Hierarchical processing of sensory information across topographically organized thalamocortical-like circuits in the zebrafish brain

Thalamocortical projections contribute to the spatial organization and functional hierarchies of the mammalian cortex. Primary sensory cortices receive topographically segregated information from first-order thalamic nuclei, which process distinct sensory modalities. In contrast, higher-order cortical regions integrate information from multiple information channels. While such hierarchical processing and integration of information is the foundation for neural computations in the mammalian cortex, the fundamental principles of thalamocortical computations in non-mammalian vertebrates remains unexplored. The zebrafish pallium, located in the dorsal telencephalon, is regarded as the homolog of the mammalian cortex. However, it remains unclear how the zebrafish pallium receives and processes sensory information, and how the architecture and function of these processes compare to the thalamocortical circuits in other vertebrates. Using anatomical tracing, electrophysiological circuit mapping, and in vivo Ca2+ imaging, we revealed a thalamocortical-like pathway in the zebrafish brain. We found that the preglomerular nucleus (PG) is the primary source of visual and mechano-vibrational information to the zebrafish pallium. We demonstrated that PG neurons and their pallial projections exhibit sensory-specific and topographically organized responses. In contrast, the sensory responses of pallial neurons display multiple layers of topographically organized hierarchies, ranging from simple sensory-specific responses to multimodal and coincidence-detecting nonlinear responses. Notably, we observed a progressive increase in the complexity of sensory computations, which is organized topographically along the posterior-anterior axis of the zebrafish pallium. Collectively, our results suggest that hierarchical sensory processing across topographically organized pallial regions is a conserved functional feature of the vertebrate pallium.