Transcriptomic neuron types vary topographically in function and morphology

Inbal Shainer, Johannes M. Kappel, Eva Laurell, Joseph C. Donovan, Martin W. Schneider, Enrico Kuehn, Irene Arnold-Ammer, Manuel Stemmer, Johannes Larsch and Herwig Baier (herwig.baier@bi.mpg.de)
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Inbal Shainer: Max Planck Institute for Biological Intelligence
Johannes M. Kappel: Max Planck Institute for Biological Intelligence
Eva Laurell: Max Planck Institute for Biological Intelligence
Joseph C. Donovan: Max Planck Institute for Biological Intelligence
Martin W. Schneider: Max Planck Institute for Biological Intelligence
Enrico Kuehn: Max Planck Institute for Biological Intelligence
Irene Arnold-Ammer: Max Planck Institute for Biological Intelligence
Manuel Stemmer: Max Planck Institute for Biological Intelligence
Johannes Larsch: Max Planck Institute for Biological Intelligence
Herwig Baier: Max Planck Institute for Biological Intelligence

Nature, 2025, vol. 638, issue 8052, 1023-1033

Abstract: Abstract Neuronal phenotypic traits such as morphology, connectivity and function are dictated, to a large extent, by a specific combination of differentially expressed genes. Clusters of neurons in transcriptomic space correspond to distinct cell types and in some cases—for example, Caenorhabditis elegans neurons1 and retinal ganglion cells2–4—have been shown to share morphology and function. The zebrafish optic tectum is composed of a spatial array of neurons that transforms visual inputs into motor outputs. Although the visuotopic map is continuous, subregions of the tectum are functionally specialized5,6. Here, to uncover the cell-type architecture of the tectum, we transcriptionally profiled its neurons, revealing more than 60 cell types that are organized in distinct anatomical layers. We measured the visual responses of thousands of tectal neurons by two-photon calcium imaging and matched them with their transcriptional profiles. Furthermore, we characterized the morphologies of transcriptionally identified neurons using specific transgenic lines. Notably, we found that neurons that are transcriptionally similar can diverge in shape, connectivity and visual responses. Incorporating the spatial coordinates of neurons within the tectal volume revealed functionally and morphologically defined anatomical subclusters within individual transcriptomic clusters. Our findings demonstrate that extrinsic, position-dependent factors expand the phenotypic repertoire of genetically similar neurons.

Date: 2025
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DOI: 10.1038/s41586-024-08518-2

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