Evolution of pallial high-order sensory processing circuits

Résumé

Understanding the appearance of the neocortex in evolution requires the study of its stereotyped sensory processing circuits andtheir formation during embryonic development. These circuits appear in sensory structures of the telencephalon of different amniotespecies, which suggests their homology. However, their evolutionary history is still a matter of debate. If they were homologous,they would have evolved from a common ancestral circuit that was already present over 320 mya and inherit its developmentalpattern. Accordingly, only circuits generated in an equivalent fashion can be considered homologous. In this thesis, we have aimedto compare the development of high-order sensory processing circuits in different pallial regions of selected amniote species inorder to study their evolution. For that, we have used traditional birthdating in vivo methods at different neurogenic timepoints,focusing on the main sensory processing circuits: cortical in mammals and DVR and hyperpallium in birds. For their neuronalpopulations we have defined 1) the neurogenic period when these are generated and 2) their final brain position. An additionalsource of evidence on the developmental trajectories has derived from an exhaustive analysis of neuronal transcriptomes by scRNASeq,after the isolation of birthdated neurons with BirthSeq, a novel method we have developed to isolate viable cells according totheir birthdate. We have identified different developmental instructions for the constructions of these circuits. Crucial differencesare that 1) most hyperpallial neurons are preferentially born at mid-neurogenic stages, versus the wide temporal spread of thecortical neuronal birthdate; and 2) while the latest born neurons of the pallium do not participate in the DVR circuit, theirmammalian homologues actively contribute as cortical integrators. Additionally, we have described the existence of a highdivergence of the pallial glutamatergic neurons that comprise sensory circuits. Taken together, all our results suggest that high-ordersensory circuits evolved separately in vertebrates but in parallel, and reached equivalent functional features by evolutionary convergence.