Transient compartmentalization and accelerated volume growth coincide with the expected development of cortical afferents in the human neostriatum.

Ivica Kostović, Domagoj Džaja, Marina Raguž, Janja Kopić, Andrea Blažević, Željka Krsnik

Cerebral cortex (New York, N.Y. : 1991) 2022 Dec 20

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The neostriatum plays a central role in cortico-subcortical circuitry underlying goal-directed behavior. The adult mammalian neostriatum shows chemical and cytoarchitectonic compartmentalization in line with the connectivity. However, it is poorly understood how and when fetal compartmentalization (AChE-rich islands, nonreactive matrix) switches to adult (AChE-poor striosomes, reactive matrix) and how this relates to the ingrowth of corticostriatal afferents. Here, we analyze neostriatal compartments on postmortem human brains from 9 postconceptional week (PCW) to 18 postnatal months (PM), using Nissl staining, histochemical techniques (AChE, PAS-Alcian), immunohistochemistry, stereology, and comparing data with volume-growth of in vivo and in vitro MRI. We find that compartmentalization (C) follows a two-compartment (2-C) pattern around 10PCW and is transformed into a midgestational labyrinth-like 3-C pattern (patches, AChE-nonreactive perimeters, matrix), peaking between 22 and 28PCW during accelerated volume-growth. Finally, compartmentalization resolves perinatally, by the decrease in transient "AChE-clumping," disappearance of AChE-nonreactive, ECM-rich perimeters, and an increase in matrix reactivity. The initial "mature" pattern appears around 9 PM. Therefore, transient, a 3-C pattern and accelerated neostriatal growth coincide with the expected timing of the nonhomogeneous distribution of corticostriatal afferents. The decrease in growth-related AChE activity and transfiguration of corticostriatal terminals are putative mechanisms underlying fetal compartments reorganization. Our findings serve as normative for studying neurodevelopmental disorders. © The Author(s) 2022. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

Citation

Ivica Kostović, Domagoj Džaja, Marina Raguž, Janja Kopić, Andrea Blažević, Željka Krsnik. Transient compartmentalization and accelerated volume growth coincide with the expected development of cortical afferents in the human neostriatum. Cerebral cortex (New York, N.Y. : 1991). 2022 Dec 20;33(2):434-457