian Chen, Katherine J Lee, Charlotte Molesworth, Terrie E Inder, Alan Connelly, Lex W Doyle and Deanne K Thompson declare that they have no conflict of interest.
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent was obtained from all individual participants included in the study.
- Boardman, J. P., Counsell, S. J., Rueckert, D., Kapellou, O., Bhatia, K. K., Aljabar, P., et al. (2006). Abnormal deep grey matter development following preterm birth detected using deformation-based morphometry. Neuroimage, 32(1), 70–78. https://doi.org/10.1016/j.neuroimage.2006.03.029.CrossRefGoogle Scholar
- Draganski, B., Kherif, F., Klöppel, S., Cook, P. A., Alexander, D. C., Parker, G. J. M., et al. (2008). Evidence for Segregated and Integrative Connectivity Patterns in the Human Basal Ganglia. Journal of Neuroscience, 28(28), 7143–7152. https://doi.org/10.1523/jneurosci.1486-08.2008.CrossRefGoogle Scholar
- Fischi-Gomez, E., Vasung, L., Meskaldji, D. E., Lazeyras, F., Borradori-Tolsa, C., Hagmann, P., et al. (2015). Structural Brain Connectivity in School-Age Preterm Infants Provides Evidence for Impaired Networks Relevant for Higher Order Cognitive Skills and Social Cognition. Cerebral Cortex, 25(9), 2793–2805. https://doi.org/10.1093/cercor/bhu073.CrossRefGoogle Scholar
- Henderson, S. E., Sugden, D. A., & Barnett, A. L. (2007). Movement Assessment Battery for Children - second edition (Movement ABC-2). London: The Psychological Corporation.Google Scholar
- Hoon, A. H., Jr., Stashinko, E. E., Nagae, L. M., Lin, D. D. M., Keller, J., Bastian, A., et al. (2009). Sensory and motor deficits in children with cerebral palsy born preterm correlate with diffusion tensor imaging abnormalities in thalamocortical pathways. Developmental Medicine and Child Neurology, 51(9), 697–704, https://doi.org/10.1111/j.1469-8749.2009.03306.x.
- Kesler, S. R., Ment, L. R., Vohr, B., Pajot, S. K., Schneider, K. C., Katz, K. H., et al. (2004). Volumetric analysis of regional cerebral development in preterm children. Pediatric Neurology, 31(5), 318–325. https://doi.org/10.1016/j.pediatrneurol.2004.06.008.CrossRefGoogle Scholar
- Ligam, P., Haynes, R. L., Folkerth, R. D., Liu, L., Yang, M., Volpe, J. J., et al. (2009). Thalamic damage in periventricular leukomalacia: Novel pathologic observations relevant to cognitive deficits in survivors of prematurity. Pediatric Research, 65(5), 524–529. https://doi.org/10.1203/PDR.0b013e3181998baf.CrossRefGoogle Scholar
- Lin, Y., Okumura, A., Hayakawa, F., Kato, T., Kuno, K., & Watanabe, K. (2001). Quantitative evaluation of thalami and basal ganglia in infants with periventricular leukomalacia. Developmental Medicine and Child Neurology, 43(7), 481–485. https://doi.org/10.1111/j.1469-8749.2001.tb00747.x.CrossRefGoogle Scholar
- Loh, W. Y., Anderson, P. J., Cheong, J. L. Y., Spittle, A. J., Chen, J., Lee, K. J., et al. (2017). Neonatal basal ganglia and thalamic volumes: Very preterm birth and 7-year neurodevelopmental outcomes. Pediatric Research. https://doi.org/10.1038/pr.2017.161.
- Manly, T., Anderson, V., Nimmo-Smith, I., Turner, A., Watson, P., & Robertson, I. H. (2001). The differential assessment of children's attention: The test of everyday attention for children (TEA-Ch), normative sample and ADHD performance. Journal of Child Psychology and Psychiatry and Allied Disciplines, 42(8), 1065–1081.CrossRefGoogle Scholar
- Monson, B. B., Anderson, P. J., Matthews, L. G., Neil, J. J., Kapur, K., Cheong, J. L., et al. (2016). Examination of the pattern of growth of cerebral tissue volumes from hospital discharge to early childhood in very preterm infants. JAMA Pediatrics, 170(8), 772–779. https://doi.org/10.1001/jamapediatrics.2016.0781.CrossRefGoogle Scholar
- Narvacan, K., Treit, S., Camicioli, R., Martin, W., & Beaulieu, C. (2017). Evolution of deep gray matter volume across the human lifespan. Human Brain Mapping. https://doi.org/10.1002/hbm.23604.
- Nelson, A. B., & Kreitzer, A. C. (2014). Reassessing models of basal ganglia function and dysfunction. Annual Review of Neuroscience, 37(1), 117–135. https://doi.org/10.1146/annurev-neuro-071013-013916.CrossRefGoogle Scholar
- Pickering, S., & Gathercole, S. (2001). Working memory test battery for children-manual. London: The Psychological Corporation.Google Scholar
- Pietschnig, J., Penke, L., Wicherts, J. M., Zeiler, M., & Voracek, M. (2015). Meta-analysis of associations between human brain volume and intelligence differences: How strong are they and what do they mean? Neuroscience and Biobehavioral Reviews, 57, 411–432. https://doi.org/10.1016/j.neubiorev.2015.09.017.CrossRefGoogle Scholar
- Qiu, A., Crocetti, D., Adler, M., Mahone, E. M., Denckla, M. B., Miller, M. I., et al. (2009). Basal ganglia volume and shape in children with attention deficit hyperactivity disorder. American Journal of Psychiatry, 166(1), 74–82. https://doi.org/10.1176/appi.ajp.2008.08030426.CrossRefGoogle Scholar
- Raznahan, A., Shaw, P. W., Lerch, J. P., Clasen, L. S., Greenstein, D., Berman, R., et al. (2014). Longitudinal four-dimensional mapping of subcortical anatomy in human development. Proceedings of the National Academy of Sciences of the United States of America, 111(4), 1592–1597. https://doi.org/10.1073/pnas.1316911111.CrossRefGoogle Scholar
- Setänen, S., Lehtonen, L., Parkkola, R., Aho, K., & Haataja, L. the, P. S. G.(2016). Prediction of neuromotor outcome in infants born preterm at 11 years of age using volumetric neonatal magnetic resonance imaging and neurological examinations. Developmental Medicine and Child Neurology, 58(7), 721–727. https://doi.org/10.1111/dmcn.13030.CrossRefGoogle Scholar
- Srinivasan, L., Dutta, R., Counsell, S. J., Allsop, J. M., Boardman, J. P., Rutherford, M. A., et al. (2007). Quantification of Deep Gray Matter in Preterm Infants at Term-Equivalent Age Using Manual Volumetry of 3-Tesla Magnetic Resonance Images. Pediatrics, 119(4), 759–765. https://doi.org/10.1542/peds.2006-2508.CrossRefGoogle Scholar
- Taylor, H. G., Filipek, P. A., Juranek, J., Bangert, B., Minich, N., & Hack, M. (2011). Brain volumes in adolescents with very low birth weight: Effects on brain structure and associations with neuropsychological outcomes. Developmental Neuropsychology, 36(1), 96–117. https://doi.org/10.1080/87565641.2011.540544.CrossRefGoogle Scholar
- Verney, C., Pogledic, I., Biran, V., Adle-Biassette, H., Fallet-Bianco, C., & Gressens, P. (2012). Microglial reaction in axonal crossroads is a hallmark of noncystic periventricular white matter injury in very preterm infants. Journal of Neuropathology and Experimental Neurology, 71(3), 251–264. https://doi.org/10.1097/NEN.0b013e3182496429.CrossRefGoogle Scholar
- Wechsler, D. (1999). Wechsler abbreviated scale of intelligence (WASI). New York: The Psychological Corporation.Google Scholar
- Wilkinson, G. S., & Robertson, G. J. (2006). Wide Range Achievement Test (WRAT4) (4th ed.). Lutz: Psychological Assessment Resources.Google Scholar