Programa de Morfología, Instituto de Ciencias Biomédicas, Facultad de Medicina, Universidad de Chile, Santiago, Chile
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Abstract |
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Introduction |
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In this article I will briefly review some new findings on the control of cellular migration and the generation of the inside-out pattern by reelin, an extracellular protein whose absence or dysfunction produces the reeler malformation in mice, and by a cyclin-dependent kinase complex whose mutation generates a slightly different phenotype than reeler. Then, the reptilian and the mammalian cortices will be compared and an hypothesis for the origin of the inverted neurogenetic gradient of isocortex will be proposed in the light of recent evidence. I will also suggest a role for a transient embryological structure known as the subplate zone in the origin of the radial organization of thalamic afferents to isocortex.
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Early Cortical Development and the Inside-out Gradient of Cell Migration |
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The second wave of cell migration to the preplate [cells born in deeper portions of the ventricular zone (Valverde et al., 1995)] produces a transient subplate zone located below, which in most mammals degenerates during cortical development [however, in the rat many such cells survive into adulthood (Woo et al., 1991
)]. The subplate serves as a waiting compartment for thalamic axons which reach the cortex before the appropriate target cells have migrated to their final position in the prospective layer IV (Rakic, 1977
, 1978
; Allendoerfer and Schatz, 1994). It also contributes pioneering cortico-thalamic projections, which in turn serve as guides for thalamocortical afferents that develop at about the same time (McConnell et al., 1994
; Molnár and Blakemore, 1995
). A third, late wave of migrating neurons makes up the cortical plate (layers IIVI of isocortex). These cells cross the subplate and locate between the latter and the marginal zone (Bayer and Altman, 1991
; Marín-Padilla, 1998
), thus splitting the preplate into two separate layers. Within the cortical plate, the different cellular laminae develop in a sequence such that earlier generated cells end up in deeper laminae and late-generated cells locate more superficially. This process is known as the inside-out pattern of cell migration (Angevine and Sidman, 1961
; Rakic, 1974
) and is apparently unique to the mammalian cortex.
Reelin as a Regulator of Cortical Cell Migration
Reeler is an autosomal recessive mutant mouse that was initially characterized by its ataxic and reeling gate (Falconer, 1951). This animal has defects in the cerebellum (Hamburgh, 1960
), but also in the cerebral cortex and other brain regions (Caviness, 1977
; Caviness and Rakic, 1978
; Goffinet, 1992
; Rakic and Caviness, 1995
; DArcangelo and Curran, 1998
; Curran and DArcangelo, 1998
). The cortical defects of this mutant have been the subject of intense interest. In the reeler mouse, cortical migration occurs in an outside-in pattern, in which late-generated cells are not able to migrate past early-generated ones, thus accumulating below the latter (Caviness, 1977
). Furthermore, the preplate fails to split into the marginal zone (no cell-poor layer I is formed) and the subplate, and the latter is abnormally located between the pial surface and the cortical plate. Surprisingly, connectional patterns are remarkably conserved in the cortex of these mice.
Recently, an extracellular matrix glycoprotein reelin has been identified that maps onto chromosome 5 and whose homozygotic mutant is responsible for the reeler phenotype (DArcangelo et al., 1995, 1997
; Ogawa et al., 1995
; Frotscher, 1997
, 1998
; DArcangelo and Curran, 1998
; Curran and DArcangelo, 1998
). In the developing cortex, reelin is located mainly in the marginal zone and its gene is expressed in CajalRetzius cells (Alcántara et al., 1998
). It has been proposed that reelin acts as a stop signal for migrating neurons (Frotscher, 1997
; Goffinet, 1997
). One simple model to explain the generation of the inside-out gradient is that, since reelin is located in the marginal zone (layer I), as the earliest migrating neurons contact reelin they stop migrating (Goffinet, 1997
; Frotscher, 1998
). Nevertheless, cells blocked by reelin probably leave space for subsequent migrating cells to travel past them, and stop migrating as they contact more superficially located reelin molecules in the marginal zone (see Fig. 1
). If, as in the reeler mouse, reelin is absent or inactive during cortical plate development, neurons will migrate up to the pial surface, producing an outside-in pattern because early migrated cells accumulate in the external surface and do not leave space for late migrating cells to pass through. Reelin has also been found to act as a guidepost for axons that grow into layer I of the hippocampus (Del Río et al., 1997
; Borrell et al., 1999
), and it has been postulated that it plays a dual role, regulating axonal growth in the latter and blocking neuronal migration in the isocortex (Frotscher, 1997
, 1998
).
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The p35/cdk5 complex
An additional component involved in the generation of the inside-out gradient is a cyclin-dependent, serinethreonine protein kinase cdk5 and its neuronal specific activator p35 which are expressed in postmitotic neurons (Oshima et al., 1996; Chae et al., 1997; Goffinet, 1997
). In the cortical plate, mice lacking the cyclin-dependent kinase cdk5 or its activator p35 show an inverted lamination pattern just like the reeler. However, whereas in the latter mutant the marginal zone and the subplate are not properly differentiated, in the p35/cdk5 mutant mice these two layers are well formed and split after the arrival of cells destined to the cortical plate, as occurs in the normal mouse (Gilmore et al., 1998
; Kwon and Tsai, 1998
). Kwon and Tsai suggest that the p35/cdk5 kinase complex is required for cortical neurons to migrate past pre-existing cortical plate cells (Kwon and Tsai, 1998
). Null mutants of cdk5 also show hippocampal and cerebellar deficits, but, contrary to reeler, they die shortly after birth (DArcangelo and Curran, 1998
). On the other hand, despite their cortical deficits, p35 mutants show no hippocampal or cerebellar abnormalities (DArcangelo and Curran, 1998
), perhaps because cdk5 is activated by other proteins in these regions.
The p35/cdk5 complex has been shown to be involved in laminin-enhanced axonal growth of cerebellar macroneurons (Paglini et al., 1998) and in the elongation of cortical axon growth cones (Nikolic et al., 1998
). In neuronal growth cones, the active complex p35/cdk5 inhibits a Pak1 kinase that regulates actin polymerization, which may as a consequence permit cytoskeletal reorganization and axonal elongation (Nikolic et al., 1998
). Thus, the p35/cdk5 complex is apparently involved in a mechanism that promotes neurite extension or cell movement, which may be necessary for cortical cells to migrate past already migrated cells within the cortical plate.
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The Reptilian Cortex in Comparison to the Mammalian Isocortex |
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Connectional and histochemical comparisons between the mammalian and the reptilian cortices have led some authors to suggest that cells in the deepest layers (layers VVI) of isocortex are comparable to those of the reptilian cortex, while some cells in the more superficial granular and supragranular layers (layers IIIV) of isocortex may be considered an addition of new neuronal types in the mammalian lineage. Ebner claimed that the reptilian cortex is similar to infragranular isocortical layers in terms of their shared projections to subcortical sites (Ebner, 1976). On the other hand, in granular and supragranular layers there is an emphasis in local and cortico-cortical connections, a character that although present in the reptilian cortex is not as well developed as it is in mammals. [Yet, in the isocortex there are descending cortical projections originating in supragranular layers (Fisher et al., 1986
), as well as corticocortical projections arising from infragranular layers (Galaburda and Pandya, 1983
; Barbas and Rempel-Clower, 1997
).] Reiner found that in supragranular cortical layers many cells stain positive for neurotransmitters that are not found in reptilian cortex (CCK8, VIP and acetylcholine) (Reiner, 1991
, 1993
). On the other hand, cells in layers VVI are devoid of these neurotransmitters. Neurotransmitters common to reptilian and mammalian cortex (substance P, NPY, somatostatin, LANT6, GABA and glutamate) were found in all cortical layers.
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Hypothetical Origin of the Inside-out Gradient of Mammalian Cortical Migration |
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Suppose that the presumptive mammalian isocortex initially developed according to the traditional outside-in gradient of cell migration. That is, cells in the late-generated, new layers [many of which are corticocortical association neurons and/or local circuit cells (Valverde and Facal-Valverde, 1986; Voogd et al., 1998
)] would have ended their migration below the layer of earlier-generated (output) cells. I suggest that in this hypothetical case, the younger cells had limited access to the afferents in the superficial layer I (see Fig. 3A
). Instead, the early-produced output cells, being located more superficially than the lateproduced cells, would have benefited in their access to the axons in layer I. This situation constrained cortical processing capacity, since the newly produced cell types were limited in their ability to modify the input received by the output cells.
My proposal is that the solution to this problem was the generation of the inside-out pattern of lamination in which the new, late-produced cortical neurons were able to move past the layers of already migrated cells and make contacts with the superficial axons (Fig. 3B) (Aboitiz, 1993
). Processing capacity may have benefited significantly if the new cell types had direct access to the afferents rather than making synapses below the output layer of the cortex. Thus, one or more synapses might be established between the input axons and the output cells as occurs in the more modern isocortex (Voogd et al., 1998
). As a result, cortical inputs could be processed by corticocortical and local circuits before the output layer (now the deepest) was capable of generating a response. There are some exceptions to this in the sense that in isocortex many cells in supragranular layers perform as output cells, e.g. to the corpus striatum [although many of such projections are collaterals of corticocortical axons (Fisher et al., 1986
)], and there are some direct connections between thalamic afferents and the apical dendrites of infragranular cells. However, it is fair to say that in general terms the main difference in the organization of mammalian isocortex with respect to reptilian cortex is the emphasis on corticocortical and local circuit neurons in the former, many of which are located in the granular and in the supragranular layers (Ebner, 1976
; Valverde and Facal-Valverde, 1986
; Voogd et al., 1998
).
The mammalian hippocampus deserves brief comment here. In this structure there may also be an inside-out gradient of cell migration (Super et al., 1998), although there is no such a differentiation between superficial, associative and deep, output, neuronal layers as there is in isocortex. Perhaps the establishment of the inside-out gradient took place in the whole cortical surface, including isoand allocortex, even if the adaptive benefit was to correspond only to isocortical circuits. Recall that laminar inversion does not induce major changes in connectivity, as can be observed in the reeler cerebral cortex, and therefore it may not have been detrimental in the hippocampus. Developmental constraints that define specific compartments of gene expression in the brain may have impeded the inversion of the neurogenetic gradient occurring only in the isocortex. Contrary to other cortical structures, the dentate gyrus develops in an outside-in gradient (Curran and DArcangelo, 1998
), which may perhaps be explained if this structure belongs to a different developmental compartment than the rest of the cortical structures.
Roles of Reelin and of p35/cdk5
Reelin may have been an important component in the establishment of the inside-out gradient. In an ancestral outside-in pattern of migration, this molecule could have originally served as a stop signal only for the first wave of migrating cortical plate neurons. In turn, these migrated neurons may have secreted some protein (that may be reelin itself or some other molecule) that acted as a stop signal for the subsequent wave of migrating cells, thus forcing the latter to end their displacement immediately below the former (Fig. 3A). If this process were repeated for successive waves of cell migration, early-produced cells would have become positioned above late-produced ones in the traditional outside-in gradient. One possibility for the origin of the inverted inside-out gradient is that the cortical plate neurons ceased secreting the stop signal. In this case, the late-produced cells would not stop migrating as they reached previously migrated cells, and would traverse the existing layers to end migrating only when contacting the reelin molecules in the marginal zone. This hypothesis prescribes a stop signal in the reptilian cortical plate that is absent in mammals. If this alternative is correct, the p35/cdk5 kinase described by Kwon and Tsai (Kwon and Tsai, 1998
) might be involved in suppressing the expression of the stop signal within the cortical plate (and therefore the p35/cdk5 null mutant should be expressing a stop signal like the one present in the reptilian cortex). However, this hypothetical role of p35/cdk5 is unexpected considering its known participation in promoting neurite extension during axonal growth.
Alternatively, the p35/cdk5 kinase complex may be part of a molecular mechanism that can overcome the stop barrier produced by the migrated cells within the cortical plate but not the barrier posed by reelin in the marginal zone (see Fig. 3B). This is consistent with the described role of p35/cdk5 in promoting neurite outgrowth. This second hypothesis predicts that the stop factor within the cortical plate should be different from reelin, and that it should exist in the developing cortical plate of both mammals and reptiles. Cortical neurons are apparently able to migrate past subplate cells in p35/cdk5 mutants. Thus, the capacity of cortical neurons to cross the subplate may depend on different molecular factors than those required for the inside-out gradient within the cortical plate. Even simpler, perhaps the subplate neurons do not secrete any stop signal for cells generated later.
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The Role of the Subplate in Isocortical Evolution |
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A preplate has been described in the development of the reptilian cortex (Nacher et al., 1996), suggesting that it originated as an embryonic structure before the evolution of the isocortex and the inverted neurogenetic gradient, possibly in ancestral amniotes (reptiles and mammals). The reptilian preplate splits into a prominent external plexiform layer with primitive CajalRetzius cells (corresponding to the mammalian marginal zone or layer I), and a poorly differentiated inner plexiform layer that corresponds to the subplate (Fig. 4
). It will be of the greatest interest to determine if the CajalRetzius-like cells in the external plexiform layer express reelin; if they do, this molecule may serve as a substrate for tangential growth of axons in this layer as it occurs in the mammalian hippocampus (Del Río et al., 1997
; Frotscher, 1997
). Between these two layers, a cell-dense layer develops that has been compared to the mammalian cortical plate and from which the reptilian cortex develops (Super et al., 1998
). I suggest that in the origin of mammalian isocortex, the subplate had a role in promoting the shift from a radial to a tangential organization of the cortical inputs. This probably happened in two successive steps, to be described below.
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Step 1: Vertical Entrance of Axons from the White Matter |
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The subplate or inner plexiform layer, which is located below the cortical plate, may have played a key role in this transition, by replacing the outer plexiform layer/marginal zone in its axonal guidepost function. If reelin served as a substrate for these growing axons in the plexiform layer, perhaps other molecules in the subplate (L1, J1, fibronectin) may have replaced reelin in its axonal guiding function (Allendoerfer and Shatz, 1994). In this way, thalamic terminals would have become located underneath the cortical plate and would have had to enter into the isocortex radially. However, this only produced a vertical entrance to the cortex, not a columnar organization of the inputs. An array of this kind is found in the primitive isocortex of some mammals such as the opossum (Didelphis, marsupialia) and the hedgehog (Erinaceus, insectivora). In these species, thalamic axons enter the cortex radially from the white matter, and then run tangentially in the supragranular layers and especially in the marginal layer for some distance (Ebner, 1969
; Valverde et al., 1986
). Furthermore, in such primitive mammals, layer I is particularly well developed while layer IV is very thin or nonexistent (Valverde and Facal-Valverde, 1986
; Voogd et al., 1998
). In this sense, although a radial entrance to the cortex exists, the synaptic arrangement may still to a large extent be tangential. A second step was required to achieve a complete columnar organization as is observed in the sensory isocortex of more modern mammals.
Step 2: Layer IV and the Development of Synaptic Columnarity
In the sensory and association isocortex of advanced mammals, a granular layer IV featuring spiny stellate cells develops prominently. Layer IV tends to receive the thalamic axons (Voogd et al., 1998), which become organized in columnar arrays. The subplate is related to the development of some such columnar patterns like the ocular-dominance stripes in visual cortex (Ghosh and Shatz, 1992a
,b
, 1993
). Furthermore, during normal visual cortex development, transient circuits are established between the incoming axons, the subplate and cells in layer IV of the cortical plate. This presumably facilitates the subsequent arrival of afferents into the layer IV (Naegele et al., 1988
; Allendoerfer and Shatz, 1994
; Finney et al., 1998
) (see Fig. 5
). In the case of the reeler mouse, in which the subplate cells are abnormally located in the subpial zone above the cortical plate, axons grow past the cortical plate to reach the preplate and then turn back down to contact their appropriate targets (Molnár and Blakemore, 1992
).
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Final Comment |
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In particular, studies of neurogenesis, cell migration, and of particular proteins such as reelin and p35/cdk5 in reptiles and amphibians may shed light on the origins of the mammalian cerebral cortex. Furthermore, the development of allocortical structures (olfactory cortex, hippocampus and the dentate gyrus) that retain features of primitive, reptilian cortex such as the tangential organization of their inputs, but are nevertheless more complex in structure and development than reptilian cortex, also deserve further study (Super et al., 1998).
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Notes |
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Address correspondence to Francisco Aboitiz, Instituto de Ciencias Biomédicas, Facultad de Medicina, Universidad de Chile, 1027 Independencia Avenue, PO Box 70079, Santiago 07, Chile. Email: faboitiz{at}machi.med.uchile.cl.
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Note Added in Proof |
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Guirado S, Dávila JC (1999) GABAergic cell types in the lizard hippocampus. Eur J Morphol 37:89-94.
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