Feature Article: Comparative Development of the Mammalian Isocortex and the Reptilian Dorsal Ventricular Ridge. Evolutionary Considerations

Francisco Aboitiz

Programa de Morfología, Instituto de Ciencias Biomédicas, Facultad de Medicina, Universidad de Chile, Santiago, Chile

Address correspondence to Francisco Aboitiz, 1027 Independencia Ave., PO Box 70079, Santiago 07, Chile. Email: faboitiz{at}machi.med.uchile.cl.


    Abstract
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 Abstract
 Introduction
 Theories of Homology between...
 Criteria for homology
 Developmental Problems Raised by...
 Development of the Mammalian...
 The Intermediate Territory of...
 Discussion
 References
 
There has been a long debate about a possible homology between parts of the dorsal ventricular ridge (DVR) of reptiles and birds, and parts of the mammalian isocortex. Correspondence between these structures was originally proposed on the basis of connectional similarities between the DVR of birds and the mammalian auditory and extrastriate visual isocortical areas. Furthermore, the proposal of homology includes the possible embryological similarity of cells that give rise to the DVR and cells that give rise to the isocortex. Against this concept it has been claimed that the DVR and the isocortex originate in topographically different pallial compartments, an interpretation that is supported by recent developmental and molecular data. Other studies indicate that migrating cells can cross the borders between adjacent developmental compartments: cells that originate in subcortical components contribute a number of interneurons to the developing isocortex via tangential migration. This mechanism might reconcile the proposed homology with the developmental evidence, since cells originating in one compartment (the one corresponding to DVR) may become included in structures generated in a different compartment (the one corresponding to isocortex). However, there is no evidence in mammals of a structure homologous to the embryonic DVR that can produce isocortical neurons. In order to fully clarify the problem of isocortical origins, further comparative studies are needed of the embryonic development of the lateral and dorsal aspects of the cerebral hemispheres in amphibians, reptiles and mammals.


    Introduction
 Top
 Abstract
 Introduction
 Theories of Homology between...
 Criteria for homology
 Developmental Problems Raised by...
 Development of the Mammalian...
 The Intermediate Territory of...
 Discussion
 References
 
The cerebral hemispheres are a shared-derived feature of the vertebrate brain, and apparently appeared in conjunction with paired sense organs and other structures like the neural crest derived vertebrate head (Gans and Northcutt, 1983Go). They are divided into a ventral moiety or subpallium, and a dorsal component called the pallium. Interestingly, the cerebral hemispheres — particularly the pallium — are among the most diversified brain structures of vertebrates, and therefore establishing homologies between telencephalic components in diverse vertebrate classes has been a long-standing issue in comparative neuroanatomy (Ariëns Kappers et al., 1936Go; Northcutt, 1981Go; Aboitiz, 1992Go, 1995Go; Striedter, 1997Go; Nieuwenhuys et al., 1998Go). Several theories of vertebrate brain evolution have been proposed (Butler, 1994Go; Aboitiz, 1995Go; Striedter, 1997Go; Nieuwenhuys et al., 1998Go), each emphasizing distinct possible correspondences among hemisphere components. Most disagreements between the different authors are based on the diverse criteria used to determine homology between telencephalic components. Often these criteria do not match, which has given rise to long-standing debates.

In light of recent evidence, the present paper takes up a controversy regarding the evolutionary origin of mammalian isocortex from a reptilian ancestor. Based on similarities in sensory connectivity, Karten and Nauta proposed homology between parts of the mammalian isocortex and the avian dorsal ventricular ridge (DVR; see Fig. 1Go), a prominent telencephalic structure present in birds and reptiles (Karten, 1968Go, 1969Go; Nauta and Karten, 1970Go). This hypothesis implies that the isocortex has a similar embryonic and evolutionary origin as the avian/reptilian DVR. (Taxonomically, birds derive from reptiles, and together they form the taxon Sauropsida whose sister-group is the class Mammalia.)



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Figure 1.  Diagram of the cerebral hemisphere of a reptile (Gekko gecko). The lateral cortex (L) receives projections from the olfactory bulb and is comparable to the mammalian olfactory cortex. The dorsal cortex (D) – its lateral aspect, and the pallial thickening which is particularly prominent in turtles and is not shown here – receive visual projections from the dorsal lateral geniculate nucleus (Ulinski, 1990), and have been proposed to be comparable to the primary visual cortex or striate cortex of mammals (Nauta and Karten, 1970Go). The medial (M) and the dorsomedial (DM) cortices (and also the medial aspect of the dorsal cortex) (Guirado et al., 1998Go) are considered to be homologues to the mammalian hippocampal formation (Nieuwenhuys et al., 1998Go). The anterior dorsal ventricular ridge (ADVR) has been compared to several mammalian telencephalic structures, among them the corpus striatum (Ariëns Kappers et al., 1936Go), the extrastriate isocortex (Karten, 1969Go), the basolateral amygdala (Bruce and Neary, 1995Go; Smith-Fernández et al., 1998Go), and the endopiriform nucleus (Striedter, 1997Go). Medial is to the left. S, striatum; Se, septum; V, lateral ventricle. Redrawn from Butler (Butler, 1976Go).

 
Two recent reports are of special relevance to the above proposal. In one of these (Anderson et al., 1997aGo), a population of subpallial cells is identified that migrate dorsally and medially into the developing isocortex and give rise to a significant proportion of the GABAergic isocortical neurons. This alternative raises the possibility that cells originating in the lateral wall of the hemisphere (where the reptilian DVR originates) take a similar migratory route to more dorsal and medial positions (where the isocortex develops), which would support the concept of developmental similarity between cells in the reptilian DVR and cells in the isocortex. The latter hypothesis implies that there is an embryonic structure in the mammalian hemisphere that corresponds to the embryonic primordium of the reptilian DVR. In the second report (Smith-Fernández et al., 1998Go), an intermediate territory (IT) between the pallium and the subpallium is described in the developing telencephalon, which gives rise to part of the DVR (anterior DVR) in reptiles but not to the isocortex in mammals, indicating that these two structures originate in different embryonic compartments. Interestingly, in mammals the IT apparently disappears during late development, which complicates the possibility of determining a mammalian homologue of the embryonic DVR and supports the early proposal that some parts of the reptilian DVR have no mammalian counterpart (Aboitiz, 1992Go, 1995Go).


    Theories of Homology between the Dorsal Ventricular Ridge and the Isocortex
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 Abstract
 Introduction
 Theories of Homology between...
 Criteria for homology
 Developmental Problems Raised by...
 Development of the Mammalian...
 The Intermediate Territory of...
 Discussion
 References
 
The reptilian and avian DVR was originally believed to be part of the corpus striatum (Ariëns Kappers et al., 1936Go), but connectional and histochemical studies revealed a pallial nature for this structure (Karten, 1969Go; Parent and Olivier, 1970Go). The DVR has two main components: an anterior part (ADVR) and a basal or posterior part (PDVR) (Ulinski, 1983Go). The ADVR is a periventricular structure located immediately dorsal to the corpus striatum (see Figs 1 and 3GoGo) that receives visual, auditory and somatosensory projections; these are relayed in the midbrain and then in distinct thalamic nuclei before reaching the telencephalon. In some species (turtles, lacertid lizards, Sphenodon), the ADVR consists of a core, nuclear structure and a periventricular cell-poor layer in which cells are organized in clusters, while in other species, such as iguanid lizards, this structure is fully nuclear and cell clusters are spread evenly through it (Ulinski, 1983Go; Nieuwenhuys et al., 1998Go). The PDVR has been related to the amygdaloid complex of mammals (Lanuza et al., 1998Go, 1999Go; Nieuwenhuys et al., 1998Go).



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Figure 3.  (A) Coronal section of the adult telencephalon of Liolaemus tenuis, an iguanid lizard. (B) Right telencephalic hemisphere of a 70-day Liolaemus embryo. (C) Coronal section of the right telencephalic hemisphere of a brain of a 19-week human fetus. For both (B) and (C), medial is toward the left. ADVR, anterior dorsal ventricular ridge; D, dorsal cortex; DM, dorsomedial cortex; ISO, isocortex; L, lateral cortex; LG, lateral ganglionic eminence; M, medial cortex; MG, medial ganglionic eminence; OLF, olfactory cortex; S, corpus striatum. The subventricular zone is the dark region surrounding the ventricular epithelium (indicated by asterisks). Arrowhead in (C) indicates the caudato-pallial junction. Bar is 0.5 mm (A,B), 2 mm (C).

 
Karten and co-workers (Karten, 1968Go, 1969Go; Nauta and Karten, 1970Go; Karten and Shimizu, 1989Go; Karten, 1991Go, 1997Go; Shimizu and Karten, 1991aGo, bGo) have argued that despite their architectural differences, the DVR of birds is comparable to the auditory and extrastriate visual isocortices of mammals by virtue of sharing the same type of sensory input. Furthermore, they proposed the equivalent cell hypothesis between birds and mammals, stating that the projections from the ectostriatum to the neostriatum (both components of the avian ADVR) and from there to the archistriatum (PDVR) were homologues of connections from layer IV to layers II–III and from there to layers V–VI of the mammalian extrastriate isocortex respectively. A similar scheme has been proposed by Veenman et al. (Veenman et al., 1995Go). If this homology is correct, the same connectivity should be found in the reptilian ADVR, although no such studies have been reported in this class. Furthermore, the precise homologues of the components of the avian ADVR (such as the hyperstriatum ventrale, neostriatum and ectostriatum) (Nieuwenhuys et al., 1998Go) have not been established in reptiles.

Homology between the ADVR and parts of the isocortex has also been proposed by Reiner (Reiner, 1993Go, 1996Go), for whom the lateral part of the dorsal pallium elaborated into the ADVR in reptiles and birds, while in mammals this region became part of the isocortex (mainly extrastriate isocortex), together with the more dorsal aspect of dorsal cortex (which would have become striate cortex). Butler (Butler, 1994Go) agrees with Reiner's suggestion and prescribes homology between the ADVR and part of the isocortex on the basis of the existence of a subventricular zone in both structures during development [see Aboitiz (Aboitiz, 1995Go) for comments on Reiner (Reiner, 1993Go) and Butler (Butler, 1994Go)]. On the other hand, a number of authors (Northcutt, 1981Go; Lohman and Smeets, 1991Go; Aboitiz, 1992Go, 1995Go; Northcutt and Kaas, 1995Go, 1996Go; Bruce and Neary, 1995Go; Andreu et al., 1996Go; Striedter, 1997Go) have questioned the homology between the ADVR and the isocortex. Most of these authors emphasize the embryological relation between the ADVR and the lateral (olfactory) cortex and propose that the origin of the isocortex is mainly a consequence of an expansion within the dorsal pallium. Furthermore, some authors argue for homology between the ADVR and other pallial components of mammals such as the ventral anterior and lateral amygdala (Bruce and Neary, 1995Go) or the endopiriform nucleus — ventral claustrum (Striedter, 1997Go).


    Criteria for homology
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 Abstract
 Introduction
 Theories of Homology between...
 Criteria for homology
 Developmental Problems Raised by...
 Development of the Mammalian...
 The Intermediate Territory of...
 Discussion
 References
 
The above controversies result in large part from the fact that at this point there is no consensus on the criteria that should be used to determine structural identity between two structures (Wagner, 1994Go). Karten and collaborators are relying on connectional evidence to validate their proposals; others argue that developmental evidence will determine whether the distinct cell groups are comparable or not. Before the discussion of the comparative data, I will now briefly describe the advantages and limitations of these criteria [for a full review, see Aboitiz (Aboitiz, 1995Go)].

Connectivity as a Criterion for Homology

Karten's approach emphasizes the phylogenetic conservation of processing circuits as a tool to determine phylogenetic relations between brain parts (Karten, 1969Go; Nauta and Karten, 1970Go). One problem with using connectional patterns to determine homology is that there is documented species variability in neural projections. For example, auditory projections to the forebrain, which were initially used by Karten (Karten, 1968Go, 1969Go) to propose homology between the ADVR and the auditory isocortex, terminate in the medial pallium but most importantly, in the corpus striatum of amphibians (Frost and Masterton, 1992Go; Butler, 1994Go). Likewise, the visual projections that relay in the optic tectum also project (via specific thalamic nuclei) mainly to the corpus striatum of frogs and salamanders (Butler, 1994Go; Nieuwenhuys et al., 1998Go). Will this force us to conclude that the avian ADVR and the extrastriate and auditory isocortices are homologues of the amphibian striatum? Furthermore, the capacity for plasticity of connections in the forebrain is surprising in the sense that sensory inputs can be rerouted into regions that normally receive input from a different sensory modality; yet the region receiving the new input appears to process it in a similar way as it would normally be processed (Sur et al., 1990Go). This supports the possibility that in phylogeny the targets of specific sensory inputs can be shifted from one brain region to another with relative facility.

Developmental Homology

The oldest criteria for establishing homology are similarity of adult topographic position and similar embryonic origin (Aboitiz, 1995Go). In the case of the telencephalon, adult position of the distinct components is sometimes greatly distorted by the various deformations that take place during the development of the hemispheres, which obscures the comparisons between brain parts in different vertebrate classes (Northcutt, 1981Go; Striedter, 1997Go, 1998Go). Embryological similarity remains an important criterion in most cases (Striedter, 1997Go, 1998Go), especially in those cases in which adult diversification takes place starting from a relatively conserved embryonic form, as occurs in telencephalic evolution. In the forebrain, this criterion is further supported by the fact that most neurons originate in the ventricular zone and then migrate radially to the surface, establishing a topographic map of the adult structures in the embryonic ventricular layer (Nieuwenhuys, 1974Go; Rakic, 1988Go). Furthermore, studies of the expression patterns of regulatory genes in early neural development have determined specific compartments along the different regions of the prosencephalon, from which particular brain components arise (Puelles and Rubenstein, 1993Go). One caveat for the use of embryological criteria is that homologous structures can in some instances arise from nonhomologous anlage (Striedter and Northcutt, 1991Go). However, this tends to occur in cases of adult conservatism with diversity of embryological processes (Aboitiz, 1995Go), and as mentioned, the case of the cerebral hemispheres is one of embryological conservatism and adult diversification.

Homology at Different Levels

Following Striedter and Northcutt's (Striedter and Northcutt, 1991Go) concept of homology at different levels of organization [see also Lauder (Lauder, 1994Go)], Reiner has distinguished between homology at the level of brain components and cellular homology (Reiner, 1996Go). For example, cells originating in homologous embryonic anlages in, say, birds and mammals may have migrated in distinct directions and have been incorporated into different structures in each case. These cells, although located in nonhomologous structures, would be homologues between birds and mammals. The possibility of diverse migratory pathways may distort the straightforward correspondence between the embryonic ventricular zone and adult structures that is implied by a strictly radial mode of cell migration (Nieuwenhuys, 1974Go; Rakic, 1988Go). Below I will discuss how this bears directly to the question of isocortical origins from a DVR-like structure.


    Developmental Problems Raised by the Equivalent Cell Hypothesis
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 Abstract
 Introduction
 Theories of Homology between...
 Criteria for homology
 Developmental Problems Raised by...
 Development of the Mammalian...
 The Intermediate Territory of...
 Discussion
 References
 
Embryologically, the reptilian ADVR has been reported to arise as a late proliferative event in the ventricular layer, in a similar topographical position to the lateral cortex, but after the cells destined for the cortical layers have been produced and have migrated (Källén, 1951Go; Yanes et al., 1987Go, 1989Go). More recently, using the highly sensitive probe biotinylated dextran in chick embryos, Striedter et al. were able to observe that cells destined to the neostriatum originate in a region that corresponds to the lateral pallium (Striedter et al., 1998Go). In other words, the ADVR develops in situ in the ventricular zone of the lateral hemisphere, deep to lateral cortex. A radial glia scaffolding has been described during development of the DVR in both reptiles (Kalman et al., 1997Go) and birds (Striedter and Beydler, 1997Go); this may act as a substrate for radial cell migration within this structure. In the adult bird brain, migrating neurons have been described as following pathways determined by radial glia (Álvarez-Buylla et al., 1988Go; Álvarez-Buylla and Kirn, 1997Go). However, in the developing avian brain there is also a substantial degree of tangential migration (i.e. across the direction imposed by the radial glia) (Szele and Cepko, 1998Go).

Implications for Homology with Isocortex

Given the position of the ADVR internal to the lateral cortex, for parts of the isocortex to originate from an ADVR-like structure, a massive cell migration would be predicted for cells from underneath the lateral or olfactory cortex towards more dorsal parts of the hemisphere, where the auditory and extrastriate isocortices are located (Butler, 1994Go; Reiner, 1993Go; Karten, 1997Go). The main mode of cell migration during mammalian isocortical development has been shown to be radial, as the radial glia provides a matrix for neuronal migration (Rakic, 1988Go, 1995aGo, bGo). Since the processes of the radial glia do not span the distance between the lateral hemisphere and the developing isocortex, migration from a DVR-like embryonic structure into isocortex would have to take place in a direction perpendicular or oblique to the orientation of the radial glia. Such tangential migration has been shown to occur to some extent within the developing isocortex of mammals and birds, but until recently there was no evidence of migration from lateral to dorsal pallial components to make up the extrastriate isocortex. To clarify this point, I will now review the evidence for radial and for tangential migration in isocortical development.


    Development of the Mammalian Isocortex
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 Abstract
 Introduction
 Theories of Homology between...
 Criteria for homology
 Developmental Problems Raised by...
 Development of the Mammalian...
 The Intermediate Territory of...
 Discussion
 References
 
An important feature of the mammalian isocortex is its columnar organization, which is evident in terms of the ontogenic arrangement of the migrating neurons that build up this structure (cells aggregate in columns as they end migration into the cortical plate), but also in terms of the organization of the extrinsic connections (thalamic axons tend to enter radially to the cortex (Rakic, 1988Go, 1995aGo, bGo). Rakic has proposed the radial unit hypothesis, asserting that the radial column makes up a developmental unit that consists of a polyclonal arrangement of cells that share the same migratory pathway (the same or neighboring radial glial cells) through the intermediate zone (IZ) that separates the ventricular zone (where cell proliferation occurs) from the marginal zone and cortical plate (Rakic, 1988Go, 1995aGo, bGo). The cellular composition of the radial unit seems to be relatively conserved across mammals, and in the course of evolution cortical expansion has occurred through an increase in the number of cortical columns rather than through the expansion or radial growth of each column (Rakic, 1988Go).

Evidence for Tangential Migration in Isocortical Development

Cells migrating in directions oblique or transverse to the radial glia scaffolding, following trajectories specified by tangentially oriented axons, have been reported extensively in the hindbrain (Rakic, 1985Go). Recent studies using retroviral markers indicated that there is a significant degree of tangential dispersion of clonally related cells in the developing isocortex (up to 40–50% of the clones were reported to disperse tangentially) (Walsh and Cepko, 1992Go, 1993Go). Interestingly, in early corticogenesis tangential dispersion was found to be limited but tended to increase in later periods (O'Rourke et al., 1995Go). Time-lapse video techniques (O'Rourke et al., 1992Go, 1995Go) confirmed the tangential migration of cells across radial glia, but the proportion of such cells was less than that obtained by Walsh and Cepko (between 20 and 30%). By inserting cells with a lacZ transgene on an X chromosome into the embryo, Tan and Breen were able to determine that the majority of migrating cells followed a radial pathway (Tan and Breen, 1993Go). If the majority of cells dispersed tangentially, cells positive and negative for lacZ would intermingle in the developing isocortex. However, a pattern of alternate positive and negative stripes was obtained, indicating that most clonally related cells follow a radial route similar to that of their siblings. Still, the observed stripes were not pure, and it was calculated that ~30% of the cells move tangentially. Finally, more recent studies of transgenic mice using ß-galactosidase as a marker have also revealed a predominantly radial arrangement of most clones (Soriano et al., 1995Go; Tan et al., 1995Go), with ~30% of the clones dispersing in a tangential direction. A point of interest is that tangential dispersion of clones does not necessarily imply migration across radial glia in the IZ. In mammals, much of the tangential dispersion of clones occurs by dispersion within the ventricular or the subventricular zones before the beginning of cell migration (Fishell et al., 1993Go; Reid et al., 1995Go); however, this does not seems to be the case in birds (Szele and Cepko, 1998Go).

One additional issue regarding clonal specification in corticogenesis is to what extent clonally related cells share the same phenotype (Luskin, 1994Go). Using retroviral lineage-tracing methods, Mione et al. observed that pyramidal cells tend to be arranged in discrete clusters, but nonpyramidal neurons were found to be much more dispersed, usually in pairs or as single cells (Mione et al., 1997Go). A more recent study using stem cell chimeras (Tan et al., 1998Go) identified clones of glutamatergic neurons that were predominatly radially dispersed, and clones of GABAergic neurons that tended to be tangentially scattered. This suggests that the pattern of migration depends both on the cell's lineage and on its future phenotype. However, other studies have revealed phenotypic heterogeneity of the distinct clones (Soriano et al., 1995Go; Lavdas et al., 1996Go), both in neurotransmitter contents and in morphological characteristics. Clonal heterogeneity tends to decrease as cortical development advances, i.e. late-generated clones tend to be phenotypically more homogeneous than early-generated ones (Lavdas et al., 1996Go).

Migration of cortical neurons along radial glia is supported by specific membrane proteins that act as adhesion molecules between the two cell types (Cameron and Rakic, 1994Go; Anton et al., 1996Go; Cameron et al., 1997Go) [see also Río et al. (Río et al., 1997Go)]. In addition, soluble proteins such as glial growth factor, which are expressed in migrating neurons, promote migration of the latter and elongation and maintenance of the radial glial cells (Anton et al., 1997Go). Furthermore, migration partly depends on genes of the Pax family (Caric et al., 1997Go). Recently, retroviral lineage-tracing methods have permitted the visualization of neighboring, clonally related cells that can be tangentially or radially arranged (Kornack and Rakic, 1995Go). These two patterns may respectively result from symmetric cell divisions (one progenitor cell gives rise to two migrating neurons that are born simultaneously and consequently end up at the same horizontal level in the cortical plate); or from asymmetric cell divisions (one progenitor cell gives rise to a migrating neuron and to a progenitor that keeps dividing in the ventricular zone; therefore the labelled neurons arise at different times and are consequently located in different horizontal layers but in the same radial column).

Using genetically tagged embryonic stem cells, Kuan et al. (Kuan et al., 1997Go) reported horizontally arranged clones in layers V and VI, which contrasts with the predominantly radial disposition of clones in granular and supragranular layers (Tan and Breen, 1993Go; Rakic, 1995bGo). This was interpreted by Kuan et al. as evidence supporting a dual origin of neocortex, in which tangentially oriented clones might derive from progenitor cells originating in the dorsal pallium, while the progenitor cells of radially oriented clones would originally derive from the lateral pallium, having migrated dorsomedially in the evolution of mammals. In my view, Kuan et al.'s findings are consistent with the interpretation that the granular and supragranular layers of isocortex represent an evolutionary innovation (Aboitiz, 1999Go), and perhaps derive from a different progenitor pool to the infragranular layers which resemble the reptilian cortex (Ebner, 1976Go; Reiner, 1993Go); however, these results do not point to any specific place of origin of the respective progenitor cells.

Notwithstanding all the evidence supporting the notion of tangential migration, it may be worth bearing in mind that during development the telencephalic hemisphere expands considerably in the tangential domain. Migrating a small distance (say 300 µm) before telencephalic growth may result in a net distance of 1 mm or more after the expansion. This over- estimation of the actual migrated distance might be called the ‘ballooning artifact’, and should be considered in future studies of cellular migration.

Tangential Migration Across Developmental Boundaries: The Caudato-pallial Junction in Mammals

Despite their degree of tangential dispersion, cells within the mammalian ventricular zone do not tend to cross developmental barriers like the pallial–subpallial border (also called the cortico-striatal border or caudato-pallial junction) (Fishell et al., 1993Go). However, migrating cells in the IZ have been observed that cross this compartment boundary (De Diego et al., 1994Go; De Carlos et al., 1996Go). In the postnatal mouse, the subventricular zone in this latter region is a source of migrating neurons to multiple structures in the central nervous system, including the olfactory bulb (Lois and Álvarez-Buylla, 1994Go; Lim et al., 1997Go). It is likely that once cells start migrating they are more free to cross developmental barriers, but perhaps part of the disagreements mentioned stem from the fact that the pallial–subpallial boundary is still an ill-defined border in mammals.

The lateral and medial ganglionic eminences (LGE, MGE) are embryonic structures positioned ventral to the corticostriatal sulcus (a ventricular sulcus located close to the pallial–subpallial border) in the mammalian hemisphere (Figs 2 and 3GoGo), which give rise to the corpus striatum. Nevertheless, some findings indicate that from the LGE curved radial glia develop that end in the lateral aspect of the hemisphere; neurons migrate along these glia towards the basolateral telencephalon, and form the primary olfactory cortex (De Carlos et al., 1996Go). Furthermore, some early cells migrate through this pathway up to the marginal zone and then move tangentially in a dorsomedial direction, presumably to become Cajal–Retzius cells in isocortical layer I (DeDiego et al., 1994Go; De Carlos et al., 1996Go).



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Figure 2.  The position of the lateral and medial ganglionic eminences (LG, MG) in the embryonic cerebral hemisphere of a mammal (mouse), compared with the reptilian (Gallotia galloti) ventricular zone b and the sulcus lateralis (SL), from where the anterior dorsal ventricular ridge (DVR) arises. Medial is to the left. Cx, cortex; S, striatum; SVZ, subventricular zone; VZ, ventricular zone. Mammalian hemisphere was drawn from Smart and Smart (Smart and Smart, 1977Go), and reptile hemisphere from Yanes et al. (Yanes et al., 1987Go).

 
An elegant series of recent experiments (Porteus et al., 1994Go; Anderson et al., 1997aGo,bGo) traced migrating cells from the sub-ventricular zone of the LGE and MGE, and determined that although most of these neurons migrate radially to form the corpus striatum, a fraction of these cells (especially from the LGE, which is adjacent to the cortico-striatal sulcus) migrate tangentially — across the radial glia — and become incorporated into the cerebral cortex as interneurons (mostly GABAergic). These cells keep expressing the Dlx-1 and Dlx-2 genes, which are markers for the ganglionic eminences. Furthermore, surgical detachment of the developing cortex from the LGE/MGE produces a decrease in cells positive for the Dlx genes in the cerebral cortex; and Dlx-1/2 mutant mice have a reduced number of GABAergic cortical cells (between 75 and 85% of the GABA-positive cells disappear). This suggests that the ganglionic eminences (especially LGE) can be important sources of some types of interneurons in the cerebral cortex, including lateral cortex, isocortex and hippocampus. This notion has been confirmed by findings indicating that the majority of tangentially migrating neurons in the isocortical IZ originate in the LGE (Tamamaki et al., 1997Go).

These experiments raise the possibility that some structures in the lateral pallium (where the DVR originates in reptiles) may also contribute cells to isocortex by using a similar migratory pathway, supporting the concept of a dual origin of the latter. This possibility relies on finding a structure in the developing mammalian hemisphere that can be compared to the embryonic DVR (or ADVR) of reptiles. However, the cells that incorporate into isocortex from the LGE are mainly GABAergic interneurons (Anderson et al., 1997aGo), which are not components of the equivalent circuits between mammals and reptiles (Karten and Shimizu, 1989Go). Furthermore, new evidence suggests that the ADVR of reptiles and the LGE of mammals originate from different neuroepithelial sectors (see below).


    The Intermediate Territory of the Cortico-striatal Border in Reptiles and Mammals
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 Abstract
 Introduction
 Theories of Homology between...
 Criteria for homology
 Developmental Problems Raised by...
 Development of the Mammalian...
 The Intermediate Territory of...
 Discussion
 References
 
The cortico-striatal border is marked by changes in the expression of specific regulatory genes. As mentioned, Dlx-type genes are expressed in what is considered the presumptive corpus striatum — the LGE and MGE — and genes such as Emx-1/2 and Otx-1/2 are expressed in the presumptive pallium (Simeone et al., 1992Go; Fishell et al., 1993Go; Puelles and Rubenstein, 1993Go). An outstanding paper (Smith Fernández et al., 1998Go) describes an intermediate territory (IT) between the pallium and the sub-pallium that is negative for Emx-1 and Dlx-1 genes and largely positive for the gene Pax-6. In mammals, parts of the paleocortex and the laterobasal amygdala (among other structures) originate from this region, while in reptiles most of the ADVR derives from this territory. Based on the expression patterns of Pax-6, these authors suggest homology between the reptilian ADVR, the avian neostriatum (an important part of the avian ADVR) and the laterobasal part of the amygdala of mammals. On the other hand, the PDVR of reptiles, the archistriatum of birds, and the corticomedial and central amygdala of mammals express Emx-1 and should be comparable. These results are consistent with a more recent report on patterns of gene expression in the developing telencephalon of birds and mammals that describes a ‘ventral pallial’ subdivision which may correspond to the IT (Puelles et al., 1999Go). This interpretation agrees with that of Bruce and Neary (Bruce and Neary, 1995Go), who propose homology between ADVR and the ventral and lateral amygdala. The latter components have been recently included in a subdivision of the amygdalar complex defined as the ‘frontotemporal’ system by virtue of its connections with the frontal, temporal and limbic cortices (Swanson and Petrovic, 1998). It should be noted that these same authors suggest that the term ‘amygdala’ refers to a connectionally and embryologically heterogeneous group of nuclei, each probably having different evolutionary origins. It must be mentioned that, on the basis of similarities in sensory connections, Lanuza et al. (Lanuza et al., 1998Go) recently proposed homology between the laterobasal amygdala and the PDVR, instead of the ADVR as proposed by Bruce and Neary (Bruce and Neary, 1995Go) and Smith-Fernández et al. (Smith-Fernández et al., 1998Go).

Karten's equivalent cell hypothesis may now imply that, in mammals, cells from the IT migrate tangentially into isocortex (Karten, 1991Go, 1997Go). Interestingly, Smith-Fernández et al. (Smith-Fernández et al., 1998Go) found that the mammalian IT is only a transient structure that in later developmental stages is compressed between the pallial and the subpallial neuroepithelia (see their Fig. 7). Thus, the IT generates neurons during early development only, giving rise to the mentioned structures (parts of paleocortex and laterobasal amygdala). In reptiles and birds on the other hand, this structure remains as a distinct component of the neuroepithelium until late developmental periods, producing neurons that will partly form the reptilian ADVR and the avian neostriatum. Consequently, the authors conclude that, although early generated populations of neurons of the IT can be considered homologous in different vertebrates, late-produced structures such as the ADVR and the neostriatum (especially the deeper parts) of birds and reptiles do not have a mammalian counterpart [‘We argue that the early generated populations of neurons can be considered as homologous in chick and mouse . . . and that on the contrary, later generated structures although produced by homologous developmental brain subdivisions, should not be considered properly as homologs' (Smith-Fernández et al., 1997), p. 2109]. Aboitiz originally proposed a similar hypothesis, in which the reptilian ADVR had no strict embryonic homologue in mammals (Aboitiz, 1992Go, 1995Go). However, there are alternative explanations such as the possibility that, since during development the IT bulges inwardly in birds, it remains as a distinct neuroepithelial element. In mammals, on the other hand, outward bulging of the neuroepithelium may distort the topographical relations in the developing hemisphere, producing the erroneous impression that the IT disappears. Thus, further studies are needed to confirm the disappearance of the IT during late telencephalic development in mammals. Additionally, although studies of patterns of gene expression are especially promising, some caveats are also indicated. For example, some cranial nerve nuclei have been described to shift their segmental position in phylogeny (Gilland and Baker, 1993Go), suggesting that genetically defined developmental compartments are not infallible as tools to determine phylogenetic homology.


    Discussion
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 Abstract
 Introduction
 Theories of Homology between...
 Criteria for homology
 Developmental Problems Raised by...
 Development of the Mammalian...
 The Intermediate Territory of...
 Discussion
 References
 
The present paper has summarized recent evidence on the comparative development of the telencephalon in the light of specific evolutionary theories about the origin of mammalian isocortex. Some new data are being helpful in discriminating between alternative hypotheses, but also raise new questions that will hopefully fuel the comparative analysis of brain development through the use of molecular labels.

Evolutionary Scenarios

I have reviewed evidence supporting the possibility that the ADVR originated from an in situ expansion of the lateral pallial wall during late telencephalic development (i.e. after cells destined for lateral cortex had migrated and formed this structure). On the other hand, the mammalian isocortex probably derives mostly from expansion of the dorsal pallium. At this point, perhaps the most parsimonious interpretation of amniote telencephalic evolution is that the ADVR of reptiles and birds, on one hand, and the mammalian isocortex, on the other, arose separately in different lineages, the former in the stem reptiles that gave rise to the taxon sauropsida (reptiles and birds), and the latter in the mammal-like reptiles that diverged quite early from their reptilian ancestors (Aboitiz, 1992Go, 1995Go). In other words, neither of these structures is likely to be ancestral to the other.

One possible solution to the apparent discrepancy between the connectional evidence (which indicates similarity in the processing circuits of DVR and of isocortex) and the developmental data (indicating that DVR arises in different embryonic compartments from isocortex), is to invoke Ebbesson's parcellation theory (Ebbesson, 1984Go). This prescribes that in phylogeny and in ontogeny, neural projections tend to progressively restrict their fields of termination into increasingly specific brain components, with the result that some regions will become deprived of such inputs. It is conceivable that, in a hypothetical ancestor of tetrapods, the visual and auditory projections originating in the mesencephalon, and reaching the telencephalon via specific thalamic nuclei, projected to a wide area of the lateral hemisphere including the lateral pallium, parts of the dorsal pallium and parts of the subpallium (corpus striatum). These projections became progressively restricted in all lineages (amphibians, birds/reptiles and mammals), but in each group a different place of termination was selected. However, there is no outgroup evidence of such widespread ancestral connections. Ascending projections to the telencephalon tend to be highly specific and to be restricted areas in all vertebrates studied (Nieuwenhuys et al., 1998Go). Alternatively, it is possible that instead of undergoing parcellation, the thalamic sensory inputs were rerouted to different telencephalic locations in each group of terrestrial vertebrates. This possibility is consistent with the evidence of plasticity in the developing forebrain and has not received the attention it deserves. This hypothesis would explain part of the connectional data without implying homology between the distinct components receiving the respective sensory terminations.

Conclusions and New Problems

Although the adult structures have diverged significantly in the different terrestrial vertebrates, there remains an important embryological similarity in the telencephali of the different groups (Aboitiz, 1995Go; Striedter, 1997Go, 1998Go). Furthermore, considering the divergent distortions that take place in reptilian and mammalian brain evolution, perhaps the ancestry of ADVR and that of isocortex might be better searched for in a generalized hemisphere such as the amphibian telencephalon — especially in its embryonic form (Bruce and Neary, 1995Go). The latter has been considered somewhat regressive in its organization, particularly regarding the limited extent of cell migration that occurs in such brains (Northcutt and Kaas, 1996Go). However, and because of its regressive nature, its topographical relations are similar to those found in the embryonic telencephali of birds, reptiles and mammals. Since cell bodies tend to concentrate in the periventricular region, usually there are no ‘deeper’ and ‘more superficial’ structures as they are found in more complex brains. Of particular interest in regard to the origin of the reptilian ADVR, research should focus on the development of the amphibian lateral pallium and the pallial and subpallial amygdalar subdivisions (Nieuwenhuys et al., 1998Go).

The evidence reviewed indicates that the majority of isocortical cells (including extrastriate isocortex) derive from the cortical ventricular zone and show a radial mode of cell migration. Even in the report by Anderson et al. (Anderson et al., 1997aGo) the overall cortical architecture is not significantly altered when the incorporation of cells from the ganglionic eminences is impeded. Thus, as originally proposed by Rakic, not denying the contribution of subpallial components, perhaps the major developmental event leading to the origin of isocortex has been the expansion of a proliferating zone in the dorsal aspect of the hemisphere and an increase in neuroblast proliferation in this region (Rakic, 1988Go). The regions adjacent to the caudato-pallial junction (more specifically the LGE) as well as other brain regions may have contributed to the evolutionary origin of isocortex. However, it is of interest to note that GABAergic cells do exist in the pallium of reptiles (Nieuwenhuys et al., 1998Go) and therefore the importation of such interneurons from subpallial sectors comparable to the LGE may also occur in this vertebrate class. The possibility raised by the work of Kuan et al., that the migration of neural progenitors (instead of postmitotic neurons) from the lateral pallium into the dorsal pallium gave rise to isocortex, should be considered further (Kuan et al., 1997Go). If correct, we would expect to find cells expressing lateral pallium markers (such as Pax-6) in the ventricular zone that gives rise to isocortex. However, this alternative would not be consistent with the finding that, in the ventricular zone, tangential cell migration is restricted across developmental compartments (Fishell et al., 1993Go).

The IT described by Smith-Fernández et al. raises many important questions (Smith-Fernández et al., 1998Go) [see also Puelles et al. (Puelles et al., 1999Go)]. This region gives rise to the ADVR in birds and reptiles and to the laterobasal amygdala in mammals. If Smith-Fernández et al. are correct, the IT disappears promptly in mammals. Therefore, if there is a contribution from this territory to isocortex, I predict that it will be small. Of special interest in this context is the region of the mammalian LGE that has been described as sending radial glia toward the olfactory cortex (De Carlos et al., 1996Go). This region may perhaps represent a remnant of the IT that is obliterated between the pallium and the developing corpus striatum. Additionally, one particularly intriguing point is that the IT gives rise to the amphibian lateral (olfactory) pallium, but its contribution to the olfactory cortex of reptiles, birds and mammals is less clear. This might call into question the homology between the amphibian lateral pallium and parts of the amniote olfactory cortex. Further studies are strongly needed to determine more details of the developmental fate of the IT in mammals, reptiles and amphibians.

Finally, there is some controversy regarding the possibility of homology between the mammalian laterobasal amygdala and the ADVR (Bruce and Neary, 1995Go; Smith-Fernández et al., 1998Go), or the PDVR (Lanuza et al., 1998Go) of reptiles. The latter interpretation might support other alternatives such as Striedter's, who considers that the ADVR is an homologue of the mammalian endopiriform nucleus (Striedter, 1997Go). The line of argumentation along this paper has been that, at least for the argument of homology between the ADVR and the isocortex, developmental evidence may be a better criterion than connectional evidence. Nevertheless, this controversy also points to what I consider can be an important bias among comparative neuroanatomists, which is the assumption that most brain components are directly comparable across different taxa. Perhaps in some cases attention should be drawn into the establishment of general homologies at the embryological level rather than a one-to-one correspondence between adult brain structures. If, in the different vertebrate classes, the distinct telencephalic components underwent separate and parallel expansion during evolution, it is certainly possible that subdivision of these components took place independently in each class, and consequently there may be no relation in the arrangement of such lesser compartments across the diverse vertebrate groups.


    Acknowledgments
 
I am especially grateful to my colleagues Miguel Concha, Albert M. Galaburda, Salvador Guirado and Georg Striedter for reading early drafts of this paper and contributing with criticism and ideas. Many students also participated with stimulating discussions on these issues, especially Olivia Casanueva, Juan Montiel and Daniver Morales. I am also grateful to the anonymous reviewers for their help in clarifying certain parts of the paper. The idea of the ‘ballooning artifact’ was given to me by one of these reviewers. Artwork in Figs 1 and 2GoGo was made by Samuel Valenzuela and Ángel Rodríguez. Figure 3Go was kindly provided by David Lemus and Susana Domínguez. Andrés Ide and Juan Montiel prepared the figures in their final form. I also want to thank Claudia Andrade for secretarial assistance. Supported by Fondecyt Grant 1970294 and by a gift from EMEC SA and ENAEX SA to F.A.


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 The Intermediate Territory of...
 Discussion
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