Developmental Changes in Diffusion Anisotropy Coincide with Immature Oligodendrocyte Progression and Maturation of Compound Action Potential

Drobyshevsky, Alexander; Song, Sheng; Gamkrelidze, Georgi; Wyrwicz, Alice M.; Derrick, Matthew; Meng, Fan Gang; Liu, Limin; Ji, Xinhai; Trommer, Barbara L.; Beardsley, Douglas J.; Luo, Ning; Back, Stephen A.; Tan, Sidhartha

doi:10.1523/jneurosci.4983-04.2005

Cited by 182 publications

(168 citation statements)

References 37 publications

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“…It is likely that the relative increases in tract count seen between certain region-pairs is primarily due oligodendrocyte maturation [16]. Myelin sheath maturation begins as early as 30 weeks but does not occur simultaneously throughout the brain, instead propagating up the corticospinal tracts and outwards, affecting major fiber bundles first [33].…”

Section: Discussionmentioning

confidence: 99%

Structural network analysis of brain development in young preterm neonates

et al. 2014

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Preterm infants develop differently than those born at term and are at higher risk of brain pathology. Thus, an understanding of their development is of particular importance. Diffusion tensor imaging (DTI) of preterm infants offers a window into brain development at a very early age, an age at which that development is not yet fully understood. Recent works have used DTI to analyze structural connectome of the brain scans using network analysis. These studies have shown that, even from infancy, the brain exhibits small-world properties. Here we examine a cohort of 47 normal preterm neonates (i.e., without brain injury and with normal neurodevelopment at 18 months of age) scanned between 27 and 45 weeks post-menstrual age to further the understanding of how the structural connectome develops. We use fullbrain tractography to find white matter tracts between the 90 cortical and sub-cortical regions defined in the University of North Carolina Chapel Hill neonatal atlas. We then analyze the resulting connectomes and explore the differences between weighting edges by tract count versus fractional anisotropy. We observe that the brain networks in preterm infants, much like infants born at term, show high efficiency and clustering measures across a range of network scales. Further, the development of many individual region-pair connections, particularly in the frontal and occipital lobes, is significantly correlated with age. Finally, we observe that the preterm infant connectome remains highly efficient yet becomes more clustered across this age range, leading to a significant increase in its small-world structure.

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Section: Discussionmentioning

confidence: 99%

Structural network analysis of brain development in young preterm neonates

et al. 2014

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“…Under this hypothesis, infants born with Canavan disease are normal at birth because ASPA activity is not critical until myelin synthesis is dramatically increased shortly after birth. The maturation of oligodendrocytes and the myelination of axons in the brain accelerates shortly after birth (Drobyshevsky et al, 2005). Therefore, the increase in expression of ASPA that parallels myelination in early development (D'Adamo, Jr.…”

Section: Naa Breakdown and Myelin Lipid Synthesismentioning

confidence: 99%

N-Acetylaspartate in the CNS: From neurodiagnostics to neurobiology

Moffett

Ross

Arun

et al. 2007

Progress in Neurobiology

1,229

1,126

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The brain is unique among organs in many respects, including its mechanisms of lipid synthesis and energy production. The nervous system-specific metabolite N-acetylaspartate (NAA), which is synthesized from aspartate and acetyl-coenzyme A in neurons, appears to be a key link in these distinct biochemical features of CNS metabolism. During early postnatal CNS development, the expression of lipogenic enzymes in oligodendrocytes, including the NAA-degrading enzyme aspartoacylase (ASPA), is increased along with increased NAA production in neurons. NAA is transported from neurons to the cytoplasm of oligodendrocytes, where ASPA cleaves the acetate moiety for use in fatty acid and steroid synthesis. The fatty acids and steroids produced then go on to be used as building blocks for myelin lipid synthesis. Mutations in the gene for ASPA result in the fatal leukodystrophy Canavan disease, for which there is currently no effective treatment. Once postnatal myelination is completed, NAA may continue to be involved in myelin lipid turnover in adults, but it also appears to adopt other roles, including a bioenergetic role in neuronal mitochondria. NAA and ATP metabolism appear to be linked indirectly, whereby acetylation of aspartate may facilitate its removal from neuronal mitochondria, thus favoring conversion of glutamate to alpha ketoglutarate which can enter the tricarboxylic acid cycle for energy production. In its role as a mechanism for enhancing mitochondrial energy production from glutamate, NAA is in a key position to act as a magnetic resonance spectroscopy marker for neuronal health, viability and number. Evidence suggests that NAA is a direct precursor for the enzymatic synthesis of the neuron specific dipeptide N-acetylaspartylglutamate, the most concentrated neuropeptide in the human brain. Other proposed roles for NAA include neuronal osmoregulation and axon-glial signaling. We propose that NAA may also be involved in brain nitrogen balance. Further research will be required to more fully understand the biochemical functions served by NAA in CNS development and activity, and additional functions are likely to be discovered.

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“…When changes in fractional anisotropy were noted, we determined whether this difference was primarily associated with changes in axial diffusivity (λ 1 ; the diffusion of water parallel to the primary direction of the tracts) or radial diffusivity (water diffusion perpendicular to the tracts [(λ 2 + λ 3 )/2]). As brain white matter matures, mean diffusivity decreases and fractional anisotropy increases due to a decrease in radial diffusivity reflecting the maturation of the oligodendrocyte lineage and early myelination [23,33]. Inter-rater and intra-rater reliability of DTT were very high as assessed on 20 randomly selected scans, using intraclass correlation and BlandAltman limits of agreement [34](see Supplemental Table 1).…”

Section: Magnetic Resonance and Diffusion Tensor Imagingmentioning

confidence: 99%

“…Higher SNAP-II was associated with lower fractional anisotropy of the corticospinal tract over time, even after adjusting postnatal adversities. Lower fractional anisotropy was related to lesser changes in radial diffusivity, which suggests that very early illness severity may interfere with maturation of the oligodendrocyte lineage or early events of myelination of the corticospinal tract [23,33]. SNAP-II was initially developed to predict mortality of infants admitted to neonatal intensive care units [14].…”

Section: Snap-ii Predicts Microstructural Development Of the Corticosmentioning

confidence: 99%

Score for Neonatal Acute Physiology–II and Neonatal Pain Predict Corticospinal Tract Development in Premature Newborns

Zwicker¹,

Grunau²,

Adams³

et al. 2013

Pediatric Neurology

116

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Premature infants are at risk for adverse motor outcomes, including cerebral palsy and developmental coordination disorder. The purpose of this study was to examine the relationship of ante-, peri-, and postnatal risk factors for abnormal development of the corticospinal tract, the major voluntary motor pathway, during the neonatal period. In a prospective cohort study, 126 premature neonates (24-32 weeks gestational age) underwent serial brain imaging near birth and at term-equivalent age. Using diffusion tensor tractography, mean diffusivity and fractional anisotropy of the corticospinal tract were measured to reflect microstructural development. Generalized estimating equation models examined associations of risk factors on corticospinal tract development.The perinatal risk factor of greater early illness severity [as measured by the Score for Neonatal Acute Physiology-II (SNAP-II)] was associated with a slower rise in fractional anisotropy of the corticospinal tract (p=0.02), even after correcting for gestational age at birth and postnatal risk factors (p=0.009). Consistent with previous findings, neonatal pain adjusted for morphine and postnatal infection were also associated with a slower rise in fractional anisotropy of the corticospinal tract (p=0.03 and 0.02 respectively). Lessening illness severity in the first hours of life might offer potential to improve motor pathway development in premature newborns.

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Developmental Changes in Diffusion Anisotropy Coincide with Immature Oligodendrocyte Progression and Maturation of Compound Action Potential

Cited by 182 publications

References 37 publications

Structural network analysis of brain development in young preterm neonates

Structural network analysis of brain development in young preterm neonates

N-Acetylaspartate in the CNS: From neurodiagnostics to neurobiology

Score for Neonatal Acute Physiology–II and Neonatal Pain Predict Corticospinal Tract Development in Premature Newborns

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