Cytology and time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon

Abstract

The fine structure, synaptic relationships, distribution and time of origin of interstitial neurons situated within the white matter subjacent to the visual, somatosensory and motor cortices were studied in the human and monkey telencephalon. The analysis was carried out on Nissl-stained serial sections, rapid Golgi impregnations, by acetylcholinesterase (AChE) histochemistry, electron microscopy and [3H]thymidine ([3H]TdR) autoradiography. Interstitial neurons have a similar distribution, morphology and histochemistry in both human and monkey telencephalon. Their highest density and the most extensive distribution is found in the neonatal period in both species. The number of interstitial neurons decreases during infancy, but numerous cells remain in the adult. Two types of interstitial neuron can be recognized in Golgi preparations: polymorphic cells, usually situated close to the cortex and fusiform cells, located predominantly in the depths of the white matter. The polymorphic cell type is prevalent during neonatal and infant stages, while fusiform cells are relatively more numerous in the adult. Interstitial cells have ultrastructural features and organelles typical of neurons of the central nervous system with well-defined axosomatic and axodendritic synapses of both symmetrical and asymmetrical types. About 20% fo the interstitial cells show strong specific AChE activity. Autoradiographic analysis of postnatal monkeys exposed to [3H]TdR at various embryonic (E) and early postnatal days indicates that interstitial neurons which lie beneath the visual and somatosensory-motor cortices are generated between E38 and E48. Contrary to the prevailing notion that interstitial neurons are the latest generated cells arreste during migration across the maturing white matter, they prove to be produced at the end of the first third of the 165-day gestation in the rhesus monkey concomitantly with the generation of neurons destined for the deep neocortical layers. These findings raise the possibility that interstitial cells represent a vestige of the transient embryonic subplate layer.

Interstitial white matter neurons express less reelin and are abnormally distributed in schizophrenia: towards an integration of molecular and morphologic aspects of the neurodevelopmental hypothesis

“…12,13,[17][18][19][20]27 We also confirmed the marked gradient in the distribution of the neurons, with the highest density being seen in the most superficial part of the white matter (Figure 1b).…”

“…The two populations differ in terms of their predominant morphology and gradient of decline during postnatal development. 12,13 They also differ in their connectivity, with superficial IWMNs forming more extensive connections with neurons in the overlying grey matter. 26 It may also be relevant that superficial IWMNs lie embedded within the corticocortical association fibres (or U-fibres), which run in the white matter immediately below layer VI, whereas, at least in the rodent, callosal fibres travel in the middle portion and corticofugal axons predominate in the deep white matter.…”

“…Firstly, the finding of aberrantly located neurons, especially interstitial white matter neurons (IWMNs). These are thought to represent the relatively few adult remnants of the cortical subplate, 11,12 a structure which is formed early in the second trimester, 13 and which plays a key role in cortical development, including neuronal migration, lamination, columnarity and formation of corticothalamic and thalamocortical connections. 14,15 IWMN abnormalities in schizophrenia have been reported in the dorsolateral prefrontal, [16][17][18] middle and medial temporal 19 and inferior parietal 20 cortices, and interpreted as reflecting aberrant migration or increased survival of the subplate neurons.…”

The emergence of functional architecture during early brain development

“…Similar to the adult connectome, the neonatal brain has repeatedly been found to display short characteristic path length, which is computed as the average number of edges that need to be Schematic overview based on findings by (Alcauter et al, 2014;Bystron et al, 2008;Gao et al, 2011;Innocenti and Price, 2005;Kostovic et al, 2014;Kostovic and Rakic, 1980;Kostovic and Vasung, 2009;Shankle et al, 1999;Stiles and Jernigan, 2010;Thomason et al, 2013Thomason et al, , 2015Vanhatalo and Kaila, 2006;Vasung et al, 2010) (Huang et al, 2009;Kostovic and Jovanov-Milosevic, 2006;Takahashi et al, 2012;Vasung et al, 2010). (Doria et al, 2010a;Gao et al, 2014a;Smyser et al, 2010;Thomason et al, 2015).…”

Extrapolating brain development from experimental species to humans

“…The result is a variety of data obtained in species born at a wide range of developmental stages and maturing at different rates, but with little explicit agreement or common understanding on how to relate them to humans. For example, how might we best study the effects of toxins on the crucial first-generated cortical cells (subplate cells) when initial studies describing these cells were done in macaques (Kostovic and Rakic, 1980), later studies used cats (Chun and Shatz, 1989;Ghosh et al, 1990), rats (Bayer and Altman, 1990) and hamsters (Miller et al, 1993;Woo and Finlay, 1996), and future studies are likely to be accomplished in mice?…”