Development of the basic architecture of neocortical circuitry in the human fetus as revealed by the coupling spatiotemporal pattern of synaptogenesis along with microstructure and macroscale in vivo MR imaging

Scientific paper - Review paper

• Author: Ivica Kostović
• Author's institution: University of Zagreb; School of Medicine; (Croatian Institiute for Brain Research)
• Scientific / art field, discipline and subdiscipline: BIOMEDICINE AND HEALTHCARE; Basic Medical Sciences; Neuroscience

Abstract (english)

In humans, a quantifiable number of cortical synapses appears early in fetal life. In this paper, we present a bridge across different scales of resolution and the distribution of synapses across the transient cytoarchitectonic compartments: marginal zone (MZ), cortical plate (CP), subplate (SP), and in vivo MR images. The tissue of somatosensory cortex (7–26 postconceptional weeks (PCW)) was prepared for electron microscopy, and classified synapses with a determined subpial depth were used for creating histograms matched to the histological sections immunoreacted for synaptic markers and aligned to in vivo MR images (1.5 T) of corresponding fetal ages (maternal indication). Two time periods and laminar patterns of synaptogenesis were identified: an early and midfetal two-compartmental distribution (MZ and SP) and a late fetal three-compartmental distribution (CP synaptogenesis). During both periods, a voluminous, synapse-rich SP was visualized on the in vivo MR. Another novel finding concerns the phase of secondary expansion of the SP (13 PCW), where a quantifiable number of synapses appears in the upper SP. This lamina shows a T2 intermediate signal intensity below the low signal CP. In conclusion, the early fetal appearance of synapses shows early differentiation of putative genetic mechanisms underlying the synthesis, transport and assembly of synaptic proteins. “Pioneering” synapses are likely to play a morphogenetic role in constructing of fundamental circuitry architecture due to interaction between neurons. They underlie spontaneous, evoked, and resting state activity prior to ex utero experience. Synapses can also mediate genetic and environmental triggers, adversely altering the development of cortical circuitry and leading to neurodevelopmental disorders.

• Keywords (english): Female; Fetus; Humans; Magnetic Resonance Imaging; Neocortex / cytology; Neocortex / embryology; Neurogenesis / physiology; Somatosensory Cortex / cytology; Somatosensory Cortex / diagnostic imaging; Somatosensory Cortex / growth & development; Synapses / physiology; Synapses / ultrastructure
• Language: english
• Publication type: Scientific paper - Review paper
• Publication status: Published
• Peer review: Peer review
• Publication version: Published version
• Journal title: Brain Structure and Function
• Numbering: vol. 229, no. 9, pp. 2339-2367
• e-ISSN: 1863-2661
• DOI: https://doi.org/10.1007/s00429-024-02838-9
• URN:NBN: urn:nbn:hr:105:913950
• Publication: 2024-08-05
• Project: Number: IP-2024-05-7157; Title (croatian): Ljudski prenatalni cerebralni neksus: neistražen prostorno-vremenski višerazmjerni kompartmentalni translacijski pristup; Title (english): Human prenatal cerebral nexus: uncharted spatiotemporal multiscale compartmental translational approach; Acronym: HUMANCOMPARTMENTOME; Leader: Ivica Kostović; Jurisdiction: Croatia; Funding stream: Research Projects
• Document URL: https://link.springer.com/10.1007/s00429-024-02838-9
• Type of resource: Text
• Access conditions: Open access
• Created on: 2025-04-01 08:24:28