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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. 1A-C 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.

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Figure 1. Schematic representation of a parasagittal section through the brains of birds (A, B), a teleost fish (C), and a rodent (D), showing the relative location of the lateral ventricle (blue) in relation to neural populations homologous to the mammalian cortex (green) and subpallial domains (magenta). In mammals (D), the cortex (pallium) lies entirely above the ventricle, which led early anatomists to consider the entire region below the ventricle in birds to be subpallial (A). More recent studies culminating in the current set of papers now show that cortical-equivalent cell groups lie both above and below the lateral ventricle (B) and its extension (blue dotted line) suggesting that the lateral ventricle is not a useful demarcation between pallial (cortex) and subpallial (striatopallidal) fields. The situation in teleosts (C) is even more extreme where the telencephalic ventricle is covered by the membranous tela choroidea and lies entirely dorsal of the telencephalic neuronal populations. The detailed organization and homologies of pallial cell groups in teleosts remains to be elucidated. More extensive arrays of gene expression data and details of connectivity are necessary in order to discern the full organization of the forebrain in ray-finned fishes. Panels A and B are adapted from Jarvis et al. (this issue); Panel C is adapted from Ganz et al., 2012; Panel D is based on the Allen Brain Atlas (http://mouse.brain-map.org).

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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 non-mammalian taxa, no neocortex exists as an obvious 6-layered structure, and the neural tissue lying above the ventricle is either non-laminated, or sparsely laminated. Hence, early comparative neuroanatomists (see, for example, Ariëns 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 large-scale 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 was entirely subpallial. But as was the case for birds, studies on molecular and hodological features of the forebrain in these fishes have led to the realization that pallial-equivalent cell groups are present despite the location of these groups below the ventricle (Wullimann and Mueller, 2004; Yamamoto et al., 2007; Northcutt, 2006; Nieuwenhuys, 2009; Mueller et al., 2011 Harvey-Girard et al., 2012; Ganz et al., 2012). Recent hodological, neurochemical, and molecular studies suggest that lampreys also possess pallial and subpallial homologues (Murakami et al., 2001; Stephenson-Jones et al., 2012; Sugahara et al., 2013). Although several hypotheses have been proposed on the homology of lamprey pallial zones (Pombal et al., 2011), an unequivocal conclusion has yet to be reached.

Homology of different pallial territories of ray-finned fishes with corresponding structures in amniotes remains disputed. As is the case for birds, teleosts have two major pallial regions, lateral and medial, that receive sensory inputs from the diencephalon (Yamamoto and Ito, 2005, 2008; Northcutt, 2006). One hypothesis considers the lateral part to be homologous to the hippocampus while the medial part would represent the claustroamygdaloid complex (Northcutt, 2006). A contravening hypothesis considers both the lateral and medial sensory recipient zones to be homologous to components of the neocortex, and perhaps only to its layer IV (Yamamoto et al., 2007; Ito and Yamamoto, 2009). These two sensory recipient zones in teleosts might arise from a common embryonic progenitor pool, as proposed by Jarvis et al. for separated pallial fields in birds. Clearly, understanding of the organization and evolution of the vertebrate forebrain will require molecular expression studies in other taxa such as teleosts and cyclostomes, equivalent to those reported in this issue by Jarvis and coworkers. Clarification of these seemingly arcane issues is likely to have a profound impact on our understanding of the molecular origins and patterns of cellular embryogenesis and migration in mammalian cortex. The most exciting aspect of the several recent studies on the comparative biology of the telencephalon is that comparative neurobiologists may be on the verge of providing a unifying formulation of the organization of the forebrain of all vertebrates.

Detailed histological data from the featured articles by Jarvis et al. and Chen et al. are available as virtual slides or whole-slide images using Biolucida Cloud image streaming technology from MBF Bioscience. This collection can be accessed at http://Wiley.Biolucida.net/JCN521-16Jarvis_Chen.

  • Thomas E. Finger

  • Naoyuki Yamamoto

  • Harvey J. Karten

  • Patrick R. Hof

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