How ‘Basal' Are the Basal Ganglia?

Abstract

years ago [Erwin et al., 2011], did not merely have a substantial rostral brain, but specifically a telencephalon, an elaborate set of forebrain structures hitherto recognized only in vertebrates. The set of structures that Strausfeld and Hirth [2013a] identify as the arthropod homolog of the basal ganglia is the central complex, a group of median neuropils located in the posterior part of the protocerebrum, the rostral-most major division of the arthropod brain. Their hypothesis is based on similarities in function, topological position, anatomical organization, neurotransmitter content and developmental genetics. Strong similarities in all these categories would indeed make a good case for homology between the central complex and basal ganglia, although the absence of these structures in the great majority of Bilaterian taxa would still pose serious problems. To usefully compare such manifestly (if perhaps superficially) different brains, one must not let differences in detail obscure deep parallels nor focus exclusively on similarities, i.e. one must chart a course between nit-picking and cherry-picking. This task is complicated by the fact that most of what we know about the ‘vertebrate’ basal ganglia is derived from the study of a handful of mammalian species. For example, what seems to be a ‘cardinal feature of the striatum’, the Of the roughly 35 metazoan phyla alive today, only 4 possess nervous tissue that is concentrated and elaborate enough to be called a ‘brain’, suggesting that brains evolved independently in these lineages [Holland, 2003; Northcutt, 2012]. However, growing knowledge of developmental genetics, particularly in vertebrates and insects, has revealed remarkable conservation in the genetic regulatory networks that pattern the developing embryo, including the developing nervous system [Carroll, 1995; Hirth and Reichert, 1999]. This has led to the hypothesis that chordates and arthropods inherited a tripartite rostral brain from their last common ancestor, which would make possession of such a brain the ancestral condition for the entire superclade of bilaterally symmetric animals (Bilateria); the many bilaterian phyla that lack such a brain would have lost it secondarily [Hirth et al., 2003]. A recent review by Strausfeld and Hirth [2013a] takes this a step further by arguing that arthropods have a homolog of the vertebrate basal ganglia, one of the major subdivisions of the telencephalon. Together with claims of a pallium homolog in annelids [Tomer et al., 2010] and suggestions of homology between the vertebrate olfactory bulb and the arthropod antennal lobe [Strausfeld, 2012], this implies that the common ancestor of all Bilateria, living more than 600 million Published online: November 26, 2013