Mapping Continued Brain Growth and Gray Matter Density Reduction in Dorsal Frontal Cortex: Inverse Relationships during Postadolescent Brain Maturation

Recent in vivo structural imaging studies have shown spatial and temporal patterns of brain maturation between childhood, adolescence, and young adulthood that are generally consistent with postmortem studies of cellular maturational events such as increased myelination and synaptic pruning. In this study, we conducted detailed spatial and temporal analyses of growth and gray matter density at the cortical surface of the brain in a group of 35 normally developing children, adolescents, and young adults. To accomplish this, we used high-resolution magnetic resonance imaging and novel computational image analysis techniques. For the first time, in this report we have mapped the continued postadolescent brain growth that occurs primarily in the dorsal aspects of the frontal lobe bilaterally and in the posterior temporo-occipital junction bilaterally. Notably, maps of the spatial distribution of postadolescent cortical gray matter density reduction are highly consistent with maps of the spatial distribution of postadolescent brain growth, showing an inverse relationship between cortical gray matter density reduction and brain growth primarily in the superior frontal regions that control executive cognitive functioning. Inverse relationships are not as robust in the posterior temporo-occipital junction where gray matter density reduction is much less prominent despite late brain growth in these regions between adolescence and adulthood. Overall brain growth is not significant between childhood and adolescence, but close spatial relationships between gray matter density reduction and brain growth are observed in the dorsal parietal and frontal cortex. These results suggest that progressive cellular maturational events, such as increased myelination, may play as prominent a role during the postadolescent years as regressive events, such as synaptic pruning, in determining the ultimate density of mature frontal lobe cortical gray matter.

[1]  P. Yakovlev,et al.  The myelogenetic cycles of regional maturation of the brain , 1967 .

[2]  P. Huttenlocher Synaptic density in human frontal cortex - developmental changes and effects of aging. , 1979, Brain research.

[3]  G. Hynd,et al.  Neuropsychological development of behavior attributed to frontal lobe functioning in children , 1985 .

[4]  P. Huttenlocher,et al.  The development of synapses in striate cortex of man. , 1987, Human neurobiology.

[5]  D. Norman,et al.  Normal maturation of the neonatal and infant brain: MR imaging at 1.5 T. , 1988, Radiology.

[6]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[7]  R. Friede Gross and Microscopic Development of the Central Nervous System , 1989 .

[8]  小野 道夫,et al.  Atlas of the Cerebral Sulci , 1990 .

[9]  T. Jernigan,et al.  Maturation of human cerebrum observed in vivo during adolescence. , 1991, Brain : a journal of neurology.

[10]  W. Bank The Human Brain. Surface, Three-Dimensional Sectional Anatomy and MRI , 1993 .

[11]  J. Mazziotta,et al.  MRI‐PET Registration with Automated Algorithm , 1993, Journal of computer assisted tomography.

[12]  D. Mathalon,et al.  A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood. , 1994, Archives of neurology.

[13]  Alan C. Evans,et al.  Multiple surface identification and matching in magnetic resonance images , 1994, Other Conferences.

[14]  F. Benes,et al.  Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. , 1994, Archives of general psychiatry.

[15]  Arthur W. Toga,et al.  A Probabilistic Atlas of the Human Brain: Theory and Rationale for Its Development The International Consortium for Brain Mapping (ICBM) , 1995, NeuroImage.

[16]  Karl J. Friston,et al.  A Voxel-Based Method for the Statistical Analysis of Gray and White Matter Density Applied to Schizophrenia , 1995, NeuroImage.

[17]  Vasken Kollokian,et al.  Performance analysis of automatic techniques for tissue classification in magnetic resonance images of the human brain , 1996 .

[18]  J. Kleim,et al.  Synaptogenesis and FOS Expression in the Motor Cortex of the Adult Rat after Motor Skill Learning , 1996, The Journal of Neuroscience.

[19]  A. Reiss,et al.  Brain development, gender and IQ in children. A volumetric imaging study. , 1996, Brain : a journal of neurology.

[20]  P. Basser,et al.  Diffusion tensor MR imaging of the human brain. , 1996, Radiology.

[21]  C. Müller,et al.  Critical Period‐dependent Reduction of the Permissiveness of Cat Visual Cortex Tissue for Neuronal Adhesion and Neurite Growth , 1997, The European journal of neuroscience.

[22]  C. Gross,et al.  Neurogenesis in the neocortex of adult primates. , 1999, Science.

[23]  A. Toga,et al.  In vivo evidence for post-adolescent brain maturation in frontal and striatal regions , 1999, Nature Neuroscience.

[24]  A. Toga,et al.  Localizing Age-Related Changes in Brain Structure between Childhood and Adolescence Using Statistical Parametric Mapping , 1999, NeuroImage.

[25]  Alan C. Evans,et al.  Brain development during childhood and adolescence: a longitudinal MRI study , 1999, Nature Neuroscience.

[26]  Alan C. Evans,et al.  Structural maturation of neural pathways in children and adolescents: in vivo study. , 1999, Science.

[27]  R. Woods,et al.  Mathematical/computational challenges in creating deformable and probabilistic atlases of the human brain , 2000, Human brain mapping.

[28]  Christopher J. Cannistraci,et al.  Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. , 2000, JAMA.

[29]  R. Woods,et al.  Cortical change in Alzheimer's disease detected with a disease-specific population-based brain atlas. , 2001, Cerebral cortex.

[30]  D. Delis,et al.  Improved memory functioning and frontal lobe maturation between childhood and adolescence: A structural MRI study , 2001, Journal of the International Neuropsychological Society.

[31]  M. Diamond Response of the brain to enrichment. , 2001, Anais da Academia Brasileira de Ciencias.

[32]  T. Jernigan,et al.  Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study , 2002, Developmental medicine and child neurology.

[33]  A. Toga,et al.  Mapping sulcal pattern asymmetry and local cortical surface gray matter distribution in vivo: maturation in perisylvian cortices. , 2002, Cerebral cortex.