Hostname: page-component-8448b6f56d-sxzjt Total loading time: 0 Render date: 2024-04-17T19:38:43.967Z Has data issue: false hasContentIssue false

Preterm birth and maternal responsiveness during childhood are associated with brain morphology in adolescence

Published online by Cambridge University Press:  08 July 2010

RICHARD E. FRYE*
Affiliation:
Department of Pediatrics, University of Texas Health Science Center, Houston, Texas
BENJAMIN MALMBERG
Affiliation:
Department of Pediatrics, University of Texas Health Science Center, Houston, Texas
PAUL SWANK
Affiliation:
Department of Pediatrics, University of Texas Health Science Center, Houston, Texas
KAREN SMITH
Affiliation:
Department of Pediatrics, University of Texas Medical Branch, Galveston, Texas
SUSAN LANDRY
Affiliation:
Department of Pediatrics, University of Texas Health Science Center, Houston, Texas
*
*Correspondence and reprint requests to: Richard E. Frye, MD, PhD, Division of Child and Adolescent Neurology and The Children’s Learning Institute, Department of Pediatrics, University of Texas Health Science Center, 7000 Fannin – UCT 2478, Houston, TX 77030. E-mail: richard.e.frye@uth.tmc.edu

Abstract

Although supportive parenting has been shown to have positive effects on development, the neurobiological basis of supportive parenting has not been investigated. Thirty-three adolescents were systemically selected from a longitudinal study on child development based on maternal responsiveness during childhood, a measure of supportive parenting, and whether they were born term or preterm. We analyzed the effect of preterm birth on hemispheric and regional (frontal, temporal, parietal) cortical thickness and surface area using mixed-model analysis while also considering the effect of brain hemisphere (left vs. right). We then determined whether these factors were moderated by maternal responsiveness during childhood. Preterm birth was associated with regional and hemispheric differences in cortical thickness and surface area. Maternal responsiveness during childhood moderated hemispheric cortical thickness. Adolescence with mothers that were inconsistently responsive during childhood demonstrated greater overall cortical thickness and greater asymmetry in cortical thickness during adolescence as compared to adolescence with mothers who were consistently responsive or unresponsive during childhood. Maternal responsiveness and preterm birth did not interact. These data suggest that changes in brain morphology associated with preterm birth continue into adolescence and support the notion that the style of maternal-child interactions during childhood influence brain development into adolescence. (JINS, 2010, 16, 784–794.)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abernethy, L.J., Cooke, R.W., & Foulder-Hughes, L. (2004). Caudate and hippocampal volumes, intelligence, and motor impairment in 7-year-old children who were born preterm. Pediatric Research, 55, 884893.CrossRefGoogle ScholarPubMed
Anderson, P., Doyle, L.W., & Victorian Infant Collaborative Study Group. (2003). Neurobehavioral outcomes of school-age children born extremely low birth weight or very preterm in the 1990s. Journal of the American Medical Association, 289, 32643272.CrossRefGoogle ScholarPubMed
Anderson, P.J., Doyle, L.W., & Victorian Infant Collaborative Study Group. (2004). Executive functioning in school-aged children who were born very preterm or with extremely low birth weight in the 1990s. Pediatrics, 114, 5057.CrossRefGoogle ScholarPubMed
Aylward, G.P. (2002). Cognitive and neuropsychological outcomes: More than IQ scores. Mental Retardation and Developmental Disability Research Reviews, 8, 234240.CrossRefGoogle ScholarPubMed
Bayless, S., & Stevenson, J. (2007). Executive functions in school-age children born very prematurely. Early Human Development, 83, 247254.CrossRefGoogle ScholarPubMed
Beckwith, L., Rodning, C., & Cohen, S. (1992). Preterm children at early adolescence and continuity and discontinuity in maternal responsiveness from infancy. Child Development, 63, 11981208.CrossRefGoogle ScholarPubMed
Bhutta, A.T., Cleves, M.A., Casey, P.H., Cradock, M.M., & Anand, K.J. (2002). Cognitive and behavioral outcomes of school-aged children who were born preterm: A meta-analysis. Journal of the American Medical Association, 288, 728737.CrossRefGoogle ScholarPubMed
Byrne, M., Agerbo, E., Bennedsen, B., Eaton, W.W., & Mortensen, P.B. (2007). Obstetric conditions and risk of first admission with schizophrenia: A Danish national register based study. Schizophrenia Research, 97, 5159.CrossRefGoogle ScholarPubMed
Cannon, M., Jones, P.B., & Murray, R.M. (2002). Obstetric complications and schizophrenia: Historical and meta-analytic review. American Journal of Psychiatry, 159, 10801092.CrossRefGoogle ScholarPubMed
Dale, A.M., Fischl, B., & Sereno, M.I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage, 9, 179194.CrossRefGoogle ScholarPubMed
Dale, A.M., & Sereno, M.I. (1993). Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: A linear approach. Journal of Cognitive Neuroscience, 5, 162176.CrossRefGoogle ScholarPubMed
Desikan, R.S., Segonne, 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, 968980.CrossRefGoogle ScholarPubMed
Dragovic, M. (2004). Categorization and validation of handedness using latent class analysis. Neuropsychiatrica, 16, 212218.CrossRefGoogle ScholarPubMed
Eshel, N., Daelmans, B., de Mello, M.C., & Martines, J. (2006). Responsive parenting: Interventions and outcomes. Bulletin of the World Health Organization, 84, 991998.Google ScholarPubMed
Eskildsen, S.F., & Ostergaard, L.R. (2007). Quantitative comparison of two cortical surface extraction methods using MRI phantoms. Medical Image Computing and Computer-Assisted Intervention, 10, 409416.Google ScholarPubMed
Fischl, B., & Dale, A.M. (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences of the United States of America, 97, 1105011055.CrossRefGoogle ScholarPubMed
Fischl, B., Liu, A., & Dale, A.M. (2001). Automated manifold surgery: Constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Transactions on Medical Imaging, 20, 7080.CrossRefGoogle ScholarPubMed
Fischl, B., Salat, D.H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., et al. . (2002). Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron, 33, 341355.CrossRefGoogle ScholarPubMed
Fischl, B., Salat, D.H., van der Kouwe, A.J., Makris, N., Segonne, F., Quinn, B.T., et al. . (2004). Sequence-independent segmentation of magnetic resonance images. Neuroimage, 23(Suppl. 1), S69S84.CrossRefGoogle ScholarPubMed
Fischl, B., Sereno, M.I., & Dale, A.M. (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage, 9, 195207.CrossRefGoogle Scholar
Fischl, B., Sereno, M.I., Tootell, R.B., & Dale, A.M. (1999). High-resolution intersubject averaging and a coordinate system for the cortical surface. Human Brain Mapping, 8, 272284.3.0.CO;2-4>CrossRefGoogle Scholar
Fischl, B., van der Kouwe, A., Destrieux, C., Halgren, E., Segonne, F., Salat, D.H., et al. . (2004). Automatically parcellating the human cerebral cortex. Cerebral Cortex, 14, 1122.CrossRefGoogle ScholarPubMed
Fletcher, A., Walls, J., Cook, E., Madison, K., & Bridges, T. (2008). Parenting style as a moderator of associations between maternal disciplinary strategies and child well-being. Parenting style as a moderator of associations between maternal disciplinary strategies and child well-being. Journal of Family Issues, 29, 17241744.CrossRefGoogle Scholar
Frye, R.E., Fisher, J.M., Coty, A., Zarella, M., Liederman, J., & Halgren, E. (2007). Linear coding of voice onset time. Journal of Cognitive Neuroscience, 19, 14761487.CrossRefGoogle ScholarPubMed
Frye, R.E., Fisher, J.M., Witzel, T., Ahlfors, S.P., Swank, P., Liederman, J., et al. . (2008). Objective phonological and subjective perceptual characteristics of syllables modulate spatiotemporal patterns of superior temporal gyrus activity. Neuroimage, 40, 18881901.CrossRefGoogle ScholarPubMed
Frye, R.E., Hasan, K., Xue, L., Strickland, D., Malmberg, B., Liederman, J., et al. . (2009). Splenium microstructure is related to two dimensions of reading skill. Neuroreport, 19, 16271631.CrossRefGoogle Scholar
Frye, R.E., Landry, S.H., Swank, P.R., & Smith, K.E. (2009). Executive dysfunction in poor readers born prematurely at high risk. Developmental Neuropsychology, 34, 254271.CrossRefGoogle ScholarPubMed
Frye, R.E., Liederman, J.L., Malmberg, B., MacLean, J., Strickland, D., & Beauchamp, M.S. (2010). Surface area accounts for the relation of gray matter volume to reading-related skills and history of dyslexia. Cerebral Cortex, [Epub ahead of print].CrossRefGoogle ScholarPubMed
Gogtay, N., Giedd, J.N., Lusk, L., Hayashi, K.M., Greenstein, D., Vaituzis, A.C., et al. . (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences of the United States of America, 101, 81748179.CrossRefGoogle ScholarPubMed
Guajardo, N., Snyder, G., & Petersen, R. (2009). Relationships among parenting practices, parental stress, child behaviour, and children’s social-cognitive development. Infant and Child Development, 18, 3760.CrossRefGoogle Scholar
Geuze, E., Westenberg, H.G., Heinecke, A., de Kloet, C.S., Goebel, R., & Vermetten, E. (2008). Thinner prefrontal cortex in veterans with posttraumatic stress disorder. Neuroimage, 41, 675681.CrossRefGoogle ScholarPubMed
Haier, R.J., Karama, S., Leyba, L., & Jung, R.E. (2009). MRI assessment of cortical thickness and functional activity changes in adolescent girls following three months of practice on a visual-spatial task. BMC Research Notes, 2, 174.CrossRefGoogle ScholarPubMed
Han, X., Jovicich, J., Salat, D., van der Kouwe, A., Quinn, B., Czanner, S., et al. . (2006). Reliability of MRI-derived measurements of human cerebral cortical thickness: The effects of field strength, scanner upgrade and manufacturer. Neuroimage, 32, 180194.CrossRefGoogle ScholarPubMed
Herold, R., Feldmann, A., Simon, M., Tenyi, T., Kover, F., Nagy, F., et al. . (2009). Regional gray matter reduction and theory of mind deficit in the early phase of schizophrenia: A voxel-based morphometric study. Acta Psychiatrica Scandinavica, 119, 199208.CrossRefGoogle ScholarPubMed
Im, K., Lee, J.M., Seo, S.W., Yoon, U., Kim, S.T., Kim, Y.H., et al. . (2008). Variations in cortical thickness with dementia severity in Alzheimer’s disease. Neuroscience Letters, 436, 227231.CrossRefGoogle ScholarPubMed
Im, K., Lee, J.M., Won Seo, S., Hyung Kim, S., Kim, S.I., & Na, D.L. (2008). Sulcal morphology changes and their relationship with cortical thickness and gyral white matter volume in mild cognitive impairment and Alzheimer’s disease. Neuroimage, 43, 103113.CrossRefGoogle ScholarPubMed
Janssen, J., Reig, S., Alemán, Y., Schnack, H., Udias, J.M., Parellada, M., et al. . (2009). Gyral and sulcal cortical thinning in adolescents with first episode early-onset psychosis. Biological Psychiatry, 66, 10471054.CrossRefGoogle ScholarPubMed
Kapellou, O., Counsell, S.J., Kennea, N., Dyet, L., Saeed, N., Stark, J., et al. . (2006). Abnormal cortical development after premature birth shown by altered allometric scaling of brain growth. PLoS Medicine, 3, e265.CrossRefGoogle ScholarPubMed
Kobayashi, C., Glover, G.H., & Temple, E. (2007a). Children’s and adults’ neural bases of verbal and nonverbal ’theory of mind’. Neuropsychologia, 45, 15221532.CrossRefGoogle ScholarPubMed
Kobayashi, C., Glover, G.H., & Temple, E. (2007b). Cultural and linguistic effects on neural bases of ’Theory of Mind’ in American and Japanese children. Brain Research, 1164, 95107.CrossRefGoogle ScholarPubMed
Kobayashi, C., Glover, G.H., & Temple, E. (2008). Switching language switches mind: Linguistic effects on developmental neural bases of ‘Theory of Mind’. Social Cognitive and Affective Neuroscience, 3, 6270.CrossRefGoogle ScholarPubMed
Kuban, K.C., O’Shea, T.M., Allred, E.N., Tager-Flusberg, H., Goldstein, D.J., & Leviton, A. (2009). Positive screening on the Modified Checklist for Autism in Toddlers (M-CHAT) in extremely low gestational age newborns. Journal of Pediatrics, 154, 535540.CrossRefGoogle ScholarPubMed
Landing, B.H., Shankle, W.R., Hara, J., Brannock, J., & Fallon, J.H. (2002). The development of structure and function in the postnatal human cerebral cortex from birth to 72 months: Changes in thickness of layers II and III co-relate to the onset of new age-specific behaviors. Pediatric Pathology and Molecular Medicine, 21, 321342.CrossRefGoogle Scholar
Landry, S.H., Smith, K.E., Miller-Loncar, C.L., & Swank, P. (1997). Predicting cognitive-linguistic and social growth curves from early maternal behaviors in children at varying degrees of biologic risk. Child Development, 69, 105123.Google Scholar
Landry, S.H., Smith, K.E., & Swank, P.R. (2003). The importance of parenting during early childhood for school-age development. Developmental Neuropsychology, 24, 559591.CrossRefGoogle ScholarPubMed
Landry, S.H., Smith, K.E., & Swank, P.R. (2006). Responsive parenting: Establishing early foundations for social, communication, and independent problem-solving skills. Developmental Psychology, 42, 627642.CrossRefGoogle ScholarPubMed
Landry, S.H., Smith, K.E., Swank, P.R., Assel, M.A., & Vellet, S. (2001). Does early responsive parenting have a special importance for children’s development or is consistency across early childhood necessary? Developmental Psychology, 37, 387403.CrossRefGoogle ScholarPubMed
Landry, S.H., Smith, K.E., Swank, P.R., & Guttentag, C. (2008). A responsive parenting intervention: The optimal timing across early childhood for impacting maternal behaviors and child outcomes. Developmental Psychology, 44, 13351353.CrossRefGoogle ScholarPubMed
Lee, J.K., Lee, J.M., Kim, J.S., Kim, I.Y., Evans, A.C., & Kim, S.I. (2006). A novel quantitative cross-validation of different cortical surface reconstruction algorithms using MRI phantom. Neuroimage, 31, 572584.CrossRefGoogle ScholarPubMed
Limperopoulos, C., Bassan, H., Sullivan, N.R., Soul, J.S., Robertson, R.L. Jr., Moore, M., et al. . (2008). Positive screening for autism in ex-preterm infants: Prevalence and risk factors. Pediatrics, 121, 758765.CrossRefGoogle ScholarPubMed
Makris, N., Kaiser, J., Haselgrove, C., Seidman, L.J., Biederman, J., Boriel, D., et al. . (2006). Human cerebral cortex: A system for the integration of volume- and surface-based representations. Neuroimage, 33, 139153.CrossRefGoogle ScholarPubMed
Martinussen, M., Fischl, B., Larsson, H.B., Skranes, J., Kulseng, S., Vangberg, T.R., et al. . (2005). Cerebral cortex thickness in 15-year-old adolescents with low birth weight measured by an automated MRI-based method. Brain, 128, 25882596.CrossRefGoogle ScholarPubMed
Neeren, A., Alloy, L., & Abramson, L. (2008). History of parenting and bipolar spectrum disorders. Journal of Social and Clinical Psychology, 27, 10211044.CrossRefGoogle Scholar
Noel, M., Peterson, C., & Jesso, B. (2008). The relationship of parenting stress and child temperament to language development among economically disadvantaged preschoolers. Journal of Child Language, 35, 823843.CrossRefGoogle ScholarPubMed
Nordahl, C.W., Dierker, D., Mostafavi, I., Schumann, C.M., Rivera, S.M., Amaral, D.G., et al. . (2007). Cortical folding abnormalities in autism revealed by surface-based morphometry. Journal of Neuroscience, 27, 1172511735.CrossRefGoogle ScholarPubMed
Nosarti, C., Al-Asady, M.H., Frangou, S., Stewart, A.L., Rifkin, L., & Murray, R.M. (2002). Adolescents who were born very preterm have decreased brain volumes. Brain, 125, 16161623.CrossRefGoogle ScholarPubMed
Oldfield, R.C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97113.CrossRefGoogle ScholarPubMed
Peterson, B.S., Anderson, A.W., Ehrenkranz, R., Staib, L.H., Tageldin, M., Colson, E., et al. . (2003). Regional volumes and their later neurodevelopmental correlates in term and preterm infants. Pediatrics, 111, 939948.CrossRefGoogle ScholarPubMed
Pienaar, R., Fischl, B., Caviness, B., Makris, N. & Grant, P. (2008). A methodology for analyzing curvature in the developing brain from preterm to adult. International Journal of Imaging Systems and Technology Special Issue: Human Brain Imaging, 18, 4268.CrossRefGoogle ScholarPubMed
Rabinowicz, T., Petetot, J.M., Khoury, J.C., & de Courten-Myers, G.M. (2009). Neocortical maturation during adolescence: Change in neuronal soma dimension. Brain and Cognition, 69, 328336.CrossRefGoogle ScholarPubMed
Raznahan, A., Toro, R., Daly, E., Robertson, D., Murphy, C., Deeley, Q., et al. . (2009). Cortical anatomy in autism spectrum disorder: An in vivo mri study on the effect of age. Cerebral Cortex, [Epub ahead of print].Google Scholar
Sansavini, A., Guarini, A., Alessandroni, R., Faldella, G., Giovanelli, G., & Salvioli, G. (2006). Early relations between lexical and grammatical development in very immature Italian preterms. Journal of Child Language, 33, 199216.CrossRefGoogle ScholarPubMed
Sansavini, A., Guarini, A., Alessandroni, R., Faldella, G., Giovanelli, G., & Salvioli, G. (2007). Are early grammatical and phonological working memory abilities affected by preterm birth? Journal of Communication Disorders, 40, 239256.CrossRefGoogle ScholarPubMed
Segonne, F., Pacheco, J., & Fischl, B. (2007). Geometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Transactions of Medical Imaging, 26, 518529.CrossRefGoogle ScholarPubMed
Seo, S.W., Im, K., Lee, J.M., Kim, Y.H., Kim, S.T., Kim, S.Y., et al. . (2007). Cortical thickness in single- versus multiple-domain amnestic mild cognitive impairment. Neuroimage, 36, 289297.CrossRefGoogle ScholarPubMed
Shaw, P., Kabani, N.J., Lerch, J.P., Eckstrand, K., Lenroot, R., Gogtay, N., et al. . (2008). Neurodevelopmental trajectories of the human cerebral cortex. Journal of Neuroscience, 28, 35863594.CrossRefGoogle ScholarPubMed
Shaw, P., Lalonde, F., Lepage, C., Rabin, C., Eckstrand, K., Sharp, W., et al. . (2009). Development of cortical asymmetry in typically developing children and its disruption in attention-deficit/hyperactivity disorder. Archives of General Psychiatry, 66, 888896.CrossRefGoogle ScholarPubMed
Short, E.J., Klein, N.K., Lewis, B.A., Fulton, S., Eisengart, S., Kercsmar, C., et al. . (2003). Cognitive and academic consequences of bronchopulmonary dysplasia and very low birth weight: 8-year-old outcomes. Pediatrics, 112, e359.CrossRefGoogle ScholarPubMed
Skranes, J., Vangberg, T.R., Kulseng, S., Indredavik, M.S., Evensen, K.A., Martinussen, M., et al. . (2007). Clinical findings and white matter abnormalities seen on diffusion tensor imaging in adolescents with very low birth weight. Brain, 130, 654666.CrossRefGoogle ScholarPubMed
Smith, K.E., Landry, S.H., & Swank, P.R. (2000). Does the content of mothers’ verbal stimulation explain differences in children’s development of verbal and nonverbal cognitive skills? Journal of School Psychology, 38, 2749.CrossRefGoogle Scholar
Smith, K.E., Landry, S.H., & Swank, P.R. (2005). The influence of decreased parental resources on the efficacy of a responsive parenting intervention. Journal of Consulting and Clinical Psychology, 73, 711720.CrossRefGoogle ScholarPubMed
Smith, K.E., Landry, S.H., & Swank, P.R. (2006). The role of early maternal responsiveness in supporting school-aged cognitive development for children who vary in birth status. Pediatrics, 117, 16081617.CrossRefGoogle ScholarPubMed
Stolt, S., Klippi, A., Launonen, K., Munck, P., & Lehtonen, L. (2007). Size and composition of the lexicon in prematurely born very-low-birth-weight and full-term Finnish children at two years of age. Journal of Child Language, 34, 283310.CrossRefGoogle Scholar
Tamnes, C.K., Ostby, Y., Fjell, A.M., Westlye, L.T., Due-Tønnessen, P., & Walhovd, K.B. (2010). Brain maturation in adolescence and young adulthood: Regional age-related changes in cortical thickness and white matter volume and microstructure. Cerebral Cortex, 20, 534548CrossRefGoogle Scholar
Taylor, S.E., Eisenberger, N.I., Saxbe, D., Lehman, B.J., & Lieberman, M.D. (2006). Neural responses to emotional stimuli are associated with childhood family stress. Biological Psychiatry, 60, 296301.CrossRefGoogle ScholarPubMed
Voets, N.L., Hough, M.G., Douaud, G., Matthews, P.M., James, A., Winmill, L., et al. . (2008). Evidence for abnormalities of cortical development in adolescent-onset schizophrenia. Neuroimage, 43, 665675.CrossRefGoogle ScholarPubMed
Volpe, J.J. (2009). Brain injury in premature infants: A complex amalgam of destructive and developmental disturbances. Lancet Neurology, 8, 110124.CrossRefGoogle ScholarPubMed
White, T., Andreasen, N.C., Nopoulos, P., & Magnotta, V. (2003). Gyrification abnormalities in childhood- and adolescent-onset schizophrenia. Biological Psychiatry, 54, 418426.CrossRefGoogle ScholarPubMed
Wolke, D., & Meyer, R. (1999). Cognitive status, language attainment, and prereading skills of 6-year-old very preterm children and their peers: The Bavarian Longitudinal Study. Developmental Medicine and Child Neurology, 41, 94109.Google ScholarPubMed
Yap, M.B., Whittle, S., Yucel, M., Sheeber, L., Pantelis, C., Simmons, J.G., et al. . (2008). Interaction of parenting experiences and brain structure in the prediction of depressive symptoms in adolescents. Archives of General Psychiatry, 65, 13771385.CrossRefGoogle ScholarPubMed