Departamento de Anatomía, Universidad de La Laguna, 38071 Tenerife, Spain, , 1 Neurobiology Unit, FUNDP Medical School, B5000 Namur, Belgium and , 2 Instituto de Neurociencias, CSIC, Universidad Miguel Hernández, 03550 San Juan de Alicante, Spain
Address correspondence to Dr Gundela Meyer, Departamento de Anatomía, Facultad de Medicina, Universidad de La Laguna, 38071 La Laguna, Tenerife, Spain. Email: gmeyer{at}ull.es.
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The Need for a Revised Definition of the CajalRetzius cell' |
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The currently prevailing view on CajalRetzius cells is based on the hypothesis of the dual origin of the cerebral cortex, initially proposed by Marín-Padilla (Marín-Padilla, 1971, 1972
, 1978
). It holds that the cerebral cortex derives from an early neural network, originally named the primordial plexiform layer' (Marín-Padilla, 1971
, 1972
, 1978
) and subsequently renamed the preplate' (Rickmann and Wolff, 1981
). The preplate contains mutually interconnected early generated neurons and is split apart by the cortical plate (CP) that will contribute layers IIVI, with the result that preplate derivatives settle superficially, in the marginal zone (MZ), or future layer I, as well as deeply, in the subplate, at the interface with the future white matter. It is generally inferred that the derivatives of the preplate that settle in the MZ are the CajalRetzius cells. According to Marín-Padilla, early CajalRetzius cells send axonal projections into the subplate. The descending axons, together with ascending fibers from Martinotti-type cells, are essential components of his concept of a primordial cortical neuropil (Marín-Padilla, 1971
, 1978
, 1998
).
The hypothesis of an early birth of neurons in the MZ and subplate, originating from the preplate, followed by the division of the preplate when the CP appears, has been amply confirmed (König et al., 1977; Rickmann et al., 1977; Raedler and Raedler, 1978
; Luskin and Shatz, 1985
; Chun and Shatz, 1989
; Wood et al., 1992
). These studies provided unequivocal evidence that the oldest neurons of the cortex do in fact settle above the cortical plate, in layer I, as well as below, in the superficial white matter. However, while simple and attractive, the inference that the preplate elements in the MZ correspond to the classical Cajal Retzius cells is far from obvious. In the present paper, we wish to propose that this view is too restricted to account for some observations in the human and rodent developing cortex (Meyer and Gonzalez-Hernandez, 1993
; Meyer and Goffinet, 1998
; Meyer et al., 1998
, 1999
; Soria et al., 1998
; Soria and Fairén, 1999
) and needs to be significantly modified.
Recently, so-called CajalRetzius cells were shown to secrete Reelin (Reln), the product of the reeler gene (Ogawa et al. 1995; D'Arcangelo et al., 1995
, 1997
; Ikeda and Terashima, 1997
; Schiffmann et al., 1997
; Alcántara et al., 1998
; Meyer and Goffinet, 1998
; Meyer et al., 1998
). The availability of new markers provides an opportunity to study in more detail the typology of developing neurons in the neocortical marginal zone. We studied brains from various species, namely human fetuses (Meyer and Goffinet, 1998
), pre- and postnatal mice and rats (Meyer and Fairén, 1996; Meyer et al., 1998
; Soria et al., 1998
) and late fetal and postnatal kittens (unpublished). We used anti-Reelin antibodies (de Bergeyck et al., 1998
), as well as other immunohistochemical markers such as calretinin, calbindin, GABA and GAD antibodies, and bromodeoxyuridine (BrdU) birthdating. Our data show that Reln is expressed by different neuronal populations in the developing marginal zone MZ, some of which appear quite different from the cells described in the classical studies of Cajal and Retzius. Although some preplate derivatives do express Reln, others do not. Furthermore, at variance with the dual-origin hypothesis of Marín-Padilla, we have observed that a substantial contingent of Reln-positive cells in the MZ seem to derive from a discrete sector of the neuroepithelium in the basal forebrain and to invade the MZ by tangential subpial migration. In addition, some early-born neurons in the marginal zone, which do not express Reln, give rise to the first pioneer axon projections of the embryonic cortex reaching as far as the lateral ganglionic eminence before subplate neurons are generated; we named these cells pioneer neurons' of the MZ (Meyer et al., 1998
). Together with subplate cells, these pioneers contribute an early efferent projection from the preplate.
These data suggest that it would be inappropriate and confusing to label all neurons in the MZ as CajalRetzius cells'. We would rather define CajalRetzius cells' loosely, as the family of Reln-immunoreactive (ir) neurons in the marginal zone, and reserve the term of pioneer neurons for the early, Reln-negative preplate derivatives that settle in the MZ and project to sub-cortical levels. This terminology avoids confusion and reflects the complexity of early corticogenesis.
The early descriptions by Cajal and Retzius referred to the neocortex. Similarly, the present account deals with the neo-cortical MZ, even though the term CajalRetzius cell' has been extended to neurons in the marginal zone of the hippocampus (Soriano et al., 1994; Drakew et al., 1998
; Supèr et al., 1998
; Alcántara et al., 1998
). Although these hippocampal neurons do express Reln (D'Arcangelo et al., 1995
; Ikeda and Terashima, 1997
; Drakew et al., 1998
), studies of the fetal human hippocampus suggest that their development is largely independent from that of the neocortical CajalRetzius cell family (Meyer, 1998
).
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The Cells Described by Retzius and Cajal in the Human MZ Differ in their Morphology and Developmental Kinetics |
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Programmed cell death occurs widely during development, particularly in the subplate (Wahle and Meyer, 1987; Valverde and Facal-Valverde 1988
; Kostovic and Rakic, 1990
; Spreafico et al., 1995
; Price et al., 1997
) and in the cortical plate (Meyer and Wahle, 1988
; Wahle and Meyer, 1987
, 1989
; Blaschke et al., 1996
), and Retzius cells in the MZ may provide a further example of this phenomenon (Ranke, 1910
; Sas and Sanides, 1970
; Bradford et al., 1977
; Derer and Derer, 1990
; Meyer and Gonzalez-Hernandez, 1993
; Del Rio et al., 1995
). However, a recent report by Spreafico et al. using the terminal dUTP nick-end labelling (TUNEL) method to assess apoptosis in the fetal human MZ failed to identify dying CajalRetzius cells after mid-gestation (Spreafico et al., 1999
). Two explanations may be offered for this discrepancy with our own results: Retzius cells may die through a mechanism not visualized by the TUNEL method; or, alternatively, the apoptotic neurons identified by these authors as subpial granule cells would actually correspond to dying Retzius cells, which shortly before their death display shrunken and thus smaller nuclei (Meyer and Gonzalez-Hernandez, 1993
).
The cells described by Cajal in humans were Golgi-impregnated in the cortex of newborn infants (Cajal, 1899a,b
, 1911
); similar neurons were also described by Retzius in a paper that included material from a 9-month-old fetus (Retzius, 1894
). These Cajal cells' differ from Retzius cells in that they lie closer to the pia and display smaller, often triangular or pyriform somata, and less complex processes that lack the ascending branchlets (see Fig. 1
, cell labelled Cajal, 1889', A). Small horizontal bipolar forms are also common. The pyriform Cajal cells show, as their most peculiar morphological trait, a thick descending process from which thin horizontal processes with short collaterals originate. The neuron in Figure 1
, cell d, Meyer, 1993', is a DiI-labelled Cajal-type neuron, and shows surprising similarities with the neurons in Cajal's drawings.
In a previous study (Meyer and Gonzalez-Hernandez, 1993), this cell population was termed persisting CajalRetzius cells', to set it apart from the transient polymorphic cells. Our recent studies (Meyer and Goffinet, 1998
) show that Reln-ir neurons, morphologically similar to those drawn by Cajal (Fig. 3
), are found in the MZ only from the last trimester of gestation onwards. When Cajal cells appear, Retzius cells have already largely disappeared from the MZ; while Cajal cells are occasionally found in adult brains, Retzius cells are not. A theoretical possibility is that transformation of Retzius cells into Cajal cells accounts for the changes of neuronal populations in the MZ (Cajal, 1911
; Marín-Padilla, 1998
). However, we based our observations and conclusions on a large gapless ontogenetic series of fetal human brains labelled by DiI or stained for acetylcholinesterase and Reln (Meyer and Gonzalez-Hernandez, 1993
; Meyer and Goffinet, 1998
), which visualize the entire populations of Retzius and Cajal cells, in contrast to the Golgi method which stains at random only a few neurons in each preparation. Therefore, we favour the idea that Retzius and Cajal cells develop sequentially in the MZ.
In accordance with our proposed timetable, immunohistochemical studies performed at advanced developmental stages of human and macaque cortex, or in adult humans, visualize mostly triangular or small bipolar MZ neurons, our Cajal cells (Belinchenko et al., 1995; Uylings and Delalle, 1997; Huntley and Jones, 1990
). In contrast, studies of the human mid-gestation period clearly describe the Retzius type (Verney and Derer, 1995
).
How do the cells depicted by Marín-Padilla (Marín-Padilla, 1978, 1998
) fit in our scheme? First of all, the Golgi-stained human material of this author, similarly to Cajal's sections, covers predominantly the late gestation or early postnatal period. It is not surprising, therefore, that most of his CajalRetzius cells look like the Cajal type rather than the Retzius type.
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Late-generated Retzius Cells and Cajal Cells Could Migrate Tangentially via the Subpial Granular Layer |
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Neurons in the early human preplate showing similar distribution and morphology have been shown to express GABA (Zecevic and Milosevic, 1997), and the possibility that they coexpress Reln needs to be explored further. This is suggested by the fact that Reln is co-expressed with GABA in an early preplate cell population of the rat cerebral cortex (Meyer et al., 1998
).
Slightly later in development, from the 8th to the 13th GW, Reln-ir cells in prospective neocortical territories are closely apposed to the pial surface and display a very simple mono- or bipolar horizontal morphology (Fig. 3B). Their location and shape, together with the presence of a latero-medial gradient in their packing density apparently originating at the retrobulbar neuroepithelium, strongly suggest tangential subpial migration (Meyer and Wahle, 1999
). If this hypothesis is correct, both radial and tangential migration would contribute Reln-positive neurons to the embryonic and early fetal MZ. This point, however, remains to be demonstrated further.
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The Reelin-producing Cells of the Non-primate Marginal Zone |
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Birthdating studies in rat (Raedler and Raedler, 1978; Bayer and Altman, 1990
; Rickman et al., 1997), mouse (Fairén et al., 1986
) and ferret (Peduzzi, 1988
) show that neurons are added to the MZ during the entire period of corticogenesis. The simplest way for these neurons to reach layer I would be by tangential migration. Furthermore, the SGL and neuronal elements with features of early subpial Reln-ir neurons, Retzius cells and Cajal cells can be defined in all species examined.
Contrary to the assumption that the SGL is specific to the human or primate cortex, our observations (Meyer et al., 1998) have confirmed the existence of a rodent SGL as a distinct cellular component of the MZ. Granule cells in the rodent SGL most likely arise from a specific sector of the neuroepithelium behind the olfactory bulb, the retrobulbar area (Fig. 4C,D
), from where they appear to spread through tangential subpial migration into the MZ of the neocortex.
The limited spatiotemporal resolution in these species compared to human fetuses makes it difficult to distinguish the early preplate neurons from later SGL neurons. Several subpopulations can be defined in the preplate and MZ, however, on neurochemical grounds. In the rat, GABA is expressed by early neuron cohorts of the preplate (Van Eden et al., 1989; Cobas et al., 1991
) [reviewed by Fairén et al. (Fairén et al.,1998
)], and these early GABA-ir cells co-express Reln (Meyer et al., 1998
). In addition, SGL cells express calbindin and calretinin. The rat SGL neurons start expressing Reln before they differentiate into Retzius or Cajal cells (Meyer et al., 1998
), but we have chosen to designate as Retzius or Cajal cells only MZ Reln-ir cells in postnatal animals. In this aspect we differ from most current studies on rodent cortical development.
The rationale of our choice is based on the initial description by Cajal (Cajal, 1891) of these cells in postnatal lagomorphs (see Fig. 2
), and the different time-course of corticogenesis in primates compared to rodents. Although the ascending processes are less visible than in humans, Retzius-type cells are characterized by vertical processes that ascend to the pia. By contrast, SGL cells look like the undifferentiated, possibly migratory cells in the human SGL. The transformation of SGL cells into Retzius cells concurs with their descent in the MZ (Meyer et al., 1998
), a process that does not take place in reeler mice (Derer, 1985
). Retzius cells attain their highest differentiation in the first postnatal week and die during the second week. Contrary to the case in the mouse (Weisenhorn et al., 1994
; del Rio et al., 1995
), calretinin is not a permanent marker of Retzius cells in rats, where an important cohort of calretinin-expressing cells does not express Reln and dies during the early postnatal period. Other Retzius cells, co-expressing Reln and calretinin, survive for longer periods in layer I. During the early postnatal period, GABA downregulates in layer I or, alternatively, the cells expressing it die, so that Retzius cells do not express GABA (Meyer et al., 1998
).
The most likely homologues of the Cajal-type cells appear as small subpial pyriform elements subjacent to the pial surface; they differentiate from the SGL by the end of the first week; some of them persist and continue to express Reln into adult life. Subpial pyriform cells express Reln and calretinin (Meyer et al., 1998) and also GABA (Imamoto et al., 1994
).
It may seem ironic that the first description of Retzius cells (as defined here) was indeed due to Cajal (Cajal, 1891) (Fig. 2
). Therefore, we suggest maintaining the name CajalRetzius to designate the Reln-expressing cells of the early postnatal period of the rodent (Meyer et al., 1998
).
Derer and Derer stained CajalRetzius cells in late prenatal and postnatal mice using HRP in vitro labelling and in tangential sections (Derer and Derer, 1995). These authors confirmed the existence of the ascending appendages reaching the pia in this species, and described very long axons of CajalRetzius cells, in the range of millimetres. The axons, at variance with primates, extend within the same depth as the cell bodies and dendrites. These morphological features imply advanced differentiation, which is not present in SGL cells.
Reln-ir Retzius cells are also present in the perinatal cat cortex (G. Meyer, unpublished results) (Fig. 6A). Although there are considerable morphological differences between the human Retzius cells and the much simpler cat homologues, the defining features such as the comb-like ascending appendages and the large soma are evident (Meyer and Ferres-Torres, 1984
). At post- natal day 20, most Retzius cells have disappeared, and instead the MZ is now populated by Cajal cells (Fig. 6B,C
), along with many small non-pyramidal cells, all of which secrete Reln. As in the human cortex, the cat Cajal cells have a subpial position, triangular or pyriform somata, and a single descending process (Fig. 5B,C
, arrows).
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The Reelin-negative Pioneer Neurons of the Marginal Zone |
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Pioneer neurons are generated before subplate neurons and their axonal projection is seen when the preplate is formed by a monolayer of cells (Fig. 6A,B, arrows). The axons fasciculate as they pass through the intermediate zone of the cortical primordium (Fig. 7
) to the incipient internal capsule in the lateral ganglionic eminence; axon collaterals also reach the ventricular zone (Meyer et al., 1998
). In keeping with their pioneer character (Bovolenta and Mason, 1987
; Kim et al., 1991
), their axons are cupped with large, elaborate growth-cones. This pioneer axon projection appears before the pioneer descending projection from the subplate (de Carlos and O'Leary, 1992
; Métin and Godement, 1996
; Richards et al., 1997
; Molnár et al., 1998
). Pioneer cells are clearly different from subplate cells. In tangential views of the cortical surface they appear as a huge neuronal population that is maintained after the appearance of the cortical plate. At this developmental period (Figs 6C
, 7C
), MZ cell axons can be followed through the cortical plate to the subplate (Meyer et al., 1998
) but the projection into the incipient internal capsule seems to be lost, being replaced by the subcortical projection from the subplate.
|
An important question concerns the presence of pioneer neurons in the human cortex, in which they have not yet been described. Our preliminary data suggest that some calretinin-ir neurons may be the homologues of the rodent pioneer neurons (Fig. 7A,B).They are placed in the lower part of the MZ, have a descending axon and invade the upper tier of the cortical plate. Clearly, the identification of the early preplate derivative of the human or primate MZ requires further investigation.
In sum, the theory that all CajalRetzius cells are derivatives of the preplate and remain unchanged from the first moments of corticogenesis is no longer tenable. Recent observations suggest that there are dynamic changes of cell populations in the marginal zone during corticogenesis, with new neurons being continuously added, while others die after having fulfilled their developmental role. The Reln-producing members of the Cajal Retzius family are an important part of these populations. While some of them may derive from the preplate, as it has been universally accepted, others invade the MZ by tangential, subpial migration. Retzius cells correspond more closely to what is commonly understood as the prototype of the human Cajal Retzius cell, and they are transient, restricted to the period of cortical migration. Cajal cells mature later in development, and may persist into adult life. In addition to Reln-positive cells, the developing MZ, from its earliest developmental stage, contains Reln-negative pioneer neurons that establish the first efferent projections of the cortex, and may play a significant role in the territorialization of the early cortical vesicle.
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Acknowledgments |
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References |
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---|
Anton ES, Cameron RS, Rakic P (1996) Role of neuron-glial junctional domain proteins in the maintenance and termination of neuronal migration across the embryonic cerebral wall. J Neurosci 16: 22832293.[Abstract]
Bate CM 1976 Pioneer neurones in an insect embryo. Nature 260:5456[ISI][Medline]
Bayer SA, Altman J (1990) Development of layer I and the subplate in the rat neocortex. Exp Neurol 107:4862.[ISI][Medline]
Belichenko PV, Vogt Weisenhorn DM, Myklossy J, Celio MR (1995) Calretinin-positive CajalRetzius cells persist in the adult human neocortex. NeuroReport 6:18691874.[ISI][Medline]
Blaschke AJ, Staley K, Chun J (1996) Widespread programmed cell death in proliferative and postmitotic regions of the fetal cerebral cortex. Development 122:11651174.
Bovolenta P, Mason C (1987) Growth cone morphology varies with position in the developing mouse visual pathway from retina to first targets. J Neurosci 7:14471460.[Abstract]
Bradford, R, Parnavelas JG, Lieberman AR (1977) Neurons in layer I of the developing occipital cortex of the rat. J Comp Neurol 176:121132.[ISI][Medline]
Brun A (1965) The subpial granular layer of the foetal cerebral cortex in man. Its ontogeny and significance in congenital cortical malformations. Acta Pathol Microbiol Scand 179(Suppl):198.
Cajal SR (1891) Sur la structure de l'ecorce cérébrale de quelques mammifères. La Cellule 7:123176. English translation in DeFelipe J, Jones EG (1988) Cajal on the cerebral cortex, pp. 2354. Oxford: Oxford University Press.
Cajal SR (1899a) Estudios sobre la corteza cerebral humana. I. Corteza visual. Rev Trimestral Micrográfica 4:163. English translation in DeFelipe J, Jones EG (1988) Cajal on the cerebral cortex, pp. 147187. Oxford: Oxford University Press.
Cajal SR (1899b) Estudios sobre la corteza cerebral humana. II. Estructura de la corteza motriz del hombre y mamíferos superiores. Rev Trimestral Micrográfica 4:117200. English translation in DeFelipe J, Jones EG (1988) Cajal on the cerebral cortex, pp. 188250. Oxford: Oxford University Press.
Cajal SR (1911) Histologie du système nerveux de l'homme et des vertébrés, vol. 2. Paris: Maloine.
Chun JJ, Shatz CJ (1989) The earliest-generated neurons of the cat cerebral cortex: characterization by MAP2 and neurotransmitter immunohistochemistry during fetal life. J Neurosci 9:16481667.[Abstract]
Cobas A, Fairén A, Alvarez-Bolado G, Sanchez MP(1991) Prenatal development of the intrinsic neurons of the rat neocortex: a comparative study of the distribution of GABA-immunoreactive cells and the GABAA receptor. Neuroscience 40:375397.[ISI][Medline]
D'Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374:719723.[ISI][Medline]
D'Arcangelo G, Nakajima K, Miyata T, Ogawa M, Mikoshiba K, Curran T (1997) Reelin is a secreted glycoprotein recognized by the Cajal Retzius-50 monoclonal antibody. J Neurosci 17:2331.
de Bergeyck V, Naerhuyzen B, Goffinet AM, Lambert de Rouvroit C (1998) A panel of monoclonal antibodies against Reelin, the extracellular matrix protein defective in reeler mutant mice. J Neurosci Methods 82:1724.[ISI][Medline]
de Carlos JA, O'Leary DDM (1992) Growth and targeting of subplate axons and establishment of major cortical pathways. J Neurosci 12:11941211.[Abstract]
del Rio JA, Martinez A, Fonseca M, Auladell C, Soriano E (1995) Glutamate-like immunoreactivity and fate of CajalRetzius cells in the murine cortex as identified with calretinin antibody. Cereb Cortex 5:1321.[Abstract]
Derer P (1985) Comparative localization of CajalRetzius cells in the neocortex of normal and reeler mutant mice fetuses. Neurosci Lett 54:16.[ISI][Medline]
Derer P, Derer M (1990) CajalRetzius cell ontogenesis and death in mouse brain visualized with horseradish peroxidase and electron microscopy. Neuroscience 36:839856.[ISI][Medline]
Drakew A, Frotscher M, Deller T, Ogawa M, Heimrich B (1998) Developmental distribution of a reeler gene-related antigen in the rat hippocampal formation visualized by CajalRetzius-50 immunocytochemistry. Neuroscience 82:10791086.[ISI][Medline]
Duckett S, Pease AGE (1968) The cells of CajalRetzius in the developing human brain. J Anat 102:183187.[ISI][Medline]
Fairén A, Cobas A, Fonseca M (1986) Times of generation of glutamic acid decarboxylase immunoreactive neurons in mouse somatosensory cortex. J Comp Neurol 251:6783.[ISI][Medline]
Fairén A, Alvarez-Bolado G, DeDiego I, Smith-Fernandez A (1998) GABA-immunoreactive cells of the cortical primordium contribute to distinctly fated neuronal populations. Perspect Dev Neurobiol 5:159173.[ISI][Medline]
Gadisseux JF, Goffinet AM, Lyon G, Evrard P (1992) The human transient subpial granular layer: an optical, immunohistochemical, and ultrastructural analysis. J Comp Neurol 324:94114.[ISI][Medline]
Harrison RG (1910) The outgrowth of the nerve fiber as a mode of protoplasmic movement. J Exp Zool 9:787848.
Hendrickson AE, Van Brederode JF, Mulligan KA, Celio MR (1991) Development of the calcium-binding protein parvalbumin and calbindin in monkey striate cortex. J Comp Neurol 307:626646.[ISI][Medline]
Huntley GW, Jones EG (1990) CajalRetzius cells in the developing monkey neocortex show immunoreactivity for calcium-binding proteins. J Neurocytol 19:200212.[ISI][Medline]
Ikeda Y, Terashima T (1997) Expression of Reelin, the gene responsible for the reeler mutation, in embryonic development and adulthood in the mouse. Dev Dynam 210:157172.[ISI][Medline]
Imamoto K, Karasawa N, Isomura G, Nagatsu I (1994) CajalRetzius neurons identified by GABA immunohistochemistry in layer I of the rat cerebral cortex. Neurosci Res 20:101105.[ISI][Medline]
Kim GJ, Shatz CJ, McConnell SK (1991) Morphology of pioneer and follower growth cones in the developing cerebral cortex. J Neurobiol 22:629642.[ISI][Medline]
König N (1978) Retzius-Cajal cells or CajalRetzius cells? Neurosci Lett 9:361363.[ISI]
König N, Roch G, Marty R (1975) The onset of synaptogenesis in rat temporal cortex. Anat Embryol 148:7387.[ISI][Medline]
König N, Valat J, Fulcrand J, Marty R (1977) The time of origin of CajalRetzius cells in the rat temporal cortex. An autoradiographic study. Neurosci Lett 4:2126.[ISI]
Kostovic I, Rakic P (1990) Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 297:441470.[ISI][Medline]
Lavdas AA, Grigoriu M, Pachnis V, Parnavelas JG (1999) The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J Neurosci (in press).
Luskin MB, Shatz CJ (1985) Studies of the earliest generated cells of the cat's visual cortex: cogeneration of subplate and marginal zones. J Neurosci 5:10621075.[Abstract]
Marín-Padilla M (1971) Early prenatal ontogenesis of the cerebral cortex (neocortex) of the cat (Felis domestica). A Golgi study. I. The primordial neocortical organization. Z Anat Entwickl-Gesch 134:117145.[ISI][Medline]
Marín-Padilla M (1972) Prenatal ontogenetic history of the principal neurons of the neocortex of the cat (Felis domestica). A Golgi study. II. Developmental differences and their significances. Z Anat Enwickl-Gesch 136:125142.
Marín-Padilla M (1978) Dual origin of the mammalian neocortex and evolution of the cortical plate. Anat Embryol 152:109126.[ISI][Medline]
Marín-Padilla M (1990) Three-dimensional structural organization of layer I of the human cerebral cortex: a Golgi study. J Comp Neurol 299:89105.[ISI][Medline]
Marín Padilla M (1995) Prenatal development of fibrous (white matter), protoplasmic (gray matter) and layer I astrocytes in the human cerebral cortex: a Golgi study. J Comp Neurol 357:554572.[ISI][Medline]
Marín-Padilla M (1998) CajalRetzius cells and the development of the neocortex. Trends Neurosci 21:6471.[ISI][Medline]
McConnell SK, Ghosh A, Shatz CJ (1989) Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 245:978982.[ISI][Medline]
Métin C, Godement P (1996) The ganglionic eminence may be an intermediate target for corticofugal and thalamocortical axons. J Neurosci 15:32193235.
Meyer G (1998) Reelin-immunoreactive neurons in the fetal human hippocampus. Soc Neurosci Abstr 24:305.
Meyer G, Ferres-Torres R (1984) Postnatal maturation of nonpyramidal neurons in the visual cortex of the cat. J Comp Neurol 228: 226244.[ISI][Medline]
Meyer G, Gonzalez-Hernandez T (1993) Developmental changes in layer I of the human neocortex during prenatal life: a DiI-tracing and AChE and NADPH-d histochemistry study. J Comp Neurol 338:317336.[ISI][Medline]
Meyer G, Goffinet AM (1998) Prenatal development of Reelin-immunoreactive neurons in the human neocortex. J Comp Neurol 397:2940.[ISI][Medline]
Meyer G, Soria JM, Martínez-Galán JR, Martín-Clemente B, Fairén A (1998) Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex. J Comp Neurol 397:493518.[ISI][Medline]
Meyer G, Castro R, Soria JM, Fairén A (1999) The subpial granular layer in the developing cerebral cortex of rodents. In: Mouse brain development (Goffinet AM, Rakic P, eds). Berlin: Springer-Verlag (in press).
Meyer G, Wahle P (1988) Early postnatal development of cholecystokinin- immunoreactive structures in the visual cortex of the cat. J Comp Neurol 276:360386.[ISI][Medline]
Meyer G, Wahle P (1999) The paleocortical ventricle is the origin of Reelin-expressing neurons in the marginal zone of the fetal human neocortex. Eur J Neurosci (in press).
Molnár Z, Adams R, Blakemore C (1998) Mechanisms underlying the early establishment of thalamocortical connections in the rat. J Neurosci 18:57235745.
Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaka K, Yamamoto H, Mikoshiba K (1995) The reeler gene-associated antigen on CajalRetzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14:899912.[ISI][Medline]
O'Rourke NA, Dailey ME, Smith SJ, McConnell SK (1992) Diverse migratory pathways in the developing cerebral cortex. Science 258:299302.[ISI][Medline]
O'Rourke NA, Sullivan DP, Kaznowski CE, Jacobs AA, McConnell SK (1995) Tangential migration of neurons in the developing cerebral cortex. Development 121:21652176.
Peduzzi JD (1988) Genesis of GABA-immunoreactive neurons in the ferret visual cortex. J Neurosci 8:920931.[Abstract]
Price DJ, Aslam S, Tasker L, Gillies K (1997) Fates of the earliest generated cells in the developing murine neocortex. J Comp Neurol 377:414422.[ISI][Medline]
Raedler E, Raedler A (1978) Autoradiographic study of early ontogenesis in rat neocortex. Anat Embryol 154:267284.[ISI][Medline]
Ranke G (1910) Beiträge zur Kenntnis der normalen und pathologischen Hirnrindenbildung. Zieglers Beiträge 47:51125.
Retzius G (1893) Die Cajal'schen Zellen der Grosshirnrinde beim Menschen und bei Säugetieren. Biologische Untersuchungen, Neue Folge 5:18.
Retzius G (1894) Weitere Beiträge zur Kenntniss der Cajal'schen Zellen der Grosshirnrinde des Menschen. Biologische Untersuchungen, Neue Folge 6:2936.
Richards LJ, Koester SE, Tuttle R, O'Leary DDM (1997) Directed growth of early cortical axons is influenced by a chemoattractant released from an intermediate target. J Neurosci 17:24452458.
Rickmann M, Wolff JR (1981) Differentiation of preplate' neurons in the pallium of the rat. Biblio Anat 19:142146.[Medline]
Rickman M, Chronwall BM, Wolff JR (1977) On the development of non-pyramidal neurons and axons outside the cortical plate: the early marginal zone as a pallial anlage. Anat Embryol 151:285307.[ISI][Medline]
Sas E, Sanides F (1970) A comparative Golgi study of Cajal foetal cells. Z Mikrosk Anat Forsch 82:385396.[Medline]
Schiffmann SN, Bernier B, Goffinet AM (1997) Reelin mRNA expression during mouse brain development. Eur J Neurosci 9:10551071.[ISI][Medline]
Soria JM, Fairén A (1999) Cellular mosaics in the rat marginal zone define an early neocortical territorialization. Cereb Cortex (in press).
Soria JM, Meyer G, Fairén A (1998) Cortical pioneer cells acquire specific tangential distributions during rat corticogenesis. Eur J Neurosci 10(Suppl 10):8.
Soria JM, Martínez-Galán JR, Luján R, Valdeolmillos M, Fairén A (1999) Functional N-methyl-D-aspartate (NMDA) and GABAA receptors in pioneer neurons of the cortical marginal zone. Eur J Neurosci (in press).
Soriano E, Del Rio JA, Martinez A, Supèr H (1994) Organization of the embryonic and early postnatal murine hippocampus. I. Immunocytochemical characterization of neuronal populations in the subplate and marginal zone. J Comp Neurol 342:571595.[ISI][Medline]
Spreafico R, Arcelli P, Frassoni C, Canetti P, Giaccone G, Rizzuti T, Mastrangelo M, Bentivoglio M (1999) Development of layer I of the human cerebral cortex after midgestation: architectonic findings, immunocytochemical identification of neurons and glia, and in situ labelling of apoptotic cells. J Comp Neurol 410:126142.[ISI][Medline]
Spreafico R, Frassoni C, Arcelli P, Selvaggio M, De Biasi S (1995) In situ labelling of apoptotic cell death in the cerebral cortex and thalamus of rats during development. J Comp Neurol 363:281295.[ISI][Medline]
Supèr H, Soriano E, Uylings HBM (1998) The functions of the preplate in development and evolution of the neocortex and hippocampus. Brain Res Rev 27:4064.[ISI][Medline]
Tamamaki N, Fujimori KE, Takauji R (1997) Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone. J Neurosci 17:83138323.
Uylings HB, Delalle I (1997) Morphology of neuropeptide Y-immunoreactive neurons and fibers in human prefrontal cortex during prenatal and postnatal development. J Comp Neurol 379:523540.[ISI][Medline]
Valverde F, Facal-Valverde MV (1988) Postnatal development of interstitial (subplate) cells in the white matter of the temporal cortex of kittens: a correlated Golgi and electron microscopic study. J Comp Neurol 269:168192.[ISI][Medline]
Van Eden CG, Mrzljak L, Voorn P, Uylings HB (1989) Prenatal development of GABA-ergic neurons in the neocortex of the rat. J Comp Neurol 289:213227.[ISI][Medline]
Verney C, Derer P (1995) CajalRetzius neurons in human cerebral cortex at midgestation show immunoreactivity for neurofilament and calcium-binding proteins. J Comp Neurol 359:144153.[ISI][Medline]
Wahle P, Meyer G (1987) Morphology and quantitative changes of transient NPY-ir neuronal populations during early postnatal development of the cat visual cortex. J Comp Neurol 261:165192.[ISI][Medline]
Wahle P, Meyer G (1989) The early postnatal development of VIP/PHI ir structures in the visual cortex of the cat. J Comp Neurol 282:215248.[ISI][Medline]
Weisenhorn DM, Prieto EW, Celio MR (1994) Localization of calretinin in cells of layer I (CajalRetzius cells) of the developing cortex of the rat. Dev Brain Res 82:293297.[ISI][Medline]
Wood JG, Martin S, Price DJ (1992) Evidence that the earliest generated cells of the murine cerebral cortex form a transient population in the subplate and marginal zone. Dev Brain Res 66:137140.[ISI][Medline]
Yan YH, van Brederode JF, Hendrickson AE (1995a) Developmental changes in calretinin expression in GABAergic and nonGABAergic neurons in monkey striate cortex. J Comp Neurol 363:7892.[ISI][Medline]
Yan YH, van Brederode JF, Hendrickson AE (1995b) Transient colocalization of calretinin, parvalbumin, and calbindin-D28K in developing visual cortex of monkey. J Neurocytol 24:825837.[ISI][Medline]
Zecevic N, Milosevic A (1997) Initial development of -aminobutyric acid immunoreactivity in the human cerebral cortex. J Comp Neurol 380:495506.[ISI][Medline]