Atlas of adult Danionella fish telencephalon reveals retention of larval characters

Abstract

The adult size of the vertebrate telencephalon typically impedes our interpreting its functions within the context of brain-wide circuit dynamics. Danionella, a genus of miniature and transparent teleost fishes closely related to zebrafish (Danio rerio), holds promise for whole-brain imaging and connectomics in an adult vertebrate. These advantages result from progenesis, a form of heterochrony characterized by early developmental onset of sexual maturation and cessation of growth leading to the retention of larval or juvenile characters in adults. Using molecular markers, tract tracing, and quantitative comparisons of cellular distribution patterns, we report a detailed neuroanatomical atlas of the adult Danionella dracula (Dracula fish) telencephalon. The results demonstrate that adults of Dracula fish and other Danionella species show extreme reduction in cellular migration from periventricular zones and topographic reorganization of major pallial divisions, including a compartment-like caudal pallium reminiscent of insect glomeruli (a dense neuropil surrounded by a thin layer of somata). We further document these characters in larval zebrafish, providing essential evidence corroborating a larval-like telencephalon in Danionella adults. Despite this phenotype, most canonical regions of the adult teleost telencephalon are identified. We also generate a transgenic GCaMP Dracula fish line, an annotated 3-dimensional atlas, and align functional imaging data to demonstrate the usefulness of this atlas as a resource for deciphering how the novel progenetic cytoarchitecture of the adult Danionella telencephalon can support its rich behavioral repertoire.