A telencephalon cell type atlas for goldfish reveals diversity in the evolution of spatial structure and cell types

Teleost fish form the largest group of vertebrates, making them critically
important for the study on the mechanisms of brain evolution. In fact,
teleosts show a tremendous variety of adaptive behaviors similar to birds
and mammals, however, the neural basis mediating these behaviors remains
elusive. We performed a systematic comparative survey of the goldfish
telencephalon: the seat of plastic behavior, learning, and memory in
vertebrates. We delineated and mapped goldfish telencephalon cell types
using single-cell RNA-seq and spatial transcriptomics, resulting in de
novo molecular neuroanatomy parcellation. Glial cells were highly
conserved across 450 million years of evolution separating mouse and
goldfish, while neurons showed diversity and modularity in gene
expression. Specifically, somatostatin (SST) interneurons, famously
interspersed in the mammalian isocortex for local inhibitory input, were
curiously aggregated in a single goldfish telencephalon nucleus, but
molecularly conserved. Cerebral nuclei including the striatum, a hub for
motivated behavior in amniotes, had molecularly conserved goldfish
homologs. We further suggest different elements of a hippocampal formation
across the goldfish pallium. Finally, aiding study of the teleostan
everted telencephalon, we describe substantial molecular similarities
between the goldfish and zebrafish neuronal taxonomies. Together, our
atlas provides new insights into organization and evolution of vertebrate
forebrains and may serve as a resource for the functional study underlying
cognition in teleost fish.