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Dryad

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

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Sep 19, 2023 version files 96.71 MB
Sep 26, 2023 version files 96.71 MB

Abstract

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.