Evolution of the forebrain — revisiting the pallium

In 1973, Theodosius Dobzhansky wrote a short essay whose title "Nothing in biology makes sense except in the light of evolution" became a highly popular catch phrase for evolutionary biologists. Whereas Dobzhansky was criticizing at the time anti-evolutionary creationism, his words reflect, in the context of neuroscience, that since the earliest microscopic studies on the structure of the brains of vertebrates, neuroanatomists have noted many striking similarities in organization across species. The brainstems of all vertebrates clearly follow a common plan of development and organization with increasing divergence in the structure of the diencephalon and telencephalon. In mammals, the telencephalon is dominated by the neocortex, which lies entirely above the lateral ventricle and envelops the deeper telencephalic structures of the basal ganglia including striatum (caudate nucleus and putamen) and pallidum (globus pallidus) (compare Fig. 1AC and 1D). Because the cortex enshrouds the lateral ventricle, cerebral cortex was also called the pallium (cloak or mantle) by early anatomists (e.g., Smith, 1919). Similarly, structures of the telencephalon below the lateral ventricle were considered subpallial. The reliance on the lateral ventricle as an important boundary separating pallial and subpallial structures has, however, caused confusion when attempting to extend this distinction to non-mammalian vertebrates. In nonmammalian taxa, no neocortex exists as an obvious 6layered structure, and the neural tissue lying above the ventricle is either non-laminated, or sparsely laminated. Hence, early comparative neuroanatomists (see, for example, Ari€ens Kappers et al., 1967) considered this supraventricular part of the forebrain to be pallial, and the remainder, below the ventricle, to be subpallial (Fig. 1A). Based purely on these topological considerations, the subpallial components were equated with mammalian basal ganglia and were named, accordingly, neostriatum. With the advent of histochemical techniques and the ability to trace connectivity reliably over long distances in the 1960s (Karten, 1969; Nauta and Karten, 1969; Karten, 1991, 1997; Wang et al., 2010; Butler et al., 2011; Karten, 2013), it became evident that the classic formulation of organization of non-mammalian brains was incorrect. Many structures lying below the lateral ventricle had anatomical, biochemical, and functional properties more characteristic of neocortex than of basal ganglia. The realization that subventricular cell groups could be equivalent to cortical populations led to a revolution in thinking about the organization of the avian forebrain, culminating in 2004 with a renaming of the structures in the telencephalon of birds (Reiner et al., 2004; Jarvis et al., 2005), to represent better contemporary views of telencephalic organization. For example, the neostriatum — a structure below the lateral ventricle now recognized to participate in cortex-like functions — was renamed nidopallium, reflecting its probable homology to part of the mammalian pallium. The pair of papers by Jarvis and coworkers in this issue of the Journal of Comparative Neurolology, involves a largescale survey of gene expression patterns across key regions of the telencephalon of birds. (For supplementary histological materials, see http://Wiley.Biolucida.net/ JCN521-16Jarvis_Chen). The patterns of expression largely confirm (see also Dugas-Ford et al., 2012) the pallial nature of many of the structures situated ventral to the lateral ventricle, which classical neuroanatomists had considered to be subpallial. More importantly, the current studies demonstrate that several subventricular populations are topologically continuous with, and share molecular expression properties with, populations situated above the lateral ventricle suggesting an origin from a common embryonic cytological field. Thus, a single population of cells, all equivalent to a set of neocortical neurons, may lie both above and below the lateral ventricle when viewed in transverse sections (Fig. 1B). In mammals (Fig. 1D), the neocortex does not arise by simple radial migration from a proliferative ependymal layer, but also entails long-distance radial and tangential migrations from basal forebrain areas (Anderson et al., 1997). In fishes too, large-scale migrations of neuronal populations from their site of origin may account for the final appearance of the adult telencephalon (Yamamoto et al., 2007). The realization that a cell group’s location in adults with respect to the lateral ventricle may not be related to its function or embryonic site of origin is of fundamental importance when trying to define homologies for parts of non-mammalian and mammalian brains. The topography of neuronal populations with respect to the lateral ventricle is especially confounding when considering the forebrains of ray-finned fishes. In this group, no neuronal populations lie above the ventricle (Fig. 1C); the ventricle is covered only by a thin membrane, the tela choroidea, produced by fusion of pia and ventricular ependyma, without obvious intercalated neurons. This organization led early comparative anatomists to the view that the telencephalon in teleosts