A developmental approach to homology and brain evolution

Abstract

Although homology is central to evolutionary interpretations, establishing it has become a highly disputed issue in some instances. Here I argue for a developmental understanding of evolution, where modifications of the developmental programs are a key source of evolutionary novelty. Although this perspective is not new, in comparative neurobiology it has remained controversial. Specifically, the evolutionary origin of the mammalian neocortex has been a particularly debated point. I propose a perspective that could help reconcile a long standing controversy: either the mammalian neocortex corresponds as a whole to the dorsal hemisphere of reptiles and birds, or alternatively its lateral aspect corresponds to the lateral cerebral hemisphere and is partly homologous to the dorsal ventricular ridge (DVR), a brain mass that receives the bulk of sensory input in reptiles and birds. Genetic and embryonic evidence strongly favor a dorsal origin for the whole neocortex, while the DVR derives from the lateral hemisphere. Nevertheless, the phylogenetically new elements of both the neocortex and the avian DVR derive largely from intermediate progenitor cells located in the embryonic subventricular zone (SVZ), a zone of late proliferating activity located deep to the ventral, the lateral and the dorsal hemisphere. I suggest that, despite originating in different embryonic regions (lateral vs. dorsal hemisphere), the evolutionary new cellular elements in both the avian brain and in the mammalian neocortex derive from the activation of a similar genetic pathway, possibly activated by the gene Pax-6, that induces the late proliferation of embryonic neural progenitors. This pathway can be ancestral to amniotes, reflecting genetic homology. In mammals and birds independently, this precursor proliferative activity differentiated into an SVZ, recruiting neuronal precursors from different parts of the cerebral hemisphere in each group, to contribute to brain expansion.Key words: dorsal ventricular ridge, neocortex, pallium, subventricular zone, ventricular zone. RESUMENSi bien la homología es central en las interpretaciones evolutivas, en algunos casos su determinación ha sido causa de fuertes discusiones. Aquí propongo un enfoque evolutivo basado en la embriología, donde las modificaciones de los programas de desarrollo son una fuente crucial de novedad evolutiva. Si bien esta propuesta no es nueva, ha sido controversial en la neurobiología comparada. Específicamente, el origen de la neocorteza de los mamíferos es un tópico altamente debatido. Sugiero una perspectiva que podría ayudar a reconciliar dos antiguas posiciones en conflicto: la neocorteza deriva ya sea del hemisferio dorsal de los reptiles y aves, o alternativamente parte de ella deriva del hemisferio lateral y es homóloga a una estructura llamada cresta dorsoventricular (DVR) del cerebro de los reptiles y aves, que recibe la mayor parte de las proyecciones sensoriales. La evidencia embriológica y genética apoya fuertemente un origen dorsal de toda la neocorteza...

Evolution of the Hypothalamus and Inferior Lobe in Ray-Finned Fishes

“…Mammals have a cerebral cortex that increased tremendously in relative size during evolution [Molnár, 2011;Molnár et al, 2014;Montiel et al, 2016]. Whether the dorsal ventricular ridge of reptiles and birds is homologous with the cerebral cortex of mammals remains a matter of controversy [Northcutt and Kaas, 1995;Aboitiz, 1999Aboitiz, , 2010Dugas-Ford and Ragsdale, 2015].…”