From Sauropsids to Mammals and Back : New Approaches to Comparative Cortical Development

Evolution of the mammalian neocortex (isocortex) has been a persisting problem in neurobiology. While recent studies have attempted to understand the evolutionary expansion of the human neocortex from rodents, similar approaches have been used to study the changes between reptiles, birds, and mammals. We review here findings from the past decades on the development, organization, and gene expression patterns in various extant species. This review aims to compare cortical cell numbers and neuronal cell types to the elaboration of progenitor populations and their proliferation in these species. Several progenitors, such as the ventricular radial glia, the subventricular intermediate progenitors, and the subventricular (outer) radial glia, have been identified but the contribution of each to cortical layers and cell types through specific lineages, their possible roles in determining brain size or cortical folding, are not yet understood. Across species, larger, more diverse progenitors relate to cortical size and cell diversity. The challenge is to relate the radial and tangential expansion of the neocortex to the changes in the proliferative compartments during mammalian evolution and with the changes in gene expression and lineages evident in various sectors of the developing brain. We also review the use of recent lineage tracing and transcriptomic approaches to revisit theories and to provide novel understanding of molecular processes involved in specification of cortical regions. J. Comp. Neurol. 524:630–645, 2016. VC 2015 The Authors. The Journal of Comparative Neurology Published by Wiley Periodicals, Inc. INDEXING TERMS: intermediate progenitors; progenitors; ventricular radial glia; subventricular zone; subventricular (outer) radial glia; transcriptomics; cerebral cortex; Wulst; dorsal ventricular ridge Understanding how the mammalian neocortex (isocortex) evolved to its present complex state is a fascinating topic for neuroscience, genetics, bioinformatics, and comparative biology. Mammals have a six-layered neocortex, a trait that differentiates this clade from any other classes (Krubitzer and Kaas, 2005; Fig. 1). The impact of that characteristic on the emergence of associative cognitive repertoires is believed to be a key to the success of mammals. Our brains allow us to anticipate the future, create music, poetry, and to enjoy intellectual challenges that provide few practical rewards or material gains. These abilities have evolved recently (Moln ar and Pollen, 2014). Studies of the changes that occurred previously as the sauropsids and mammals started to diverge may well shed light on the nature of changes responsible for these abilities. Our review examines the earliest stages of cortical development (in mammals and sauropsids) and analyzes the developmental mechanisms that evolved to produce the mammalian cerebral cortex. We review some of the most pertinent differences in brain organization and investigate the possible developmental origins of these differences to define the causes of the separate phylogenetic developments. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. The first two authors contributed equally to this work. Grant sponsor: MRC, BBSRC, the Wellcome Trust. *CORRESPONDENCE TO: Department of Physiology, Anatomy and Genetics, Le Gros Clark Building, University of Oxford, South Parks Road, Oxford, OX1 3QX, UK. E-mail: zoltan.molnar@dpag.ox. ac.uk Received April 3, 2015; Revised July 21, 2015; Accepted July 21, 2015. DOI 10.1002/cne.23871 Published online August 20, 2015 in Wiley Online Library (wileyonlinelibrary.com) VC 2015 The Authors. The Journal of Comparative Neurology Published by Wiley Periodicals, Inc. 630 The Journal of Comparative Neurology |Research in Systems Neuroscience 524:630–645 (2016) REVIEW