Diffusion MR imaging characteristics of the developing primate brain

Abstract

Diffusion-based magnetic resonance imaging holds the potential to noninvasively demonstrate cellular-scale structural properties of brain. This method was applied to fixed baboon brains ranging from 90 to 185 days gestational age to characterize the changes in diffusion properties associated with brain development. Within each image voxel, a probability-theory-based approach was employed to choose, from a group of analytic equations, the one that best expressed water displacements. The resulting expressions contain eight or fewer adjustable parameters, indicating that relatively simple expressions are sufficient to obtain a complete description of the diffusion MRI signal in developing brain. The measured diffusion parameters changed systematically with gestational age, reflecting the rich underlying microstructural changes that take place during this developmental period. These changes closely parallel those of live, developing human brain. The information obtained from this primate model of cerebral microstructure is directly applicable to studies of human development. D 2004 Elsevier Inc. All rights reserved.Keywords: Magnetic resonance imaging; Diffusion anisotropy; Baboon brains; Brain development IntroductionMagnetic resonance imaging (MRI) is increasingly utilized in human and animal studies to provide information relating to cerebral injury and development in the newborn. Diffusion MRI, in particular, is being applied to assess brain development (Huppi et al., 1998;Neil et al., 2002;Partridge et al., 2004;Rutherford et al., 2004). Diffusion MRI provides information about the directional dependence of water displacements due to diffusion. This, in turn, reflects underlying tissue microstructure. In white matter, for example, water moving parallel to myelinated fibers can move within or between myelin layers, without crossing membranes. Water moving orthogonal to fibers, on the other hand, must either cross myelin layers or go around them. As a result, water displacements are smaller when measured orthogonal to myelinated fibers than when measured parallel to them. Thus, water diffusion in myelinated white matter is anisotropic. The regional changes in diffusion anisotropy within the developing white matter of the newborn brain have been well appreciated for some time (Huppi et al., 1998;Neil et al., 1998).Diffusion anisotropy has also been described within cerebral cortical gray matter in the developing human brain. Anisotropy is high early in development, with the preferred displacement direction oriented radially with respect to the cortical surface (Maas et al., 2004;Mori et al., 2001;Neil et al., 1998). This has been attributed to the orientation of radial glial fibers and the apical dendrites of pyramidal cells. As the brain matures, the magnitude of cortical diffusion anisotropy decreases (McKinstry et al., 2002;Mori et al., 2001), reflecting a loss in orientational coherence of cortical structures that restrict diffusion. This may be due to the elaboration of pyramidal cell basal dendrites, additio...

Inhaled Nitric Oxide: Effects on Cerebral Growth and Injury in a Baboon Model of Premature Delivery

“…Thus, the impact of iNO in protecting cortical development may be mediated by a direct neuronal effect. The application of advanced MRI may better delineate brain surface morphology and gyrification in this model (24); these techniques are now being used in preterm infants (25,26) and could be applied to recent randomized trials of iNO in human preterm infants.…”

Microstructural Changes of the Baboon Cerebral Cortex during Gestational Development Reflected in Magnetic Resonance Imaging Diffusion Anisotropy

“…Animal handling and ethics were approved to conform to American Association for Accreditation of Laboratory Animal Care guidelines. Procedures have been described previously (Kroenke et al, 2005). Table 1 summarizes data for seven brains analyzed by MRI.…”

“…Regional differences in cortical diffusion anisotropy have been reported in prematurely born human infants (Deipolyi et al, 2005) and in developing baboon brain analyzed postmortem (Kroenke et al, 2005), but the underlying biological source of this variation has not been described. These previous studies analyzed variation between limited regions of interest or within individual MRI slices.…”

The average baboon brain: MRI templates and tissue probability maps from 89 individuals

“…The baboon brain also has a larger degree of gyrification (folding) than other Old World monkeys and contains all the primary cortical structures found in humans (Rogers et al, 2010). Accordingly, the baboon model has been used in numerous structural and functional neuroimaging experiments (e.g., Kochunov et al, 2010aKochunov et al, , 2010bKroenke et al, 2005Kroenke et al, , 2007Liu et al, 2008;Miller et al, 2013;Phillips and Kochunov, 2011;Phillips et al, 2012;Rogers et al, 2007;Salinas et al, 2011;Szabo et al, 2007Szabo et al, , 2011aSzabo et al, , 2011bWey et al, 2013).…”