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.
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Abstract |
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Introduction |
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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. 1), a prominent telencephalic structure present in birds and reptiles (Karten, 1968
, 1969
; Nauta and Karten, 1970
). 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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Theories of Homology between the Dorsal Ventricular Ridge and the Isocortex |
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Homology between the ADVR and parts of the isocortex has also been proposed by Reiner (Reiner, 1993, 1996
), 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, 1994
) 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, 1995
) for comments on Reiner (Reiner, 1993
) and Butler (Butler, 1994
)]. On the other hand, a number of authors (Northcutt, 1981
; Lohman and Smeets, 1991
; Aboitiz, 1992
, 1995
; Northcutt and Kaas, 1995
, 1996
; Bruce and Neary, 1995
; Andreu et al., 1996
; Striedter, 1997
) 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, 1995
) or the endopiriform nucleus ventral claustrum (Striedter, 1997
).
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Criteria for homology |
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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, 1969; Nauta and Karten, 1970
). 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, 1968
, 1969
) 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, 1992
; Butler, 1994
). 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, 1994
; Nieuwenhuys et al., 1998
). 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., 1990
). 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, 1995). 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, 1981
; Striedter, 1997
, 1998
). Embryological similarity remains an important criterion in most cases (Striedter, 1997
, 1998
), 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, 1974
; Rakic, 1988
). 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, 1993
). One caveat for the use of embryological criteria is that homologous structures can in some instances arise from nonhomologous anlage (Striedter and Northcutt, 1991
). However, this tends to occur in cases of adult conservatism with diversity of embryological processes (Aboitiz, 1995
), 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, 1991) concept of homology at different levels of organization [see also Lauder (Lauder, 1994
)], Reiner has distinguished between homology at the level of brain components and cellular homology (Reiner, 1996
). 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, 1974
; Rakic, 1988
). Below I will discuss how this bears directly to the question of isocortical origins from a DVR-like structure.
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Developmental Problems Raised by the Equivalent Cell Hypothesis |
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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, 1994; Reiner, 1993
; Karten, 1997
). 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, 1988
, 1995a
, b
). 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.
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Development of the Mammalian Isocortex |
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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, 1985). 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 4050% of the clones were reported to disperse tangentially) (Walsh and Cepko, 1992
, 1993
). Interestingly, in early corticogenesis tangential dispersion was found to be limited but tended to increase in later periods (O'Rourke et al., 1995
). Time-lapse video techniques (O'Rourke et al., 1992
, 1995
) 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, 1993
). 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., 1995
; Tan et al., 1995
), 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., 1993
; Reid et al., 1995
); however, this does not seems to be the case in birds (Szele and Cepko, 1998
).
One additional issue regarding clonal specification in corticogenesis is to what extent clonally related cells share the same phenotype (Luskin, 1994). 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., 1997
). A more recent study using stem cell chimeras (Tan et al., 1998
) 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., 1995
; Lavdas et al., 1996
), 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., 1996
).
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, 1994; Anton et al., 1996
; Cameron et al., 1997
) [see also Río et al. (Río et al., 1997
)]. 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., 1997
). Furthermore, migration partly depends on genes of the Pax family (Caric et al., 1997
). Recently, retroviral lineage-tracing methods have permitted the visualization of neighboring, clonally related cells that can be tangentially or radially arranged (Kornack and Rakic, 1995
). 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., 1997) 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, 1993
; Rakic, 1995b
). 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, 1999
), and perhaps derive from a different progenitor pool to the infragranular layers which resemble the reptilian cortex (Ebner, 1976
; Reiner, 1993
); 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 pallialsubpallial border (also called the cortico-striatal border or caudato-pallial junction) (Fishell et al., 1993). However, migrating cells in the IZ have been observed that cross this compartment boundary (De Diego et al., 1994
; De Carlos et al., 1996
). 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, 1994
; Lim et al., 1997
). 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 pallialsubpallial 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 pallialsubpallial border) in the mammalian hemisphere (Figs 2 and 3), 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., 1996
). Furthermore, some early cells migrate through this pathway up to the marginal zone and then move tangentially in a dorsomedial direction, presumably to become CajalRetzius cells in isocortical layer I (DeDiego et al., 1994
; De Carlos et al., 1996
).
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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., 1997a), which are not components of the equivalent circuits between mammals and reptiles (Karten and Shimizu, 1989
). Furthermore, new evidence suggests that the ADVR of reptiles and the LGE of mammals originate from different neuroepithelial sectors (see below).
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The Intermediate Territory of the Cortico-striatal Border in Reptiles and Mammals |
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Karten's equivalent cell hypothesis may now imply that, in mammals, cells from the IT migrate tangentially into isocortex (Karten, 1991, 1997
). Interestingly, Smith-Fernández et al. (Smith-Fernández et al., 1998
) 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, 1992
, 1995
). 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, 1993
), suggesting that genetically defined developmental compartments are not infallible as tools to determine phylogenetic homology.
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Discussion |
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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, 1992, 1995
). 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, 1984). 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., 1998
). 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, 1995; Striedter, 1997
, 1998
). 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, 1995
). 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, 1996
). 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., 1998
).
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., 1997a) 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, 1988
). 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., 1998
) 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., 1997
). 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., 1993
).
The IT described by Smith-Fernández et al. raises many important questions (Smith-Fernández et al., 1998) [see also Puelles et al. (Puelles et al., 1999
)]. 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., 1996
). 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, 1995; Smith-Fernández et al., 1998
), or the PDVR (Lanuza et al., 1998
) 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, 1997
). 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.
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Acknowledgments |
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