Development of structural MR brain imaging protocols to study genetics and maturation.

Structural imaging research offers excellent translational benefits when non-human primate (NHP) models are employed. In this paper, we will discuss the development of anatomical MR imaging protocols for two important applications of structural imaging in NHPs: studies of genetic variability in brain morphology and longitudinal imaging of fetal brain maturation trends. In contrast with imaging studies of adult humans, structural imaging in the NHPs is challenging due to a comparatively small brain size (2- to 200-fold smaller volume, depending on the species). This difference in size is further accentuated in NHP studies of brain development in which fetal brain volumes are 10-50% of their adult size. The sizes of cortical gyri and sulci scale allometrically with brain size. Thus, achieving spatial sampling that is comparable to that of high-quality human studies (approximately 1.0 mm(3)) requires a brain-size-adjusted reduction in the sampling volumes of from 500-to-150 microm(3). Imaging at this spatial resolution while maintaining sufficient contrast and signal to noise ratio necessitates the development of specialized MRI protocols. Here we discuss our strategy to optimize the protocol parameters for two commonly available structural imaging sequences: MPRAGE and TrueFisp. In addition, computational tools developed for the analysis of human structural images were applied to the NHP studies. These included removal of non-brain tissues, correction for RF inhomogeneity, spatial normalization, building of optimized target brain and analysis of cerebral gyrification and individual cortical variability. Finally, recent findings in the genetics of cerebral gyrification and tracking of maturation trends in the fetal, newborn and adult brain are described.

[1]  Sterling C. Johnson,et al.  A population-average MRI-based atlas collection of the rhesus macaque , 2009, NeuroImage.

[2]  PhD Jean C. Tamraz MD,et al.  Atlas of Regional Anatomy of the Brain Using MRI , 2000, Springer Berlin Heidelberg.

[3]  J Blangero,et al.  Power of variance component linkage analysis to detect quantitative trait loci. , 1999, Annals of human genetics.

[4]  Katrin Amunts,et al.  Cortical Folding Patterns and Predicting Cytoarchitecture , 2007, Cerebral cortex.

[5]  Jean-Francois Mangin,et al.  Coordinate-based versus structural approaches to brain image analysis , 2004, Artif. Intell. Medicine.

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

[7]  J. Blangero,et al.  Comparison of variance components and sibpair‐based approaches to quantitative trait linkage analysis in unselected samples , 1999, Genetic epidemiology.

[8]  J. Blangero,et al.  BioMed Central , 2001 .

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

[10]  Laura A Cox,et al.  Localization of genes that control LDL size fractions in baboons. , 2003, Atherosclerosis.

[11]  P Kochunov,et al.  Evaluation of octree regional spatial normalization method for regional anatomical matching , 2000, Human brain mapping.

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

[13]  J. Blangero,et al.  Quantitative genetic analysis of glucose transporter 4 mRNA levels in baboon adipose. , 2004, Obesity research.

[14]  J. Mazziotta,et al.  Regional Spatial Normalization: Toward an Optimal Target , 2001, Journal of computer assisted tomography.

[15]  W. Welker,et al.  Why Does Cerebral Cortex Fissure and Fold ? A Review of Determinants of Gyri and Sulci , 2022 .

[16]  M. Raichle,et al.  A Stereotactic Method of Anatomical Localization for Positron Emission Tomography , 1985, Journal of computer assisted tomography.

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

[18]  K. Amunts,et al.  Localized morphological brain differences between English-speaking Caucasians and Chinese-speaking Asians: new evidence of anatomical plasticity , 2003, Neuroreport.

[19]  A. Schleicher,et al.  The human pattern of gyrification in the cerebral cortex , 2004, Anatomy and Embryology.

[20]  P. Fox,et al.  Global spatial normalization of human brain using convex hulls. , 1999, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

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

[22]  S. Leigh Brain growth, life history, and cognition in primate and human evolution , 2004, American journal of primatology.

[23]  P. Morosan,et al.  Probabilistic Mapping and Volume Measurement of Human Primary Auditory Cortex , 2001, NeuroImage.

[24]  P. Schoenemann Evolution of the Size and Functional Areas of the Human Brain , 2006 .

[25]  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.

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

[27]  L. Garey Brodmann's localisation in the cerebral cortex , 1999 .

[28]  J. Rogers,et al.  A quantitative trait locus for normal variation in forearm bone mineral density in pedigreed baboons maps to the ortholog of human chromosome 11q. , 2005, The Journal of clinical endocrinology and metabolism.

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

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

[31]  R. Barton Primate brain evolution: Integrating comparative, neurophysiological, and ethological data , 2006 .

[32]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[33]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

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

[35]  R. Martin Primate origins and evolution , 1990 .

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

[37]  Jean-Francois Mangin,et al.  Automatic recognition of cortical sulci of the human brain using a congregation of neural networks , 2002, Medical Image Anal..

[38]  Peter T. Fox,et al.  Mapping structural differences of the corpus callosum in individuals with 18q deletions using targetless regional spatial normalization , 2005, Human brain mapping.

[39]  Isabelle Bloch,et al.  From 3D magnetic resonance images to structural representations of the cortex topography using topology preserving deformations , 1995, Journal of Mathematical Imaging and Vision.

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

[41]  J. Rademacher,et al.  Variability and asymmetry in the human precentral motor system. A cytoarchitectonic and myeloarchitectonic brain mapping study. , 2001, Brain : a journal of neurology.

[42]  Karl J. Friston,et al.  Automatic Differentiation of Anatomical Patterns in the Human Brain: Validation with Studies of Degenerative Dementias , 2002, NeuroImage.

[43]  Todd M. Preuss,et al.  Human brain evolution , 1999 .

[44]  Jack L. Lancaster,et al.  Accurate High-Speed Spatial Normalization Using an Octree Method , 1999, NeuroImage.

[45]  J. Blangero,et al.  Genome-wide scan of resistin mRNA expression in omental adipose tissue of baboons , 2005, International Journal of Obesity.

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

[47]  J. Blangero Localization and identification of human quantitative trait loci: king harvest has surely come. , 2004, Current opinion in genetics & development.

[48]  Hans Lüders,et al.  Atlas of Regional Anatomy of the Brain Using MRI: With Functional Correlations , 2000 .

[49]  A. Galaburda,et al.  Topographical variation of the human primary cortices: implications for neuroimaging, brain mapping, and neurobiology. , 1993, Cerebral cortex.