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Fetal functional imaging portrays heterogeneous development of emerging human brain networks.

ABSTRACT: The functional connectivity architecture of the adult human brain enables complex cognitive processes, and exhibits a remarkably complex structure shared across individuals. We are only beginning to understand its heterogeneous structure, ranging from a strongly hierarchical organization in sensorimotor areas to widely distributed networks in areas such as the parieto-frontal cortex. Our study relied on the functional magnetic resonance imaging (fMRI) data of 32 fetuses with no detectable morphological abnormalities. After adapting functional magnetic resonance acquisition, motion correction, and nuisance signal reduction procedures of resting-state functional data analysis to fetuses, we extracted neural activity information for major cortical and subcortical structures. Resting fMRI networks were observed for increasing regional functional connectivity from 21st to 38th gestational weeks (GWs) with a network-based statistical inference approach. The overall connectivity network, short range, and interhemispheric connections showed sigmoid expansion curve peaking at the 26-29 GW. In contrast, long-range connections exhibited linear increase with no periods of peaking development. Region-specific increase of functional signal synchrony followed a sequence of occipital (peak: 24.8 GW), temporal (peak: 26 GW), frontal (peak: 26.4 GW), and parietal expansion (peak: 27.5 GW). We successfully adapted functional neuroimaging and image post-processing approaches to correlate macroscopical scale activations in the fetal brain with gestational age. This in vivo study reflects the fact that the mid-fetal period hosts events that cause the architecture of the brain circuitry to mature, which presumably manifests in increasing strength of intra- and interhemispheric functional macro connectivity.

SUBMITTER: Jakab A

PROVIDER: S-EPMC4205819 | biostudies-other | 2014

REPOSITORIES: biostudies-other

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Fetal functional imaging portrays heterogeneous development of emerging human brain networks.

Jakab András A Schwartz Ernst E Kasprian Gregor G Gruber Gerlinde M GM Prayer Daniela D Schöpf Veronika V Langs Georg G

Frontiers in human neuroscience 20141022

The functional connectivity architecture of the adult human brain enables complex cognitive processes, and exhibits a remarkably complex structure shared across individuals. We are only beginning to understand its heterogeneous structure, ranging from a strongly hierarchical organization in sensorimotor areas to widely distributed networks in areas such as the parieto-frontal cortex. Our study relied on the functional magnetic resonance imaging (fMRI) data of 32 fetuses with no detectable morpho ...[more]

PMID: 25374531

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Project description:Previous studies on brain functional connectivity networks in children have mainly focused on changes in function in specific brain regions, as opposed to whole brain connectivity in healthy children. By analyzing the independent components of activation and network connectivity between brain regions, we examined brain activity status and development trends in children aged 3 and 5 years. These data could provide a reference for brain function rehabilitation in children with illness or abnormal function. We acquired functional magnetic resonance images from 15 3-year-old children and 15 5-year-old children under natural sleep conditions. The participants were recruited from five kindergartens in the Nanshan District of Shenzhen City, China. The parents of the participants signed an informed consent form with the premise that they had been fully informed regarding the experimental protocol. We used masked independent component analysis and BrainNet Viewer software to explore the independent components of the brain and correlation connections between brain regions. We identified seven independent components in the two groups of children, including the executive control network, the dorsal attention network, the default mode network, the left frontoparietal network, the right frontoparietal network, the salience network, and the motor network. In the default mode network, the posterior cingulate cortex, medial frontal gyrus, and inferior parietal lobule were activated in both 3- and 5-year-old children, supporting the "three-brain region theory" of the default mode network. In the frontoparietal network, the frontal and parietal gyri were activated in the two groups of children, and functional connectivity was strengthened in 5-year-olds compared with 3-year-olds, although the nodes and network connections were not yet mature. The high-correlation network connections in the default mode networks and dorsal attention networks had been significantly strengthened in 5-year-olds vs. 3-year-olds. Further, the salience network in the 3-year-old children included an activated insula/inferior frontal gyrus-anterior cingulate cortex network circuit and an activated thalamus-parahippocampal-posterior cingulate cortex-subcortical regions network circuit. By the age of 5 years, nodes and high-correlation network connections (edges) were reduced in the salience network. Overall, activation of the dorsal attention network, default mode network, left frontoparietal network, and right frontoparietal network increased (the volume of activation increased, the signals strengthened, and the high-correlation connections increased and strengthened) in 5-year-olds compared with 3-year-olds, but activation in some brain nodes weakened or disappeared in the salience network, and the network connections (edges) were reduced. Between the ages of 3 and 5 years, we observed a tendency for function in some brain regions to be strengthened and for the generalization of activation to be reduced, indicating that specialization begins to develop at this time. The study protocol was approved by the local ethics committee of the Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences in China with approval No. SIAT-IRB-131115-H0075 on November 15, 2013.

Project description:Complicated molecular and cellular processes take place in a spatiotemporally heterogeneous and precisely regulated pattern in the human fetal brain, yielding not only dramatic morphological and microstructural changes, but also macroscale connectomic transitions. As the underlying substrate of the fetal brain structural network, both dynamic neuronal migration pathways and rapid developing fetal white matter (WM) fibers could fundamentally reshape early fetal brain connectome. Quantifying structural connectome development can not only shed light on the brain reconfiguration in this critical yet rarely studied developmental period, but also reveal alterations of the connectome under neuropathological conditions. However, transition of the structural connectome from the mid-fetal stage to birth is not yet known. The contribution of different types of neural fibers to the structural network in the mid-fetal brain is not known, either. In this study, diffusion tensor magnetic resonance imaging (DT-MRI or DTI) of 10 fetal brain specimens at the age of 20 postmenstrual weeks (PMW), 12 in vivo brains at 35 PMW, and 12 in vivo brains at term (40 PMW) were acquired. The structural connectome of each brain was established with evenly parcellated cortical regions as network nodes and traced fiber pathways based on DTI tractography as network edges. Two groups of fibers were categorized based on the fiber terminal locations in the cerebral wall in the 20 PMW fetal brains. We found that fetal brain networks become stronger and more efficient during 20-40 PMW. Furthermore, network strength and global efficiency increase more rapidly during 20-35 PMW than during 35-40 PMW. Visualization of the whole brain fiber distribution by the lengths suggested that the network reconfiguration in this developmental period could be associated with a significant increase of major long association WM fibers. In addition, non-WM neural fibers could be a major contributor to the structural network configuration at 20 PMW and small-world network organization could exist as early as 20 PMW. These findings offer a preliminary record of the fetal brain structural connectome maturation from the middle fetal stage to birth and reveal the critical role of non-WM neural fibers in structural network configuration in the middle fetal stage.

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Fetal functional imaging portrays heterogeneous development of emerging human brain networks.

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Fetal functional imaging portrays heterogeneous development of emerging human brain networks.

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