THALAMOCORTICAL-LIKE CIRCUITS HIERARCHICALLY PROCESS SENSORY INFORMATION IN TOPOGRAPHICALLY ORGANIZED REGIONS IN THE ZEBRAFISH FOREBRAIN

In the mammalian cortex, distinct first-order thalamic nuclei contribute to the regionalization of the cortex by transmitting topographically selective sensory information to specific cortical regions. In the cortex, this sensory information is further hierarchically processed along the caudal-rostral axis of the brain. Yet, it is still unknown whether similar thalamocortical and hierarchical computations are conserved in more distant vertebrate species. In zebrafish, the dorsal telencephalon (or pallium) is considered homologous to the mammalian cortex, but it is still unclear as to how sensory information is transmitted to the zebrafish pallium and whether it is architecturally similar to other vertebrates. Using a combination of anatomical tracing, electrophysiological circuit mapping, and in vivo Ca2+ imaging, we revealed a thalamocortical-like pathway in the zebrafish brain. Our results show that the preglomerular nucleus (PG) is the primary diencephalic input to the zebrafish pallium. Furthermore, we found that distinct PG neurons encode different sensory modalities (light vs mechanical vibrations) and they distribute this information to topographically distinct zones in the zebrafish pallium. In contrast, pallial neurons exhibited sensory responses that were organized in multiple layers of topographically organized hierarchies, ranging from sensory-specific responses to mixed-selective and coincidence-detecting nonlinear responses. Interestingly, we found that this increase in sensory computation complexity was spatially organized along the posterior-anterior axis of the pallium mirroring its mammalian counterpart. Thus, our results suggest that hierarchical sensory processing across topographically organized pallial regions is a highly important functional feature that evolved millions of years ago and can be generalized across all vertebrates.