Development of cerebral fiber pathways in cats by diffusion spectrum imaging

Department of Radiology, Harvard Medical School, Charlestown, MA, USA.
NeuroImage (Impact Factor: 6.36). 09/2009; 49(2):1231-40. DOI: 10.1016/j.neuroimage.2009.09.002
Source: PubMed


Examination of the three-dimensional axonal pathways in the developing brain is key to understanding the formation of cerebral connectivity. By tracing fiber pathways throughout the entire brain, diffusion tractography provides information that cannot be achieved by conventional anatomical MR imaging or histology. However, standard diffusion tractography (based on diffusion tensor imaging, or DTI) tends to terminate in brain areas with low water diffusivity, indexed by low diffusion fractional anisotropy (FA), which can be caused by crossing fibers as well as fibers with less myelin. For this reason, DTI tractography is not effective for delineating the structural changes that occur in the developing brain, where the process of myelination is incomplete, and where crossing fibers exist in greater numbers than in the adult brain. Unlike DTI, diffusion spectrum imaging (DSI) can define multiple directions of water diffusivity; as such, diffusion tractography based on DSI provides marked flexibility for delineation of fiber tracts in areas where the fiber architecture is complex and multidirectional, even in areas of low FA. In this study, we showed that FA values were lower in the white matter of newborn (postnatal day 0; P0) cat brains than in the white matter of infant (P35) and juvenile (P100) cat brains. These results correlated well with histological myelin stains of the white matter: the newborn kitten brain has much less myelin than that found in cat brains at later stages of development. Using DSI tractography, we successfully identified structural changes in thalamo-cortical and cortico-cortical association tracts in cat brains from one stage of development to another. In newborns, the main body of the thalamo-cortical tract was smooth, and fibers branching from it were almost straight, while the main body became more complex and branching fibers became curved reflecting gyrification in the older cats. Cortico-cortical tracts in the temporal lobe were smooth in newborns, and they formed a sharper angle in the later stages of development. The cingulum bundle and superior longitudinal fasciculus became more visible with time. Within the first month after birth, structural changes occurred in these tracts that coincided with the formation of the gyri. These results show that DSI tractography has the potential for mapping morphological changes in low FA areas associated with growth and development. The technique may also be applicable to the study of other forms of brain plasticity, including future studies in vivo.

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    • "Of note, the mask image is a 3D binary image created from a mean diffusion image of each brain assessment with endpoints constrained to the brain tissue itself. The brain mask volumes were used to terminate tractography structures instead of the FA threshold (Schmahmann et al. 2007; Wedeen et al. 2008; Takahashi et al. 2010, 2012; Vishwas et al. 2010), because progressive myelination and crossing fibers in the developing brain can result in low FA values that may potentially incorrectly terminate tractography tracing in the gray matter. The following 5 association pathways were segmented: the cingulum bundle, fornix, ILF, IFOF, and the arcuate fasciculus (AF). "
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    ABSTRACT: Little is known about the emergence of structural asymmetry of white matter tracts during early brain development. We examined whether and when asymmetry in diffusion parameters of limbic and association white matter pathways emerged in humans in 23 brains ranging from 15 gestational weeks (GW) up to 3 years of age (11 ex vivo and 12 in vivo cases) using high-angular resolution diffusion imaging tractography. Age-related development of laterality was not observed in a limbic connectional pathway (cingulum bundle or fornix). Among the studied cortico-cortical association pathways (inferior longitudinal fasciculus [ILF], inferior fronto-occipital fasciculus, and arcuate fasciculus), only the ILF showed development of age-related laterality emerging as early as the second trimester. Comparisons of ages older and younger than 40 GW revealed a leftward asymmetry in the cingulum bundle volume and a rightward asymmetry in apparent diffusion coefficient and leftward asymmetry in fractional anisotropy in the ILF in ages older than 40 GW. These results suggest that morphometric asymmetry in cortical areas precedes the emergence of white matter pathway asymmetry. Future correlative studies will investigate whether such asymmetry is anatomically/genetically driven or associated with functional stimulation.
    Full-text · Article · May 2014 · Cerebral Cortex
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    • "Cortical diffusion anisotropy has previously been observed in a number of DTI studies performed in the developing brain, including in the animal brain ex vivo [1]–[3], in the animal brain in vivo [4], [5], in the human brain ex vivo [6], [7], and in the human brain in vivo [8]–[11]. More recently, it has also been observed in high-resolution DTI studies performed in the adult brain, including in the macaque brain in vivo [12], in the human brain ex vivo [12]–[14], and in the human brain in vivo [12], [15]–[19]. "
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    ABSTRACT: Diffusion tensor imaging (DTI) is typically used to study white matter fiber pathways, but may also be valuable to assess the microstructure of cortical gray matter. Although cortical diffusion anisotropy has previously been observed in vivo, its cortical depth dependence has mostly been examined in high-resolution ex vivo studies. This study thus aims to investigate the cortical depth dependence of the diffusion anisotropy in the human cortex in vivo on a clinical 3 T scanner. Specifically, a novel multishot constant-density spiral DTI technique with inherent correction of motion-induced phase errors was used to achieve a high spatial resolution (0.625×0.625×3 mm) and high spatial fidelity with no scan time penalty. The results show: (i) a diffusion anisotropy in the cortical gray matter, with a primarily radial diffusion orientation, as observed in previous ex vivo and in vivo studies, and (ii) a cortical depth dependence of the fractional anisotropy, with consistently higher values in the middle cortical lamina than in the deep and superficial cortical laminae, as observed in previous ex vivo studies. These results, which are consistent across subjects, demonstrate the feasibility of this technique for investigating the cortical depth dependence of the diffusion anisotropy in the human cortex in vivo.
    Full-text · Article · Mar 2014 · PLoS ONE
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    • "Considering the recent advances on imaging microscopic myelin structure by DSI (Takahashi et al., 2010; Wedeen et al., 2012), the weaker structural connections that we found in low memory performance monkeys may indicate a largescale exhibition of myelin alterations resulting in a decrease of the flexibility in their hippocampal functional interactions. Similar aspect has been also confirmed in the studies on healthy cognitive aging in humans (Sullivan and Pfefferbaum 2006; Sullivan et al., 2010; Voineskos et al., 2012) and suggests that weakening or loss of structural connections may decrease the efficiency of the functional interactions, and therefore , result in lowered cognitive processes. "
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