Interactive histogenesis of axonal strata and proliferative zones in the human fetal cerebral wall

Išasegi, Iris Žunić; Krsnik, Željka; Radoš, Marko; Benjak, Vesna; Kostović, Ivica

doi:10.1007/s00429-018-1721-2

Cited by 42 publications

(46 citation statements)

References 122 publications

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“…D,E; see Žunić Išasegi et al. ). Synaptophysin reactivity just below the CP in the presubplate layer (see Kostović & Rakić, ) appears as a darker band at low magnification (Fig.…”

Section: Resultsmentioning

confidence: 90%

“…; Žunić Išasegi et al. ). In this period, PAS‐Alcian staining showed a spread of activity throughout the SP across the hemisphere (Fig.…”

Section: Resultsmentioning

confidence: 98%

“…Synaptic markers are expressed in SVZ, IZ, the multilaminar axonal cellular compartment (MACC; Žunić Išasegi et al. ) and the deep transforming SP. ECM markers of NCAN showed increased immunoreactivity in the deep (lower) SP (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…We viewed this fibrillar band as a marker of developing cortico‐cortical fibers (Žunić Išasegi et al. ). Stensaas Golgi‐impregnated sections revealed a presence of postmigratory multipolar neurons with a relatively mature dendritic arborization and predominantly random orientation of the associated main soma‐dendritic three axes.…”

Section: Resultsmentioning

confidence: 99%

“…It is interesting to note that the moderately expressed ‘bin’ is present in the MACC, which is composed of fibers in the sagittal strata (former IZ), and disperses the outer SVZ (Žunić Išasegi et al. ).…”

Section: Resultsmentioning

confidence: 99%

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Sublaminar organization of the human subplate: developmental changes in the distribution of neurons, glia, growing axons and extracellular matrix

2018

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The objective of this paper was to collect normative data essential for analyzing the subplate (SP) role in pathogenesis of developmental disorders, characterized by abnormal circuitry, such as hypoxic-ischemic lesions, autism and schizophrenia. The main cytological features of the SP, such as low cell density, early differentiation of neurons and glia, plexiform arrangement of axons and dendrites, presence of synapses and a large amount of extracellular matrix (ECM) distinguish this compartment from the cell-dense cortical plate (CP; towards pia) and large fiber bundles of external axonal strata of fetal white matter (towards ventricle). For SP delineation from these adjacent layers based on combined cytological criteria, we analyzed the sublaminar distribution of different microstructural elements and the associated maturational gradients throughout development, using immunocytochemical and histological techniques on postmortem brain material (Zagreb Neuroembryological Collection). The analysis revealed that the SP compartment of the lateral neocortex shows changes in laminar organization throughout fetal development: the monolayer in the early fetal period (presubplate) undergoes dramatic bilaminar transformation between 13 and 15 postconceptional weeks (PCW), followed by subtle sublamination in three 'floors' (deep, intermediate, superficial) of midgestation (15-21 PCW). During the stationary phase (22-28 PCW), SP persists as a trilaminar compartment, gradually losing its sublaminar organization towards the end of gestation and remains as a single layer of SP remnant in the newborn brain. Based on these sublaminar transformations, we have documented developmental changes in the distribution, maturational gradients and expression of molecular markers in SP synapses, transitional forms of astroglia, neurons and ECM, which occur concomitantly with the ingrowth of thalamo-cortical, basal forebrain and corticocortical axons in a deep to superficial fashion. The deep SP is the zone of ingrowing axons -'entrance (ingrowth) zone'. The process of axonal ingrowth begins with thalamo-cortical fibers and basal forebrain afferents, indicating an oblique geometry. During the later fetal period, deep SP receives long cortico-cortical axons exhibiting a tangential geometry. Intermediate SP ('proper') is the navigation and 'nexus' sublamina consisting of a plexiform arrangement of cellular elements providing guidance and substrate for axonal growth, and also containing transient connectivity of dendrites and axons in a tangential plane without radial boundaries immersed in an ECM-rich continuum. Superficial SP is the axonal accumulation ('waiting compartment') and target selection zone, indicating a dense distribution of synaptic markers, accumulation of thalamo-cortical axons (around 20 PCW), overlapping with dendrites from layer VI neurons. In the late preterm brain period, superficial SP contains a chondroitin sulfate non-immunoreactive band. The developmental dynamics for the distribution of neuronal, glial and ECM marker...

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“…D,E; see Žunić Išasegi et al. ). Synaptophysin reactivity just below the CP in the presubplate layer (see Kostović & Rakić, ) appears as a darker band at low magnification (Fig.…”

Section: Resultsmentioning

confidence: 90%

“…; Žunić Išasegi et al. ). In this period, PAS‐Alcian staining showed a spread of activity throughout the SP across the hemisphere (Fig.…”

Section: Resultsmentioning

confidence: 98%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

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Sublaminar organization of the human subplate: developmental changes in the distribution of neurons, glia, growing axons and extracellular matrix

2018

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Prenatal development of the human entorhinal cortex

Šimić

Krsnik

Knezović

et al. 2022

J of Comparative Neurology

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Little is known about the development of the human entorhinal cortex (EC), a major hub in a widespread network for learning and memory, spatial navigation, high‐order processing of object information, multimodal integration, attention and awareness, emotion, motivation, and perception of time. We analyzed a series of 20 fetal and two adult human brains using Nissl stain, acetylcholinesterase (AChE) histochemistry, and immunocytochemistry for myelin basic protein (MBP), neuronal nuclei antigen (NeuN), a pan‐axonal neurofilament marker, and synaptophysin, as well as postmortem 3T MRI. In comparison with other parts of the cerebral cortex, the cytoarchitectural differentiation of the EC begins remarkably early, in the 10th week of gestation (w.g.). The differentiation occurs in a superficial magnocellular layer in the deep part of the marginal zone, accompanied by cortical plate (CP) condensation and multilayering of the deep part of CP. These processes last until the 13–14th w.g. At 14 w.g., the superficial lamina dissecans (LD) is visible, which divides the CP into the lamina principalis externa (LPE) and interna (LPI). Simultaneously, the rostral LPE separates into vertical cell‐dense islands, whereas in the LPI, the deep LD emerges as a clear acellular layer. In the 16th w.g., the LPE remodels into vertical cell‐dense and cell‐sparse zones with a caudorostral gradient. At 20 w.g., NeuN immunoreactivity is most pronounced in the islands of layer II cells, whereas migration and differentiation inside‐out gradients are seen simultaneously in both the upper (LPE) and the lower (LPI) pyramidal layers. At this stage, the EC adopts for the first time an adult‐like cytoarchitectural organization, the superficial LD becomes discernible by 3T MRI, MBP‐expressing oligodendrocytes first appear in the fimbria and the perforant path (PP) penetrates the subiculum to reach its molecular layer and travels along through the Cornu Ammonis fields to reach the suprapyramidal blade of the dentate gyrus, whereas the entorhinal‐dentate branch perforates the hippocampal sulcus about 2–3 weeks later. The first AChE reactivity appears as longitudinal stripes at 23 w.g. in layers I and II of the rostrolateral EC and then also as AChE‐positive in‐growing fibers in islands of superficial layer III and layer II neurons. At 40 w.g., myelination of the PP starts as patchy MBP‐immunoreactive oligodendrocytes and their processes. Our results refute the possibility of an inside‐out pattern of the EC development and support the key role of layer II prospective stellate cells in the EC lamination. As the early cytoarchitectural differentiation of the EC is paralleled by the neurochemical development, these developmental milestones in EC structure and connectivity have implications for understanding its normal function, including its puzzling modular organization and potential contribution to consciousness content (awareness), as well as for its insufficiently explored deficits in developmental, psychiatric, and degenerative brain disorders.

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Is there a consensus on the location and composition of the human subplate?

Clowry

2024

J of Comparative Neurology

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Interactive histogenesis of axonal strata and proliferative zones in the human fetal cerebral wall

Cited by 42 publications

References 122 publications

Sublaminar organization of the human subplate: developmental changes in the distribution of neurons, glia, growing axons and extracellular matrix

Sublaminar organization of the human subplate: developmental changes in the distribution of neurons, glia, growing axons and extracellular matrix

Prenatal development of the human entorhinal cortex

Is there a consensus on the location and composition of the human subplate?

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