Tracking Development of the Corpus Callosum in Fetal and Early Postnatal Baboons Using Magnetic Resonance Imaging

Although the maturation of the corpus callosum (CC) can serve as a sensitive marker for normative antenatal and postnatal brain development, little is known about its development across this critical period. While high-resolution magnetic resonance imaging can provide an opportunity to examine normative brain development in humans, concerns remain over the exposure of developing fetuses to non-essential imaging. Nonhuman primates can provide a valuable model for normative brain maturation. Baboons share several important developmental characteristics with humans, including a highly orchestrated pattern of cerebral development. Developmental changes in total CC area and its subdivisions were examined across the antenatal (weeks 17 – 26 of 28 weeks total gestation) and early postnatal (to week 32) period in baboons (Papio hamadryas anubis). Thirteen fetal and sixteen infant baboons were studied using high-resolution MRI. During the period of primary gyrification, the total area of the CC increased by a magnitude of five. By postnatal week 32, the total CC area attained only 51% of the average adult area. CC subdivisions showed non-uniform increases in area, throughout development. The splenium showed the most maturation by postnatal week 32, attaining 55% of the average adult value. The subdivisions of the genu and anterior midbody showed the least maturation by postnatal week 32, attaining 50% and 49% of the average adult area. Thus, the CC of baboons shows continued growth past the postnatal period. These age-related changes in the developing baboon CC are consistent with the developmental course in humans.

[1]  J C Rajapakse,et al.  A quantitative MRI study of the corpus callosum in children and adolescents. , 1996, Brain research. Developmental brain research.

[2]  Grace Tiao,et al.  Insights into the gyrification of developing ferret brain by magnetic resonance imaging , 2007, Journal of anatomy.

[3]  E. Alvord,et al.  Agenesis of the corpus callosum. , 1968, Brain : a journal of neurology.

[4]  A. Scheibel,et al.  Fiber composition of the human corpus callosum , 1992, Brain Research.

[5]  Jagath C. Rajapakse,et al.  Development of the human corpus callosum during childhood and adolescence: A longitudinal MRI study , 1999, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[6]  Feng Gao,et al.  Retrospective motion correction protocol for high‐resolution anatomical MRI , 2006, Human brain mapping.

[7]  J. Mugler,et al.  Three‐dimensional magnetization‐prepared rapid gradient‐echo imaging (3D MP RAGE) , 1990, Magnetic resonance in medicine.

[8]  William D. Hopkins,et al.  Age-related neuroanatomical differences from the juvenile period to adulthood in mother-reared macaques (Macaca radiata) , 2008, Brain Research.

[9]  Jens Frahm,et al.  Topography of the human corpus callosum revisited—Comprehensive fiber tractography using diffusion tensor magnetic resonance imaging , 2006, NeuroImage.

[10]  R. Gorski,et al.  Sex differences in the corpus callosum of the living human being , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  Chet C. Sherwood,et al.  Cortical development in brown capuchin monkeys: A structural MRI study , 2008, NeuroImage.

[12]  A. Achiron,et al.  Development of the human fetal corpus callosum: a high‐resolution, cross‐sectional sonographic study , 2001, Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology.

[13]  A. Addington,et al.  The neurodevelopmental model of schizophrenia: What can very early onset cases tell us? , 2005, Current psychiatry reports.

[14]  Sarah Durston,et al.  New potential leads in the biology and treatment of attention deficit-hyperactivity disorder , 2007, Current opinion in neurology.

[15]  L. Luo,et al.  Axon retraction and degeneration in development and disease. , 2005, Annual review of neuroscience.

[16]  Scott D. Moffat,et al.  Testosterone is correlated with regional morphology of the human corpus callosum , 1997, Brain Research.

[17]  A J Barkovich,et al.  Normal postnatal development of the corpus callosum as demonstrated by MR imaging. , 1988, AJNR. American journal of neuroradiology.

[18]  C. Sherwood,et al.  Corpus Callosum Morphology in Capuchin Monkeys Is Influenced by Sex and Handedness , 2007, PloS one.

[19]  Paul M. Thompson,et al.  Sexual dimorphism of brain developmental trajectories during childhood and adolescence , 2007, NeuroImage.

[20]  P. Manger,et al.  Order‐specific quantitative patterns of cortical gyrification , 2007, The European journal of neuroscience.

[21]  K Zilles,et al.  Cortical gyrification in the rhesus monkey: a test of the mechanical folding hypothesis. , 1991, Cerebral cortex.

[22]  K E FOGHT-NIELSEN,et al.  [Agenesis of the corpus callosum]. , 1954, Ugeskrift for laeger.

[23]  A. Schleicher,et al.  Gyrification in the cerebral cortex of primates. , 1989, Brain, behavior and evolution.

[24]  Jagath C. Rajapakse,et al.  Regional MRI measurements of the corpus callosum: a methodological and developmental study , 1996, Brain and Development.

[25]  P. Rakić,et al.  Axon overproduction and elimination in the corpus callosum of the developing rhesus monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  Larry A. Kramer,et al.  Diffusion tensor quantification of the human midsagittal corpus callosum subdivisions across the lifespan , 2008, Brain Research.

[27]  B. C. Richardson,et al.  Human corpus callosum in aging and alzheimer's disease: a magnetic resonance imaging study , 1994, Neurobiology of Aging.

[28]  Ronald A. Cohen,et al.  Diffusion tensor imaging of the corpus callosum: a cross-sectional study across the lifespan , 2007, International Journal of Developmental Neuroscience.

[29]  Peter Kochunov,et al.  Mapping Primary Gyrogenesis During Fetal Development in Primate Brains: High-Resolution in Utero Structural MRI of Fetal Brain Development in Pregnant Baboons , 2010, Front. Neurosci..

[30]  J. Hutsler,et al.  Comparative analysis of cortical layering and supragranular layer enlargement in rodent carnivore and primate species , 2005, Brain Research.

[31]  S. Tardif,et al.  The Baboon in Biomedical Research , 2009 .

[32]  J TOMASCH,et al.  Size, distribution, and number of fibres in the human Corpus Callosum , 1954, The Anatomical record.

[33]  Larry A. Kramer,et al.  Diffusion tensor tractography quantification of the human corpus callosum fiber pathways across the lifespan , 2009, Brain Research.

[34]  C. Groves,et al.  Primate evolution--in and out of Africa. , 1998, Current biology : CB.

[35]  N. Jablonski,et al.  Primate evolution — in and out of Africa , 1999, Current Biology.

[36]  Peter Kochunov,et al.  Development of structural MR brain imaging protocols to study genetics and maturation. , 2010, Methods.

[37]  R. Rauch,et al.  Analysis of cross-sectional area measurements of the corpus callosum adjusted for brain size in male and female subjects from childhood to adulthood , 1994, Behavioural Brain Research.

[38]  J. Rilling,et al.  Differential rearing affects corpus callosum size and cognitive function of rhesus monkeys , 1998, Brain Research.

[39]  P. Basser,et al.  In vivo measurement of axon diameter distribution in the corpus callosum of rat brain. , 2009, Brain : a journal of neurology.

[40]  C. Comstock,et al.  Agenesis of the corpus callosum in the fetus: its evolution and significance. , 1985, Journal of ultrasound in medicine : official journal of the American Institute of Ultrasound in Medicine.

[41]  Gregor Kasprian,et al.  MRI of normal fetal brain development. , 2006, European journal of radiology.

[42]  G. Dawson,et al.  The role of early experience in shaping behavioral and brain development and its implications for social policy , 2000, Development and Psychopathology.

[43]  A. Schleicher,et al.  The ontogeny of human gyrification. , 1995, Cerebral cortex.

[44]  A. Toga,et al.  The Development of the Corpus Callosum in the Healthy Human Brain , 2010, The Journal of Neuroscience.

[45]  Andrew L. Alexander,et al.  Diffusion tensor imaging of the corpus callosum in Autism , 2007, NeuroImage.

[46]  A. Galaburda,et al.  Individual variability in cortical organization: Its relationship to brain laterality and implications to function , 1990, Neuropsychologia.

[47]  A Capdevila,et al.  When does human brain development end? Evidence of corpus callosum growth up to adulthood , 1993, Annals of neurology.

[48]  M. Kalia Brain development: anatomy, connectivity, adaptive plasticity, and toxicity. , 2008, Metabolism: clinical and experimental.

[49]  William D Hopkins,et al.  Cross-sectional analysis of the association between age and corpus callosum size in chimpanzees (Pan troglodytes). , 2010, Developmental psychobiology.

[50]  D. V. Essen,et al.  Surface-Based and Probabilistic Atlases of Primate Cerebral Cortex , 2007, Neuron.

[51]  Dealing with pregnancy in radiology: a thin line between science, social and regulatory aspects. , 2009, JBR-BTR : organe de la Societe royale belge de radiologie (SRBR) = orgaan van de Koninklijke Belgische Vereniging voor Radiologie.

[52]  R. Turner,et al.  Optimization of 3-D MP-RAGE Sequences for Structural Brain Imaging , 2000, NeuroImage.

[53]  Feng Liu,et al.  Study of the development of fetal baboon brain using magnetic resonance imaging at 3 Tesla , 2008, NeuroImage.

[54]  Eileen Luders,et al.  Structural and functional reorganization of the corpus callosum between the age of 6 and 8 years. , 2011, Cerebral cortex.

[55]  P. Levitt Structural and functional maturation of the developing primate brain. , 2003, The Journal of pediatrics.

[56]  Peter Kochunov,et al.  Heritability of brain volume, surface area and shape: An MRI study in an extended pedigree of baboons , 2007, Human brain mapping.