1 Graduate School of Neurosciences Amsterdam, Department of Visual System Analysis, AMC, University of Amsterdam, PO Box 12011, 1100 AA Amsterdam,, 2 The Netherlands Ophthalmic Research Institute PO Box 12141, 1100 AC Amsterdam,, 3 Graduate School of Neurosciences Amsterdam, Netherlands Institute for Brain Research KNAW, Meibergdreef 33, 1105 AZ Amsterdam ZO and, 4 Department of Anatomy, Medical Faculty, Vrije Universiteit Amsterdam, The Netherlands
H. Supèr, Graduate School of Neurosciences Amsterdam, Department of Visual System Analysis, AMC, University of Amsterdam, PO Box 12011, 1100 AA Amsterdam, The Netherlands. Email: h.super{at}ioi.knaw.nl.
![]() |
Abstract |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
In addition to the horizontal layering of the cerebral cortex, it is parcellated vertically. The reptilian cerebral cortex consists of medial, medio-dorsal, dorsal and lateral parts. The medial and medio-dorsal cortices are believed to be homologous to the mammalian hippocampal complex and the lateral cortex to the pyriform cortex. The dorsal reptilian cortex is believed to be homologous to the dorsal neocortex (Medina and Reiner, 2000) and contains several basic cortical areas (e.g. visual, somatic and motor areas). The mammalian hippocampus contains the subicular areas, areas CA1, 2 and 3, hilus and dentate gyrus (Amaral and Insausti, 1990
), which can be further divided into a few subfields (Witter et al., 2000
). The mammalian neocortex contains sensory and motor areas (primary, secondary) and, in more advanced mammalian species, it also contains so-called associational areas (Felleman and Van Essen, 1991
). Many of these neocortical areas can be further subdivided into vertically arranged cortical columns.
Thus, both the reptilian cerebral cortex and the mammalian cerebral cortex (hippocampus and neocortex) derive from the preplate layers and the cortical plate layer. However, the reptilian cortex and the mammalian hippocampus (here together referred to as the allocortex) become three-layered cortices whereas the neocortex develops into a six-layered cortical structure. Furthermore, both reptilian and mammalian cortices are functionally segregated into several regions/areas, where the neocortex shows a higher degree of area segregation than the allocortex, especially in anthropoid primates.
Similar differences in developmental patterns between the reptilian cortex/mammalian hippocampus on the one hand and the neocortex on the other, can be observed to have taken place in the course of evolution. The cortex of some reptiles has expanded laterally in the dorsal part (e.g. pleurodite turtles) and the exact cortical area numbers of extant reptiles may vary across species. However, based on variations in cell density and the configuration of the three layers, the reptilian cortex can be divided into regions typical for representative species of all four reptilian orders, i.e. the medial cortex, the dorso-medial cortex, the dorsal cortex and the lateral cortex. Thus, comparison of the cortices from different reptiles indicates that the cortex of reptiles is a relatively conservative structure where no large expansion or differentiation of the cell-dense cortical plate occurred (Reiner, 1991; Butler, 1994
; Ten Donkelaar, 1998
). However, the data regarding area diversification of advanced reptiles currently available are far from complete and we cannot exclude the possibility of considerable area diversification in extinct reptiles. As in the reptilian cerebral cortex, the evolution of the mammalian hippocampus is not characterized by a large expansion of the cortical plate. The hippocampal plate remained as one cellular layer without differentiating into several cortical laminae and did not expand laterally into numerous areas, but retained its structure containing about five basic areas dentate gyrus including the hilus, CA1, 2 and 3, and subiculum (Stephan and Manolescu, 1980
; Gall, 1990
; Frahm and Zilles, 1994
). The mammalian neocortex, in contrast, has evolved rapidly into a relatively large and complex brain structure containing several primary, secondary and association areas, leading to improved information processing. The evolution of the neocortex is reflected in its expanded size and differentiation of the cortical plate (Rakic, 1988
,1995
; Marin-Padilla, 1992
; Butler, 1994
; Nieuwenhuys, 1994
; Northcutt and Kaas, 1995
; Karten, 1997
). For example, primitive mammals have few neocortical areas (~1020), whereas human primates have ~5070 cortical areas (Felleman and Van Essen, 1991
; Krubitzer, 1995
; Northcutt and Kaas, 1995
; Rakic, 1995
).
Thus, the initial allo- and neocortical evolutionary development is characterized by the appearance of a cell-dense cortical layer. Eventually, however, these two structures emerge with very different sets of cortical differentiation and organization, where the neocortical plate shows a remarkable area and layer differentiation compared to the allocortical plate. Still, there is no satisfactory explanation for this evolutionary differentiation between the allocortex and the neocortex (Supèr et al., 1998b).
![]() |
Hypothesis on Cortical Expansion in Evolution |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The main important change is the location of ingrowth of the main afferent axonal systems into the cortex. In the reptilian cerebral cortex, axons are observed in the marginal zone above the cortical plate (Hall and Ebner, 1965; Ten Donkelaar, 1998
). In the hippocampus, afferents grow mainly into the marginal zone and are guided by preplate cells, which are the transient targets for these ingrowing afferents (Supèr and Soriano, 1994
; Supèr et al., 1998a
). Ingrowing afferents into the neocortex are guided by cells in the subplate (Allendoerfer and Shatz, 1994
; Molnár, 2000
). Therefore, in the allocortex afferents enter and branch mainly in the marginal zone above the cortical plate, whereas in the neocortex afferents run mainly below the cortical plate, from where they ascend and terminate vertically into the neocortex. We postulate that this difference in axonal distribution pattern, together with the inside-out migration of neurons, may have given the neocortex the potential to expand and differentiate.
The Main Ingrowth of Axonal Fibers
As mentioned above, an obvious difference between the allocortex and the neocortex is the way axonal afferents enter the cortex. In the allocortex, axons enter through the marginal zone, whereas in the neocortex the main afferents enter via the subplate (Fig. 3). This indicates that during evolution the distribution pattern of ingrowing axons into the cortex changed from above the cortical plate towards below the cortical plate. This change may have occurred gradually, since in some lower mammals relatively many afferents are seen both above and beneath the cortical plate (Valverde and Facal-Valverde, 1986
; Ten Donkelaar, 1998
). What caused this change of ingrowing afferents during evolution? One of the mechanisms for axonal growth into the cortex is the guidance by efferent axons of pioneer neurons. In the neocortex and hippocampus, neurons in the subplate and marginal zone cells are the first neurons to project outside the cortex and these early projections may guide growing afferents into the cortex (Allendoerfer and Shatz, 1994
; Supèr and Soriano, 1994
; Supèr et al., 1998a
; Soria and Fairen, 2000
). Likewise, in the reptilian dorsal cortex, axonal ingrowth may be guided by the marginal zone neurons (Cordery and Molnár, 1999
). The specific ingrowth of thalamic axons into the neocortical subplate in vivo may be guided by the subplate cells through the handshake principle in the internal capsule where thalamic fibers become intermingled with subplate axons (Molnár, 1998
). Besides the anatomical evidence for this proposal, genetic data may support the handshake principle, since in mutant Tbr1 mice subplate projections are defective and thalamocortical fibers fail to reach the neocortex (Dwyer and O'Leary, 2001
; Hevner et al., 2001
). In addition, the neocortical subplate cells may not only guide afferents from sub-cortical regions, but also ingrowing cortical afferents by the initial projections to other neocortical structures. These latter roles are observed in the neocortex of more advanced mammals, such as domestic cats and ferrets (McConnell et al., 1989
). That the subplate became progressively the target zone for developing axons instead of the marginal zone may be reflected by the thickness of the subplate. The subplate is larger in cats than in rodents, and larger in primates than in cats. For example, in humans the subplate develops to approximately six times the thickness of the cortical plate around 29 weeks of gestation (Mrzljak et al., 1990
), whereas in rodents it consistently remains a relatively thin layer (Uylings et al., 1990
). Furthermore, subplate cells may participate in cortical column formation by their transient connections with particular cortical zones and with layer IV, the main target layer of thalamocortical axons (Ghosh and Shatz, 1992
; Allendoerfer and Shatz, 1994
). In addition, the ganglionic eminence, a structure that is situated between thalamus and neocortex, may act as an intermediate target for growing corticofugal and thalamocortical axons (Metín and Godement, 1996
). Thus, early guidance by subplate cells and guidepost cells in the ganglionic eminence may have rerouted the entrance of growing afferent axons into the neocortex from above the cortical plate towards below the cortical plate in the course of evolution. Recently, Molnár proposed a molecular basis for this evolutionary switch of the entrance of dorsal thalamic fibers into the dorsal cortex (Molnár, 2000
).
|
Laminar Expansion of the Neocortex
During their radial migration, the cortical neurons have very small and bipolar elongated morphologies (Mrzljak et al., 1990; Uylings et al., 1990
; Auladell et al., 1995
; Uylings and Delalle, 1997
), which may facilitate their way up through the cell-dense cortical plate. After migration, when neurons settle in the cortical plate, they start to mature and a major outgrowth of dendritic and axonal branches occurs. The main neuronal cell type of the cerebral cortex, the pyramidal cell, grows a characteristically apical dendrite towards the pial surface that ramifies abundantly, resulting in an apical tuft in the marginal zone. These neurons maintain their connection with the marginal zone during development and only during late developmental periods do some of the neurons retract their apical dendrite from the marginal zone (O'Leary and Koester, 1993
). This suggests that the connection with the marginal zone is needed for the initial maturation, survival and/or processing capacities of these cortical cells.
The cortex has expanded radially in the course of evolution (Stephan and Manolescu, 1980; Hofman, 2001
), although this radial expansion is limited compared to the lateral expansion, especially in the neocortex. The radial expansion occurred by adding extra neurons to the cortical plate, which could be the result of tangential migration of non-pyramidal cells from the lateral ganglionic eminence into the cortex (Parnavelas, 2000
; Pleasure et al., 2000
). However, alterations in the proliferation kinetics in the ventricular zone resulting in an expanded size of the precursor pool seem to be essential for the expansion of the neocortex (Caviness et al., 1995
; Kornack and Rakic, 1998
). The radial expansion of the neocortical plate in the course of evolution by the addition of extra neurons is supported by the finding that during development the radial migration appears to consist of two waves of cohorts of migrating neurons, one for the lower cortical layers and one for the upper cortical layers (Bayer and Altman, 1991
; McConnell, 1995
; Frantz and McConnell, 1996
). Moreover, Ebner proposed that the dorsal cortex of reptiles lacked the neuronal types found in the superficial layers of the mammalian neocortex (Ebner, 1976
). This is supported by immunocytochemical studies from Reiner, who suggested that the neocortex in mammals was characterized by the addition of neurons to layer IIIV in the reptilemammal lineage (Reiner, 1991
).
In addition to the extra neurons, the number of axons in the cerebral cortex also increased during evolution, resulting in a radial expansion of the cortex. In the primate hippocampus, for example, the marginal zone contains more axons than the hippocampus in insectivores (Stephan and Manolescu, 1980) and the primate neocortical subplate contains many more axonal fibers than the subplate of lower mammals (Mrzljak et al., 1990
; Ten Donkelaar, 1998
). In the neocortex, the increase of axonal fiber numbers is likely to be related to the increase of cortical areas with their feedforward and feedback connections to other cortical areas. Apart from the evolutionary radial expansion of the cortical plate by the addition of more neurons and axons, the cortex also increased in thickness by the formation of extra cortical sub-layers. This, however, occurred in the neocortex and not in the allocortex. This laminar differentiation is related to the growth of axonal afferents into the cortical plate terminating into particular cortical layers. For example, the developing neocortical plate does not differentiate into well-segregated layers when thalamo-cortical fibers are absent (Dehay et al., 1991
; Windrem and Finlay, 1991
). Thus, in the course of evolution, the cortical plate increased in thickness by the addition of extra neurons and axons. The neocortical plate, however, also differentiated into cortical sublayers, whereas the hippocampal plate and reptilian cerebral cortical plate remained essentially rather undifferentiated cell layers.
We postulate a mechanistic view where the extra addition of both cortical neurons and axonal fibers have been crucial factors in the laminar differentiation of the cortical plate in the course of evolution. When the axon fiber bundles run above the cortical plate, as they do in the hippocampus, the later-generated neurons destined for the upper level of the hippocampal cortical plate may have too limited space to expand radially and to form an additional cortical layer. These neurons are able to migrate through the cell-dense cortical plate due to their elongated and slender shape. However, upon their arrival in the superficial part of the hippocampal cortical plate they are tightly enclosed by the axonal strata above them and by the more differentiated lower cortical zones of the hippocampal plate below them. This may result in a limited space for the cell-dense cortical plate to be able to create additional layers, especially during evolution, when extra neurons and axons are added to the cortex. Thus, the increasing numbers of afferent axons in the marginal zone may have been an important limitation for the radial expansion of the cortical plate during evolution (Fig. 3A,C). This may be supported by the finding that the hippocampal marginal zone expanded in the course of evolution due to the increasing number of incoming fibers, whereas radial expansion of the hippocampal plate only happened because cortical neurons dispersed towards the ventricular zone and not by a large radial extension into different laminae (Stephan and Manolescu, 1980
; Gall, 1990
; Frahm and Zilles, 1994
). In the reptilian cortex, cortical neurons follow an outside-in sequence, where late -generated neurons settle in the lower level of the cortical plate. Thus, earlier-generated cortical neurons and axons do not enclose these late-generated cortical neurons, but both are on top of them.
A further important factor in cortical layering is the functional segregation of the different cortical inputs. The laminar differentiation of the cortical plate is linked with the specific ingrowth and termination of axons into a particular cell layer without entering other cortical layers. To establish layer-specific connections, axons must therefore grow into the cortical plate and make contact specifically with a subset of cortical neurons without synapsing onto other neurons. However, in the reptilian cortex as well as in the hippocampus, the axons in the marginal zone are in the same zone as the apical dendrites of almost all cortical pyramidal neurons, which is a main receptive site of the neuron (see Fig. 3). Thus in the allocortex, the physical segregation into discrete axonal-dendritic systems is not feasible. Therefore, axons entering the same zone as the receptive fields of the cortical neurons form a limitation on cortical laminar differentiation of the cell-dense cortical plate of the mammalian hippocampus and reptilian cortex.
In contrast, in the neocortex, the newly arrived neurons that settle in the upper level of the cortical plate are not enclosed between major fiber bundles in the subplate and the expanding lower cortical layers. The ingrowing afferents run below the cortical plate and thus the axons do not have to avoid numerous apical dendrites from cortical neurons. Afferent fibers guided by the subplate cells can ascend vertically into the developing cortical plate after their arrival at the correct areal position (Catalano et al., 1996). Thus, both the radial inside-out migration of cortical neurons and the ascending axons from the subplate follow the same direction of the radial maturation of the cortex. The neocortex therefore remains an open system where, during evolution, extra neurons and axons can be added without obstructing the formation of new (sub)layers.
CajalRetzius Cells and the Inside-out Genesis of the Neocortical Plate
To develop the cortical plate, the majority of post-mitotic neurons migrate radially outward from the ventricular zone into the telencephalic pallium (Rakic, 1971; Bayer and Altman, 1991
; Parnavelas, 2000
). During evolution, this cortical migration has become more radially aligned (Rakic, 1974
; Goffinet et al., 1986
; Ten Donkelaar, 1998
) and a better radial alignment has been associated with the inside-out migration pattern (Goffinet et al., 1986
; Butler, 1994
). Recently, it has become clear that pioneer neurons (in particular Cajal-Retzius cells) play an important role in the control of the radial histogenesis of the cortical plate (Ogawa et al., 1995
; Supèr et al., 1997a
,2000
; Frotscher, 1998
; Aboitiz, 1999a
). Cajal-Retzius neurons organize the radial glial scaffold (Soriano et al., 1997
; Supèr et al., 2000
) and support the inside-out order of neuronal migration (Ogawa et al., 1995
). Here we will discuss observations suggesting that the Cajal Retzius cells achieved phenotypes that are more complex during evolution, which may have contributed to the inside-out corticogenesis.
Cajal-Retzius cells are present in the marginal zone throughout the entire cerebral cortex. However, the morphology of the Cajal-Retzius cell is different for different species and cortical areas. In reptiles, Cajal-Retzius cells are simple bipolar horizontal neurons in the outer part of the marginal zone. In the dentate gyrus of the hippocampal formation, which chiefly resembles the reptilian cortex since neurogenesis is prolonged and neurons here settle in the dentate cortical plate following an outside-in pattern of migration, Cajal-Retzius cells also display simple bipolar shapes (Von Haebler et al., 1993) (Mrzljak and Uylings unpublished observations in human brain). The morphology and peptide expression of Cajal-Retzius cells tend to be more complex in the hippocampus proper and even more so in the neocortex (Uylings et al., 1990
; Soriano et al., 1994
; Berger and Alvarez, 1996
; Supèr et al., 1997b
). Furthermore, Cajal-Retzius cells have morphologies that are more intricate in the primate neocortex than in, for example, rodents. In addition, they are divided into several subtypes (Marín-Padilla, 1988
; Huntley and Jones, 1990
; Del Río et al., 1995
; Uylings and Delalle, 1997
; Meyer et al., 1998
,1999
). Thus, in the course of evolution, Cajal-Retzius cells may have become more specialized in their contribution to the radial cortical organization, resulting in the inside-out histogenesis of the cortical plate.
Lateral Expansion of the Neocortex by Areal Segregation
The evolutionary increase in cortical size is mainly due to a lateral expansion (Rakic, 1988; Hofman, 2001
). This lateral expansion of the cortex is believed to be the result of the enlargement of existing areas by the production of extra cortical neurons, by the segregation of existing areas into additional ones and by further specification of functional cortical domains (Ebbesson, 1984
; Rakic, 1988
, 1995
; Krubitzer et al., 1993
; Caviness et al., 1995
; Krubitzer, 1995
; Northcutt and Kaas, 1995
). The proposed evolutionary mechanisms by which new cortical fields are created are related to the progressive number of axonal fiber bundles, where fiber bundles become segregated and terminating axons become spatially restricted by pruning after exuberant growth (Ebbesson, 1984
; Krubitzer et al., 1993
; Krubitzer, 1995
; Innocenti, 1995
). These events can be achieved by a further specialization of molecular guiding cues that attract or repel axons and by the segregation of overlapping axonal branches, for example by competitive neuronal activity during development. To create new areas during evolution, the axonal input has to be segregated vertically. We will argue that the development of topographic maps is facilitated when axons enter the cortical plate from below.
Targeting fiber bundles to discrete cortical areas involves the expression of a tangential mosaic pattern of positional cues and neural activity (Catalano and Shatz, 1998). It has been shown that a tangential pattern of molecular cues is expressed in the subplate and marginal zone (Allendoerfer and Shatz, 1994
; Soria and Fairen, 2000
). In order to reach their appropriate cortical area in the allocortical design, the guided afferent fibers in the marginal zone inevitably cross the fields of the apical terminal dendrites in other cortical regions (Fig. 3A,C
). Axons enter the marginal zone branch at several points on their path and can easily form synaptic contacts with the cortical apical dendrites and induce their sprouting (Mattson et al., 1988
; Fletcher et al., 1994
). Cortical neurons must therefore express a multitude of molecular cues in order to establish and maintain area- and layer-specific axon-dendritic connections. This is inefficient from a molecular point of view, as well as rather implausible, especially since specificity of axonal-dendritic connections depends on competitive interactions. Thus, the parcellation of the cortex into additional areas by the functional segregation of new incoming fiber bundles in the marginal zone would involve a complicated spatio-temporal expression pattern of molecular cues by growing apical dendrites and axons.
In the neocortical design, the main afferent systems guided by subplate neurons enter and run below the cortical plate, where there are no extensive dendritic receptive fields of cortical plate neurons (Fig. 3B,D). In order to reach a particular cortical region, the ingrowing axons can pass below other cortical areas in the subplate without encountering receptive pyramidal cell dendrites belonging to these areas. In this situation, numerous distinct fiber systems can be directed specifically to different cortical regions without having the problem of avoiding a-specific connections. Differential expression of guiding cues in the subplate can specifically target axons and, after reaching their appropriate area, the axons can ascend vertically into the cortical plate and synapse more specifically onto the target cells in their cortical area, as discussed above. This radial arrangement of ascending axons in the neocortex may have permitted the development of multiple instances of reciprocal convergent and divergent cortical pathways, which produces more complex processing. Moreover, the cortical areas can be further divided into functional segregated columns. These columns are formed by the physical segregation of axons due to the elimination of exuberant axonal fiber growth. This occurs under the influence of competitive interactions based on environmental cues and neuronal activity (Jhaveri et al., 1991
; Killackey et al., 1995
). The physical segregation of axons into vertically defined columns is almost inconceivable in the situation in which all axons run and terminate in the same zone as cortical dendrites (see Fig. 3
). Active segregation of cortical areas into distinct columns is facilitated if axons can enter separately from below the cortical plate, via the subplate, as happens in the neocortex. Therefore, we propose that area specification and formation of new cortical domains by axonal segregation of afferents is more limited in the allocortical design than in the neocortical one and thus did not allow the allocortex to expand laterally.
In addition to the proposed potential of cortical differentiation, the entrance of the axonal fibers via the subplate guarantees that the axons travel over a relatively shorter distance in a laterally expanding cortex and provides an immediate benefit in the form of increased processing velocities. The paths that the afferents follow via the marginal zone would become too long in a laterally expanding cortex, especially in the case of a gyrencephalic cortex (Aboitiz, 1999b). Moreover, to keep the increase in cortex size in a relatively compact 3D space (Thompson, 1966
), the neocortical expansion in brains >34 cm3 is coupled with cortical folding (gyrification) of the cerebral cortex (Hofman, 2001). Recently, Van Essen (Van Essen, 1997
) suggested that tension along the axonal afferents under the cortical layers is a driving force for cortical convolution. Therefore, axons running below the cortical plate may have relieved a functional constraint of the major axon bundles running in the marginal zone that limited lateral expansion of the neocortex.
![]() |
Conclusion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Notes |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Aboitiz F (1999b) Evolution of isocortical organization. A tentative scenario including roles of Reelin, p35/cdk5, and the subplate zone. Cereb Cortex 9:655661.
Allendoerfer KL, Shatz CJ (1994) The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Ann Rev Neurosci 17:185218.[ISI][Medline]
Amaral DG, Insausti R (1990) Hippocampal formation. In: The human nervous system (Paxinos G, ed.), pp. 711755. San Diego, CA: Academic Press.
Auladell C, Martinez A, Alcantara S, Supèr H, Soriano E (1995) Migrating neurons in the developing cerebral cortex of the mouse send callosal axons. Neuroscience 64:10911103.[ISI][Medline]
Bayer SA (1980) Development of the hippocampal region in the rat: I. Neurogenesis examined with 3H-thymidine autoradiography. J Comp Neurol 190:87114.[ISI][Medline]
Bayer SA, Altman J (1991) Neocortical development. New York: Raven Press.
Berger B, Alvarez C (1996) Neurochemical development of the hippocampal region in the fetal rhesus monkey. III: Calbindin-D28K, calretinin and parvalbumin with special mention of Cajal-Retzius cells and retrosplenial cortex. J Comp Neurol 366:674699.[ISI][Medline]
Bishop KM, Goudreau G, O'Leary DDM (2000) Regulation of area identity in the mammalian neocortex by Emx2 and Pax6. Science 288: 344349.
Blanton MG, Kriegstein AR (1991a) Morphological differentiation of distinct neuronal classes in embryonic turtle cerebral cortex. J Comp Neurol 310:550570.[ISI]
Blanton MG, Kriegstein AR (1991b) Appearance of putative amino acid neurotransmitters during differentiation of neurons in embryonic turtle cerebral cortex. J Comp Neurol 310:571592.[ISI][Medline]
Butler AB (1994) The evolution of the dorsal pallium in the telencephalon of amniotes: cladistic analysis and a new hypothesis. Brain Res Rev 19:66101.[ISI][Medline]
Catalano SM, Shatz CJ (1998) Activity-dependent cortical target selection by thalamic axons. Nature 281:559562.
Catalano SM, Robertson RT, Killackey HP (1996) Individual axon morphology and thalamocortical topography in developing rat somatosensory cortex. J Comp Neurol 366:3653.
Caviness VS Jr, Takahashi T, Nowakowski RS (1995) Numbers, time and neocortical neurogenesis: a general developmental and evolutionary model. Trends Neurosci 18:379383.[ISI][Medline]
Cordery P, Molnar Z (1999) Embryonic development of connections in turtle pallium. J Comp Neurol 413:2654.[ISI][Medline]
Dehay C, Horsburgh G, Berland, M, Killackey H, Kennedy H (1991) The effects of bilateral enucleation in the primate fetus on the parcellation of visual cortex. Dev Brain Res 62:137141.[ISI][Medline]
Del Rio JA, Martinez A, Fonseca M, Auladell C, Soriano E (1995) Glutamate-like immunoreactivity and fate of Cajal-Retzius cells in the murine cortex as identified with calretenin antibody. Cereb Cortex 1:1321.
Dwyer ND, O'Leary DDM (2001) Tbr1 conducts the orchestration of early cortical development. Neuron 29:309311.[ISI][Medline]
Ebbesson SOE (1984) Evolution and ontogeny of neural circuits. Behav Brain Sci 7:321366.[ISI]
Ebner FF (1976) The forebrain of reptiles and mammals. In: Evolution of brain and behavior in vertebrates (Masterton RB, Bitterman ME, Campbell CBG, Hotton N, eds), pp. 147167. New York: John Wiley.
Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex 1:147.[Abstract]
Fletcher TL, De Camilli P, Banker G (1994) Synaptogenesis in hippocampal cultures: evidences indicating that axons and dendrites become competent to form synapses at different stages of neuronal development. J Neurosci 14:66956706.[Abstract]
Frahm HD, Zilles K (1994) Volumetric comparison of hippocampal regions in 44 primate species. J Brain Res 3:343354.
Frantz GD, McConnell SK (1996) Restriction of late cerebral cortical progenitors to an upper-layer fate. Neuron 17:5561.[ISI][Medline]
Frotscher M (1998) Cajal-Retzius cells, Reelin, and the formation of layers. Curr Opin Neurobiol 8:570575.[ISI][Medline]
Gall C (1990) Comparative anatomy of the hippocampus with special reference to differences in the distributions of neuroactive peptides. In: Cortex (Jones EG, Peters A, eds), vol. 8b, pp. 167213. New York: Plenum Press.
Ghosh A, Shatz CJ (1992) Involvement of subplate neurons in the formation of ocular dominance columns. Science 255:14411443.[ISI][Medline]
Giger RJ, Wolfer DP, de Wit GMJ, Verhaagen J (1996) Anatomy of rat semaphorin III/colapsin-1 mRNA expression and relationship to developing nerve tracts during neuroembryogenesis. J Comp Neurol 375:378392.[ISI][Medline]
Goffinet AM (1983) The embryonic development of the cortical plate in reptiles: a comparative study in Emys orbicularis and Lacerta agilis. J Comp Neurol 215:437452.[ISI][Medline]
Goffinet AM, Daumerie CH, Langerwerf B, Pieau C (1986) Neurogenesis in reptilian cortical structures: 3H-thymidine autoradiographic analysis. J Comp Neurol 243:106116.[ISI][Medline]
Hall WC, Ebner FF (1965) Thalamotelencephalic projections in the turtle (Pseudemys scripta). J Comp Neurol 140:101122.
Hevner RF, Shi L, Justice N, Hsueh Y-P, Sheng M, Smiga S, Bulfone A, Goffinet AM, Campagnoni AT, Rubenstein JLR (2001) Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29:353366.[ISI][Medline]
Hofman MA (2001) Evolution and complexity of the human brain: some organizing principles. In: Brain evolution and cognition (Roth G, Wullimann MF, eds), pp. 501521. New York: Wiley.
Huntley GW, Jones EG (1990) Cajal-Retzius neurons in the developing monkey neocortex show immunoreactivity for calcium binding proteins. J Neurocytol 19:200212.[ISI][Medline]
Innocenti GM (1995) Exuberant development of connections, and its possible permissive role in cortical evolution. Trends Neurosci. 18:397401.[ISI][Medline]
Jhaveri S, Erzurumlu RS, Crossin K (1991) Barrel construction in rodent neocortex: role of thalamic afferents versus extra-cellular matrix molecules. Proc Nat Acad Sci USA 88:44894493.[Abstract]
Karten HJ (1997) Evolutionary developmental biology meets the brain: the origins of mammalian cortex. Proc Natl Acad Sci USA 94:28002804.
Killackey HP, Rhoades RW, Benett-Clarke CA (1995) The formation of a cortical somatotopic map. Trends Neurosci 18:402407.[ISI][Medline]
Kornack DR, Rakic P (1998) Changes in cell-cycle kinetics during the development and evolution of primate neocortex. Proc Nat Acad Sci USA 95:12421246.
Kostovi I, Rakic P (1990) Developmental history of transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 297:441470.[ISI][Medline]
Krubitzer LA (1995) The organization of neocortex in mammals: are species differences really so different? Trends Neurosci 18:408417.[ISI][Medline]
Krubitzer LA, Calford, MB, Schmid LM (1993) Connections of somatosensory cortex in megachiropteran bats: the evolution of cortical fields in mammals. J Comp Neurol 327:473506.[ISI][Medline]
Mallamaci A, Muzio L, Chun-Hung C, Parnavelas J, Boncinelli E (2000) Area identity shifts in the early cerebral cortex of Emx2/ mutant mice. Nature Neurosci 7:679686.
Marín-Padílla M (1978) Dual origin of the mammalian neocortex and evolution of the cortical plate. Anat Embryol 152:109126.[ISI][Medline]
Marín-Padílla M (1984) Neurons of layer I. A developmental analysis. In: Cerebral cortex, vol. I. Cellular components of the cerebral cortex (Peters A, Jones EG, eds), pp. 447478. New York: Plenum Press.
Marín-Padílla M (1988) Early ontogenesis of the human cerebral cortex. In: Cerebral cortex (Peters A, Jones EG, eds), pp. 130. New York: Plenum Press.
Marín-Padílla M (1992) Ontogenesis of the pyramidal cell of the mammalian neocortex and developmental cytoarchitectonics: a unifying theory. J Comp Neurol 321:223240.[ISI][Medline]
Mattson MP, Lee RE, Adams ME, Guthrie PB, Kater SB (1988) Interactions between entorhinal axons and target hippocampal neurons: a role for glutamate in the development of hippocampal circuitry. Neuron 1:865876.[ISI][Medline]
McConnell SK (1995) Constructing the cerebral cortex: neurogenesis and fate determination. Neuron 15:761768.[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]
Medina L, Reiner A (2000) Do birds possess homologues of mammalian primary visual, somatosensory and motor cortices? Trends Neurosci 23:112.[ISI][Medline]
Métin C, Godement P (1996) The ganglionic eminence may be an intermediate target for corticofugal and thalamocortical axons. J Neurosci 16:32193235.
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 on the fetal and neonatal rat cortex. J Comp Neurol 397:493518.[ISI][Medline]
Meyer G, Goffinet AM, Fairén A (1999) What is a Cajal-Retzius cell? A reassessment of a classical cell type based observations in the developing neocortex. Cereb Cortex 9:765775.
Molnár Z (1998) Development of thalamocortical connections. Berlin: Springer.
Molnár Z (2000) Development and evolution of thalamocortical interactions. Eur J Morphol 38:313320.[ISI][Medline]
Monuki ES, Walsh C (2000) Proto-mapping the areas of cerebral cortex: transcription factors make the grade. Nature Neurosci 7:640641.
Mrzljak L, Uylings HBM, Van Eden CG, Judas M (1990) Neuronal development in human prefrontal cortex in prenatal and postnatal stages. In: Progress in brain research, vol. 85. The prefrontal cortex: its structure, function and pathology (Uylings HBM, Van Eden CG, De Bruin JPC, Corner MA, Feenstra MGP, eds), pp. 185222. Amsterdam: Elsevier.
Nacher J, Ramirez C, Molowny A, Lopez-Garcia C (1996) Ontogeny of somatostatin immunoreactive neurons in the medial cerebral cortex and other cortical areas of the lizard Podarcis hispanica. J Comp Neurol 374:118135.[ISI][Medline]
Nieuwenhuys R (1994) The neocortex. Anat Embryol 190:307337.[ISI][Medline]
Northcutt RG, Kaas JH (1995) The emergence and evolution of mammalian neocortex. Trends Neurosci 18:373379.[ISI][Medline]
Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaka K, Yamamoto H, Mikoshiba K (1995) The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14:899912.[ISI][Medline]
O'Leary DDM, Koester SE (1993) Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex. Neuron 10:9911006.[ISI][Medline]
O'Leary DDM, Schlaggar BL, Tuttle R (1994) Specification of neocortical areas and thalamocortical connections. Ann Rev Neurosci 17: 419439.[ISI][Medline]
Parnavelas JG (2000) The origin and migration of cortical neurones: new vistas. Trends Neurosci 23:126131.[ISI][Medline]
Pleasure SJ, Anderson S, Hevner R, Bagri A, Marin O, Lowenstein DH, Rubenstein JLR (2000) Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 28:727740.[ISI][Medline]
Rakic P (1971) Guidance of neurons migrating to the fetal monkey neocortex. Brain Res 33:471476.[ISI][Medline]
Rakic P (1974) Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183:425427.[ISI][Medline]
Rakic P (1988) Specification of cerebral cortical areas. Science 241:170176.[ISI][Medline]
Rakic P (1995) A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci 18:383388.[ISI][Medline]
Reep RL (2000) Cortical layer VIII and persistent subplate cells in mammalian brains. Brain Behav Evol 56:212234.[ISI][Medline]
Reiner A (1991) A comparison of neurotransmitter-specific and neuro-peptide-specific neuronal cell types present in the dorsal cortex in turtles with those present in the isocortex in mammals: implications for the evolution of isocortex. Brain Behav Evol 38:5391.[ISI][Medline]
Rickmann 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]
Rubenstein JLR, Anderson S, Shi L, Miyashita-Lin E, Bulfone A, Hevner R (1999) Genetic control of cortical regionalization and connectivity. Cereb Cortex 9:524532.
Sanes JR, Yamagata M (1999) Formation of lamina-specific synaptic connections. Curr Opin Neurobiol 9:7987.[ISI][Medline]
Skutella T, Nitsch R (2001) New molecules for hippocampal development. Trends Neurosci 24:107113.[ISI][Medline]
Soria JM, Fairen A (2000) Cellular mosaics in the rat marginal zone define an early neocortical territorialization. Cereb Cortex 10:400412.
Soriano E, Del Río JA, Martinez A, Supèr H (1994) Organization of the embryonic and early postnatal murine hippocampus: I. Immunocyto-chemical characterization of neuronal populations in the subplate and marginal zone. J Comp Neurol 342:571595.[ISI][Medline]
Soriano E, Alvarado-Mallart RM, Dumesnil N, Del Rio JA, Sotelo C (1997) Cajal-Retzius cells regulate the radial glia phenotype in the adult and developing cerebellum and alter granule cell migration. Neuron 18:563677.[ISI][Medline]
Stephan H, Manolescu J (1980) Comparative investigations on hippocampus in insectivores and primates. Z Mikrosk Anat Forsch 94:10251050.[ISI][Medline]
Supèr H, Soriano E (1994) Organization of the embryonic and early postnatal murine hippocampus: II. Development of entorhinal, commissural, and septal connections studied with the lipophilic tracer DiI. J Comp Neurol 344:101120.[ISI][Medline]
Supèr H, Perez Sust P, Soriano E (1997a) Survival of Cajal-Retzius cells after cortical lesions in newborn mice: a possible role for Cajal-Retzius cells in brain-repair. Dev Brain Res 98:914.[ISI][Medline]
Supèr H, Martinez A, Soriano E (1997b) Degeneration of Cajal-Retzius cells in the developing cerebral cortex of the mouse after ablation of meningeal cells by 6-hydroxydopamine. Dev Brain Res 98:1520.[ISI][Medline]
Supèr H, Martinez A, Del Rio JA, Soriano E (1998a) Involvement of distinct pioneer neurons in the formation of layer-specific connections in the hippocampus. J Neurosci. 18:46164626.
Supèr H, Soriano E, Uylings HBM. (1998b) The functions of the preplate in development and evolution of the neocortex and hippocampus. Brain Res Rev 27:4064.[ISI][Medline]
Supèr H, Del Rio JA, Martinez A, Pérez Sust P, Soriano E (2000) Disruption of neuronal migration and radial glia in the developing cerebral cortex following ablation of Cajal-Retzius cells. Cereb Cortex 10:602613.
Ten Donkelaar HJ (1998) Reptiles. In: The central nervous system of vertebrates (Nieuwenhuys R, Ten Donkelaar HJ, Nicholson C, eds), vol. 2, pp. 13151524. Berlin: Springer.
Thompson D'Arcy W. (1966) On growth and form, abridged edn (Bonner, JT, ed.). Cambridge: Cambridge University Press.
Uylings HBM, Delalle I (1997) Morphology of NPY-ir neurons and fibers in human prefrontal cortex during prenatal and postnatal development. J Comp Neurol 397:523540.
Uylings HBM, Van Eden CG, Parnavelas JG, Kalsbeek A (1990) The prenatal and postnatal development of rat cerebral cortex. In: The cerebral cortex of the rat (Kolb E, Tees RC, eds), pp. 3576. Cambridge, MA: MIT Press.
Valverde F, Facal-Valverde MV (1986) Neocortical layers I and II of the hedgehog (Erinaceus europaeus). I. Intrinsic organization. Anat Embryol 173:413430.[ISI][Medline]
Van Essen DC (1997) A tension based theory of morphogenesis and compact wiring in the central nervous system. Nature 385:313318.[ISI][Medline]
Von Haebler D, Stabel J, Draguhn A, Heinemann U (1993) Properties of horizontal cells transiently appearing in the dentate gyrus during ontogenesis. Exp Brain Res 94:3342.[ISI][Medline]
Windrem MS, Finlay BL (1991) Thalamic ablations and neocortical development: alterations of cortical cytoarchitecture and cell number. Cereb Cortex 1:230240.[Abstract]
Witter MP, Wouterlood FG, Naber PA, Van Haeften T (2000) Anatomical organization of the parahippocampalhippocampal network. Ann NY Acad Sci 911:124.
Yanes C, Monzon-Mayor MS, Ghandour J, De Barry J, Gombos G (1990) Radial glia and astrocytes in developing and adult telencephalon of the lizard Gallotia galloti as revealed by immunohistochemistry with anti-GFAP and anti-vimentin antibodies. J Comp Neurol 295:559568.[ISI][Medline]