Migration Pathways of Thalamic Neurons and Development of Thalamocortical Connections in Humans Revealed by Diffusion MR Tractography

Wilkinson, Molly; Kane, Tara; Wang, Rongpin; Takahashi, Emi

doi:10.1093/cercor/bhw339

Cited by 23 publications

(30 citation statements)

References 99 publications

(120 reference statements)

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“…The early wave of migrating neurons relay thamalo-cortical projections during late fetal and early preterm development, the thalamic nuclei may exhibit different maturational trajectories: the posterior limb of the internal capsule (which include the posterior thalamic radiations) appears to develop earlier than the anterior limb (including anterior thalamic pathways [56,57]). Given that prenatal development of thalamo-cortical connectivity appears to be the time during which the most significant macroscopic changes occur, as observed using dMRI [58], and that preterm infants exhibit reduced corticothalamic connectivity [59], this may partly explain the preterm-term differences in thalamic tier membership (i.e. preterm conditions impact the laterdeveloping pathways and thus a higher degree of connectivity -later maturation -for the thalamus in terms than preterms, where the phases of thalamocortical connectivity may be impeded by interruption of the developmental environment).…”

Section: Tier Analysismentioning

confidence: 99%

Hierarchical complexity of the macro-scale neonatal brain

Blesa

Galdi

Cox³

et al. 2020

Preprint

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The human adult structural connectome has a rich topology composed of nodal hierarchies containing highly diverse connectivity patterns, aligned to the diverse range of functional specialisations in the brain. The emergence of this hierarchical complexity in human development is unknown. Here, we substantiate the hierarchical tiers and complexity of brain networks in the newborn period, assess correspondences with hierarchical complexity in adulthood, and investigate the effect of preterm birth, a leading cause of neurocognitive impairment and atypical brain development, on hierarchical complexity. We report that the neonatal and adult structural connectomes are both composed of distinct hierarchical tiers. Consistency of ROIs is found at both ends of this hierarchy during early life and in adulthood, but significant differences are evident in intermediate tiers. The neonatal connectome is hierarchically complex in term born neonates, but hierarchically complexity is altered in association with preterm birth. This is mainly due to diversity of connectivity patterns in Tier 3, which is comprised of regions that underlie sensorimotor processing and its integration with cognitive information. For neonates and adults, the highest tier (comprising hub regions) is ordered, rather than complex, with more homogeneous connectivity patterns in structural hubs. This suggests that the brain develops first a more rigid hierarchical structure in hub regions allowing for the development of greater and more diverse functional specialisation in lower level regions, while connectivity underpinning this diversity is dysmature in infants born preterm.

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Section: Tier Analysismentioning

confidence: 99%

Hierarchical complexity of the macro-scale neonatal brain

Blesa

Galdi

Cox³

et al. 2020

Preprint

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“…HARDI theoretically allows reconstruction of complex crossing tissue coherence in the brain (Tuch et al, 2003 ) and even in immature fetal brains (e.g., Takahashi et al, 2012 ), which are typically more challenging to segment due to a surplus of unmyelinated pathways. Although, past diffusion tractography studies were able to detect overall patterns of trajectories of TC and CC pathways in adults and pediatric populations (Jaermann et al, 2008 ; Lebel et al, 2010 ; Vasung et al, 2011 ; Poh et al, 2015 ), and our past study successfully revealed potential neuronal migration pathways of thalamic neurons and TC development in fetal brains (Wilkinson et al, 2016 ), there has been no report that aimed to identify convergence of TC/CT pathways and convergence of TC/CC pathways in human fetuses.…”

Section: Introductionmentioning

confidence: 85%

“…We previously detected pathways likely linked to neuronal migration from the ventricular zone and GE to the thalami (Wilkinson et al, 2016 ). Between the ventricular zone and thalami, more tractography pathways were found in anterior compared to posterior regions, which was in agreement with postnatal observations that the anterior TC segment had a higher track count and volume than the posterior segment.…”

Section: Discussionmentioning

confidence: 99%

Convergence of Cortical, Thalamocortical, and Callosal Pathways during Human Fetal Development Revealed by Diffusion MRI Tractography

et al. 2017

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There has been evidence that during brain development, emerging thalamocortical (TC) and corticothalamic (CT) pathways converge in some brain regions and follow each other's trajectories to their final destinations. Corpus callosal (CC) pathways also emerge at a similar developmental stage, and are known to converge with TC pathways in specific cortical regions in mature brains. Given the functional relationships between TC and CC pathways, anatomical convergence of the two pathways are likely important for their functional integration. However, it is unknown (1) where TC and CT subcortically converge in the human brain, and (2) where TC and CC converge in the cortex of the human brain, due to the limitations of non-invasive methods. The goals of this study were to describe the spatio-temporal relationships in the development of the TC/CT and CC pathways in the human brain, using high-angular resolution diffusion MR imaging (HARDI) tractography. Emerging cortical, TC and CC pathways were identified in postmortem fetal brains ranging from 17 gestational weeks (GW) to 30 GW, as well as in vivo 34–40 GW newborns. Some pathways from the thalami were found to be converged with pathways from the cerebral cortex as early as 17 GW. Such convergence was observed mainly in anterior and middle regions of the brain until 21 GW. At 22 GW and onwards, posterior pathways from the thalami also converged with cortical pathways. Many CC pathways reached the full length up to the cortical surface as early as 17 GW, while pathways linked to thalami (not only TC axons but also including pathways linked to thalamic neuronal migration) reached the cortical surface at and after 20 GW. These results suggest that CC pathways developed earlier than the TC pathways. The two pathways were widespread at early stages, but by 40 GW they condensed and formed groups of pathways that projected to specific regions of the cortex and overlapped in some brain regions. These results suggest that HARDI tractography has the potential to identify developing TC/CT and CC pathways with the timing and location of their convergence in fetal stages persisting in postnatal development.

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“…In the late second and third trimesters of gestation, the thalamus quadruples in size as the majority of the thalamocortical connections are established (3,4). This accelerated rate of growth and rapidly developing connectivity renders the thalamus vulnerable to injury in the prenatal period (5,6).…”

Section: Introductionmentioning

confidence: 99%

“…thalamocortical connections are established. 3,4 This accelerated rate of growth and rapidly developing connectivity renders the thalamus vulnerable to injury in the prenatal period. 5,6 A growing body of evidence supports the vulnerability of the thalamus in this time period, including recent reports of decreased thalamic volume and thalamocortical connectivity in neonates born preterm.…”

mentioning

confidence: 99%