Increased neuron density in the midbrain of foveate birds results from profound change in tissue morphogenesis

Abstract

ABSTRACTThe increase of brain neuron number in relation with brain size is currently considered to be the major evolutionary path to high cognitive power in amniotes. However, how changes in neuron density did contribute to the evolution of the information-processing capacity of the brain remains unanswered. High neuron densities are seen as the main reason why the fovea located at the optical center of the retina is responsible for sharp vision in birds and primates. The emergence of foveal vision is considered as a breakthrough innovation in visual system evolution. We found that neuron densities in the largest visual center of the midbrain – i.e., the optic tectum – are two to four times higher in modern birds with one or two foveae compared to birds deprived of this specialty. Interspecies comparisons enabled us to identify elements of a hitherto unknown developmental process set up by foveate birds for increasing neuron density in the upper layers of their optic tectum. The late progenitor cells that generate these neurons proliferate in a ventricular zone that can expand only radially. In this particular context, the number of cells in ontogenetic columns increases, thereby setting the conditions for higher cell densities in the upper layers once neurons did migrate.Graphical AbstractHighlightsThe presence of a fovea is associated with increased neuron density in the optic tectumFovea number and deepness influence neuron density in the optic tectumIncreased neuron density in the upper layers of the optic tectum requires major developmental changesPostponed cell migration, prolonged cell proliferation, hindered tissue growth are necessary settings for achieving high neuron density