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E Volutionary Divergence of the Reptilian and the Mammalian Brains Brain Research Reviews 39 (2002) 141–153 www.elsevier.com/locate/brainresrev Review E volutionary divergence of the reptilian and the mammalian brains: considerations on connectivity and development Francisco Aboitiza,* , Juan Montiel a , Daniver Morales b , Miguel Concha a,c aPrograma de Morfologıa´´, Instituto de Ciencias Biomedicas, Facultad de Medicina, Universidad de Chile, Santiago, Chile bDevelopmental Neurobiology Laboratory, The Rockefeller University, New York, NY, USA cDepartment of Anatomy and Developmental Biology, University College, London, UK Accepted 27 June 2002 Abstract The isocortex is a distinctive feature of the mammalian brain, with no clear counterpart in other amniotes. There have been long controversies regarding possible homologues of this structure in reptiles and birds. The brains of the latter are characterized by the presence of a structure termed dorsal ventricular ridge (DVR), which receives ascending auditory and visual projections, and has been postulated to be homologous to parts of the mammalian isocortex (i.e., the auditory and the extrastriate visual cortices). Dissenting views, now supported by molecular evidence, claim that the DVR originates from a region termed ventral pallium, while the isocortex may arise mostly from the dorsal pallium (in mammals, the ventral pallium relates to the claustroamygdaloid complex). Although it is possible that in mammals the embryonic ventral pallium contributes cells to the developing isocortex, there is no evidence yet supporting this alternative. The possibility is raised that the expansion of the cerebral cortex in the origin of mammals was product of a generalized dorsalizing influence in pallial development, at the expense of growth in ventral pallial regions. Importantly, the evidence suggests that organization of sensory projections is significantly different between mammals and sauropsids. In reptiles and birds, some sensory pathways project to the ventral pallium and others project to the dorsal pallium, while in mammals sensory projections end mainly in the dorsal pallium. We suggest a scenario for the origin of the mammalian isocortex which relies on the development of associative circuits between the olfactory, the dorsal and the hippocampal cortices in the earliest mammals. 2002 Elsevier Science B.V. All rights reserved. Theme: Other systems of the CNS Topic: Comparative neuroanatomy Keywords: Amygdala; Dorsal cortex; Dorsal ventricular ridge; Homology; Isocortex; Pallium; Regulatory genes; Ventral pallium Contents 1 . Introduction. the problem of isocortical origins .......................................................................................................................................... 142 2 . The pallium of amniotes........................................................................................................................................................................... 143 3 . Connectional and neurochemical comparisons: the recapitulation hypothesis................................................................................................ 143 4 . Conflicting connectional evidence: the outgroup hypothesis........................................................................................................................ 145 5 . Developmental criteria ............................................................................................................................................................................. 145 5 .1. Other components of the DVR ......................................................................................................................................................... 147 5 .2. Dorsoventral gradients and their relation to the IT/VP ....................................................................................................................... 147 6 . Different patterns of brain organization in reptiles and mammals ................................................................................................................ 148 7 . A scenario for isocortical origins: olfaction, the hippocampus and the thalamofugal visual system................................................................. 149 7 .1. Fossil brains ................................................................................................................................................................................... 149 *Corresponding author. Depto. de Psiquiatria, Facultad de Medicina, Pontificia Universidad Catolica de Chile, Marcoleta No. 387, 28 Piso, P.O. Box 114-D, Santiago 1, Chile. Fax: 156-2-665-1951. E-mail address: [email protected] (F. Aboitiz). 0165-0173/02/$ – see front matter 2002 Elsevier Science B.V. All rights reserved. PII: S0165-0173(02)00180-7 142 F. Aboitiz et al. / Brain Research Reviews 39 (2002) 141–153 8 . Final comment ........................................................................................................................................................................................ 150 Acknowledgements ...................................................................................................................................................................................... 151 References................................................................................................................................................................................................... 151 1 . Introduction. the problem of isocortical origins assumption that there are comparable components (homo- logues) in the different taxa, despite their superficial The mammalian isocortex (or neocortex) is a character dissimilarities. In order to understand the origin of the unique to the brain of mammals in several respects. First, it mammalian isocortex, it is fundamental to determine has undergone an enormous expansion, especially in the which ancestral structure(s) gave rise to it. Although tangential domain [70]. Second, it has a six-layered obviously the ancestor is unavailable to study, there are architecture which differs from the three-layered array of sister taxa (reptiles and birds) whose brains can be simpler telencephalic laminar structures such as the hip- compared with those of mammals in order to infer the pocampal formation, the olfactory cortex and the reptilian characteristics of the common ancestor. Commonly used cortices [3,92]. On the other hand, the telencephalon of criteria for determining neural homology are connectivity reptiles has a small, thin cortex and a prominent periven- [42,43,56], neurochemistry [74,75], topographical location tricular structure named dorsal ventricular ridge (DVR), [1,2,34] and embryonic origins [4,40,66,67,87,90]. Un- which receives many thalamic sensory projections (Fig. 1). fortunately, when dealing with the homologues of the There have been important disagreements as to which isocortex, these different methodologies have led to di- components of the non-mammalian telencephalon can be verging interpretations. compared to the isocortex of mammals. This problem is In this paper we will address the issue of a possible complicated by the intricate topography of the hemispheres correspondence between the reptilian dorsal cortex and the in some vertebrate classes, and by the absence of a unified mammalian isocortex, and will review recent molecular criterion to establish neural homology. Homology is a evidence supporting this interpretation. Then, the general central problem to comparative anatomy, since the organization of the mammalian and reptilian brains will be evolutionary considerations regarding the origin and di- discussed in light of these new findings, and we will versification of any structure are usually based on the propose a scenario for the origin of the mammalian brain. Fig. 1. Coronal section of the cerebral hemispheres of a reptile and a mammal, indicating in gray the different components of the pallium. The subpallium is shown in white. ADVR, anterior dorsal ventricular ridge; AM, amygdala (only part of which is pallial); CL, claustrum; DCx, dorsal cortex; DMCx, dorsomedial cortex; HIP, hippocampus; ICx, isocortex; LCx, lateral cortex; MCx, medial cortex; OCx, olfactory cortex; PT, pallial thickening (present only in turtles); STR, striatum. Medial is to the left. F. Aboitiz et al. / Brain Research Reviews 39 (2002) 141–153 143 Our main argument along this paper is that the evidence on the isocortex has a dual origin, part of it deriving from the regulatory gene expression provides a notable example of reptilian dorsal cortex, and the other part deriving from the how molecular developmental biology may help to clarify DVR (especially the ADVR). An alternative hypothesis important issues in the evolution of the nervous system. suggests that the isocortex derives mostly from the re- ptilian dorsal pallium, and has been called the outgroup hypothesis [1,2,4,61,68,90]. Below, we will summarize 2 . The pallium of amniotes some of the evidence favouring each of the two possi- bilities. The reptilian pallium has a three-layered cortex, consist- ing of a medial and a dorsomedial component (both comparable to the mammalian hippocampal formation), a dorsal cortex and a lateral or olfactory cortex [98] (Fig. 1). 3 . Connectional and neurochemical comparisons: the In birds, there is a medial hippocampus and a lateral recapitulation hypothesis olfactory cortex. The avian dorsal cortex is a relatively complex, multilaminated structure called the Wulst. The Before comparing the sensory
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