Visual recognition of social signals by a tectothalamic neural circuit

Johannes M. Kappel, Dominique Förster, Katja Slangewal, Inbal Shainer, Fabian Svara, Joseph C. Donovan, Shachar Sherman, Michał Januszewski, Herwig Baier () and Johannes Larsch ()
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Johannes M. Kappel: Max Planck Institute for Biological Intelligence (formerly Max Planck Institute of Neurobiology)
Dominique Förster: Max Planck Institute for Biological Intelligence (formerly Max Planck Institute of Neurobiology)
Katja Slangewal: Max Planck Institute for Biological Intelligence (formerly Max Planck Institute of Neurobiology)
Inbal Shainer: Max Planck Institute for Biological Intelligence (formerly Max Planck Institute of Neurobiology)
Fabian Svara: Max Planck Institute for Biological Intelligence (formerly Max Planck Institute of Neurobiology)
Joseph C. Donovan: Max Planck Institute for Biological Intelligence (formerly Max Planck Institute of Neurobiology)
Shachar Sherman: Max Planck Institute for Biological Intelligence (formerly Max Planck Institute of Neurobiology)
Michał Januszewski: Google Research
Herwig Baier: Max Planck Institute for Biological Intelligence (formerly Max Planck Institute of Neurobiology)
Johannes Larsch: Max Planck Institute for Biological Intelligence (formerly Max Planck Institute of Neurobiology)

Nature, 2022, vol. 608, issue 7921, 146-152

Abstract: Abstract Social affiliation emerges from individual-level behavioural rules that are driven by conspecific signals1–5. Long-distance attraction and short-distance repulsion, for example, are rules that jointly set a preferred interanimal distance in swarms6–8. However, little is known about their perceptual mechanisms and executive neural circuits3. Here we trace the neuronal response to self-like biological motion9,10, a visual trigger for affiliation in developing zebrafish2,11. Unbiased activity mapping and targeted volumetric two-photon calcium imaging revealed 21 activity hotspots distributed throughout the brain as well as clustered biological-motion-tuned neurons in a multimodal, socially activated nucleus of the dorsal thalamus. Individual dorsal thalamus neurons encode local acceleration of visual stimuli mimicking typical fish kinetics but are insensitive to global or continuous motion. Electron microscopic reconstruction of dorsal thalamus neurons revealed synaptic input from the optic tectum and projections into hypothalamic areas with conserved social function12–14. Ablation of the optic tectum or dorsal thalamus selectively disrupted social attraction without affecting short-distance repulsion. This tectothalamic pathway thus serves visual recognition of conspecifics, and dissociates neuronal control of attraction from repulsion during social affiliation, revealing a circuit underpinning collective behaviour.

Date: 2022
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DOI: 10.1038/s41586-022-04925-5

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