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Review
. 2010 Oct;217(4):344-67.
doi: 10.1111/j.1469-7580.2010.01283.x.

Early History of Subplate and Interstitial Neurons: From Theodor Meynert (1867) to the Discovery of the Subplate Zone (1974)

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Free PMC article
Review

Early History of Subplate and Interstitial Neurons: From Theodor Meynert (1867) to the Discovery of the Subplate Zone (1974)

Miloš Judaš et al. J Anat. .
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Abstract

In this historical review, we trace the early history of research on the fetal subplate zone, subplate neurons and interstitial neurons in the white matter of the adult nervous system. We arrive at several general conclusions. First, a century of research clearly testifies that interstitial neurons, subplate neurons and the subplate zone were first observed and variously described in the human brain - or, in more general terms, in large brains of gyrencephalic mammals, characterized by an abundant white matter and slow and protracted prenatal and postnatal development. Secondly, the subplate zone cannot be meaningfully defined using a single criterion - be it a specific population of cells, fibres or a specific molecular or genetic marker. The subplate zone is a highly dynamic architectonic compartment and its size and cellular composition do not remain constant during development. Thirdly, it is important to make a clear distinction between the subplate zone and the subplate (and interstitial) neurons. The transient existence of the subplate zone (as a specific architectonic compartment of the fetal telencephalic wall) should not be equated with the putative transient existence of subplate neurons. It is clear that in rodents, and to an even greater extent in humans and monkeys, a significant number of subplate cells survive and remain functional throughout life.

Figures

Fig. 1
Fig. 1
Meynert was first to describe neurons in the adult subcortical white matter, and Ramón y Cajal introduced the term interstitial cells in neurohistology. Neurons (red) in the subcortical white matter of the human brain (A – frontal, B – primary visual cortex) were first described by Theodor Meynert in 1867 (here reproduced from Meynert, 1884, pp. 53 and 63). However, the term interstitial cells was initially (1891–93) applied by Ramón y Cajal to describe a special type of visceral sympathetic neurons in glands and the enteric system of the gut (C–,E – here reproduced from Ramón y Cajal, 1911, pp. 924–927; (C,D) interstitial cells in Auerbach's plexus and muscular layer of the rabbit intestine, stained by methylene blue; (E) interstitial cells among muscle fibres of the guinea-pig intestine, stained by rapid Golgi method). Cajal in 1896 also described neurons in the cerebellar white matter as interstitial cells (G –Ramón y Cajal, 1896, p. 24, fig. 5b), but it should be noted that these cells were first described by Gustav Retzius (F –Retzius, 1892, fig. 4 of Plate XIX). For details, see text.
Fig. 5
Fig. 5
Von Economo & Koskinas realized that the upper intermediate zone gives rise to layer VIb and interstitial neurons in the adult human brain. Laminar development of the telencephalic wall from the stage of ependymal primordium (A, ependymären Anlage, 5th fetal week) to the completed development of the cortical plate (Pyramidenschicht) during the 5th fetal month (F), according to Von Economo & Koskinas (1925, pp. 88–89, Figs 47–52). (A–C) Sequential development of ventricular zone (M), marginal zone (RS) and intermediate zone (Z) from 5–7 weeks of gestation. (D) The appearance of the cortical plate (Py) during the 8th week of gestation. (E) During the 3rd fetal month, the cortical plate (Py) is well developed, and the intermediate zone becomes divided into an inner part (Z – fetal white matter) and an outer or upper part (Z’), which represents the transition towards the cortical plate and itself contributes to the formation of the future cortex (i.e. Z’ is future layer VIb). (F) All layers of the fetal telencephalic wall are much thicker and better developed during the 5th fetal month, but the basic arrangement is the same as in 3rd month. Z and Z’’ will transform into the deep white matter, and Z’ will transform into layer VIb and gyral white matter. le, li, external and internal limiting membrane; M, Keimschicht (ventricular zone); M’, Matrix developed from the previous Keimschicht (did they want to differentiate ventricular zone from the ependymal lining?); n, Neuroblasten (migrating neurons); P, pial membrane; Py, Pyramidenschicht, i.e. Rindenschicht (cortical plate) from which the cortex proper (die eigentliche zellführende Rinde) develops; RS, Randschleier (marginal zone), i.e. future molecular layer; x, Keimschicht (germinal layer) within the marginal zone, from which glial and Cajal-Retzius cells of the future molecular layer develop (they probably ment the subpial granular layer of Ranke); Z, Z’’, Zwischenschicht (intermediate zone) from which the future white matter develops; Z’, the upper part of the intermediate zone at its border with the cortical plate – this is a future layer VIb.
Fig. 2
Fig. 2
Ramón y Cajal (in 1891 for rodents and 1899–1902 for humans) was the first to describe neurons situated in the developing subcortical white mater of fetal and early postnatal mammals. However, Cajal regarded them simply as displaced from the adjacent cortex and called them white matter cells. (A) Golgi-stained neurons of supraventricular cortex of 1-month-old mouse: h, cells situated in the white matter (Ramón y Cajal, 1891a,;, plate II, fig. 7 – h, cellules siéegeant dans la substance blanche). (B) Rapid Golgi-staining of lateral entorhinal cortex (la corteza esfenoidal in Cajal's original) of 1-month-old human infant. (K–M) White matter cells with ascending axons (Ramón y Cajal, 1901, p. 50, Fig. 23: K–M, células de la substancia blanca provistas de axon ascendente; reproduced in German translation as Ramón y Cajal 1903, p. 61, Fig. 23: K–M, Zellen der weissen Substanz mit aufsteigendem Axencylinder; also reproduced in French translation as Ramón y Cajal, 1911, p. 696: K–M, cellules de la substance blanche munies d'un cylindre-axe ascendant).
Fig. 3
Fig. 3
Retzius published an early description of subplate neurons in the fetal dog. Gustav Retzius was among the first to described deep neurons with ascending axons (red –mz) located at the border of cortical plate and subjacent ‘fetal white matter’ in the neocortex of the fetal dog (Retzius, 1893, plate I, fig. 1). This figure also gives the first illustration of Cajal-Retzius cells (cz) in the marginal zone of the fetal dog.
Fig. 7
Fig. 7
Hatai in 1902 described the subplate zone in the fetal cat. Schematic representation (A) of six layers of the telencephalic wall in the fetal cat as described by Hatai (1902). Note that it was probably the first description of the subventricular zone (layer 2) as well as the subplate zone (layer 4) with variously oriented and better differentiated cells (B) in comparison to strictly radially oriented cells in the cortical plate (5) and the intermediate zone (3). For details, see text.
Fig. 10
Fig. 10
Karl-Erik Aström was at the brink of discovering the subplate zone in the fetal sheep (Aström, 1967, composed from his slightly modified figs 9, 13 and 25, with permission of Elsevier). (A) Well-developed stellate neurons form a separate (subpyramidal) stratum below the cortical plate in 25 g fetus (embryonic day E53). (B) The same cells can be seen as a transitional zone (E) in the Nissl-stained section of 39 g (E57) fetus. (C) Diagram summarizing connectivity of the early marginal zone, cortical plate and subpyramidal zone (subplate) between E48 and E66. Note that subpyramidal stellate cells receive afferents both from the marginal zone (blue) and from subcortical structures (red) and establish local circuit connections. Note also that these cells are absent at E66, when according to Aström all input–output and local circuitry moved within the cortical plate (because he was convinced that stellate cells become incorporated into the cortical plate as the future layer VIb). Gestation in sheep lasts 140–150 days.
Fig. 4
Fig. 4
Wilhelm His and Hans Jacob correctly described human fetal white matter but not the subplate zone. Wilhelm His (His, 1904; Figs 73, 75 and 79) published a classical description of layers of the human telencephalic wall during the 3rd (A) and 4th (B,C) fetal months. These layers are here denoted using modern terminology (for original terms of His, see text). Note that His described his layers 2–5 (C) as fetal white matter, and he described the subplate zone (his layer 6) as ‘secondary intermediate zone’. MZ, marginal zone; CP, cortical plate; IZ, intermediate zone; VZ, ventricular zone; SP, subplate zone; FWM (IZ/SV), fetal white matter, i.e. intermediate/subventricular zone. A few decades later, Hans Jacob (Jacob, 1936, p. 3, Fig. 1) confirmed His's findings in a 3-month-old human fetus (D), explicitly described the subplate zone as a secondary intermediate zone (sekundäre Zwischenschicht), and pointed out the transient presence of the Unterschicht z of Filimonov (D, arrow). For details, see text.
Fig. 6
Fig. 6
Filimonov describes his ‘Unterschicht z’ which corresponds to the upper subplate zone in humans. Regional differences in the lamination of the telencephalic wall in the occipital lobe of 3.5-month-old human fetus (Filimonoff, 1929, Plate 35, Figs 1, 2 and 3 – A, B and C, respectively). Modern designations are given at the left margin, and original Filimonov's as red letters within the sections, as follows: MZ, marginal zone (Ra –Randschleier); CP, cortical plate (Rpl –Rindenplatte); SPU, upper subplate zone (Unterschicht z); SPL, lower subplate zone (Zsch, i.e. secondary intermediate zone sensu strictiori); IZ, intermediate and subventricular zone, which Filimonov did not designate as a single zone but divided into several sublayers as follows: a = pale stripe (heller Streifen, which divides ventricular zone into Matrix I and Matrix II); b = inner pale layer (innere helle Schicht); c = dark layer (dunkle Schicht); d = middle pale layer (mittlere helle Schicht); e = outer dark layer (äussere dunkle Schicht, which corresponds to the position of the external capsule); VZ, ventricular zone (M –Matrix, which in ventral rostrolateral occipital wall is further divided in Matrix I and Matrix II, separated by a thin pale stripe of fibres –a). For additional explanation, see text.
Fig. 8
Fig. 8
Sugita in 1917 described the rodent subplate and layer VII. The first description of the rodent subplate and layer VII in the prematurely born albino rat (A) and the adult rat (B,C) published by Naoki Sugita (Sugita, 1917, Figs 3, 8, and 9, pp. 526 and 538). Note that his ental layer corresponds to the subplate (in newborn), i.e. to layer VIb or layer VII (in the adult), which are in both cases separated from the ectal layer (VIa) by a thin cell-poor band. However, the ental layer decreases in size postnatally to approximately 50% of its newborn size. Tr. = transitional layers in the newborn (corresponding to intermediate/subventricular zone) which disappear 3 or 4 days after birth. For details, see text.
Fig. 9
Fig. 9
Early description of interstitial cells in the cortex of the fetal sheep (Godina, 1951, composed and slightly modified from his figures 1, 2 and 3– A-C, respectively – and figures 15 and 16 – D,E; reproduced with permission of Springer). 1 = ventricular zone (strato germinativo, strato della matrice); 2 (in A) and 4 (in B, C) = marginal zone (velo marginale, strato marginale); 2 (in B,C) = intermediate zone (strato intermedio, zona intermedia); 3 (in B,C) = cortical plate (strato neuroblastico, strato formativo). (A–C) fetal telencephalic wall in embryos of 18 mm, 43 mm (= 45 embryonic days), and 75 mm (= 63 embryonic days), respectively. (D,E) Nissl stained section through the motor cortex of the sheep fetus 235 mm long (5th fetal month); rectangle encompases numerous interstitial cells in the gyral white matter (magnified in E). However, Godina concluded that these young fusiform neurons present in the gyral white matter are ‘in the process of migration toward the cortex’ (essi sono in migrazione verso la corteccia). Note also that he simply designated as the intermediate zone everything situated between the ventricular zone and the cortical plate. For explanation, see text.

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