Visual recognition of social signals by a tectothalamic neural circuit

Social affiliation emerges from individual-level behavioural rules that are driven by conspecific signals. Long-distance attraction and short-distance repulsion, for example, are rules that jointly set a preferred interanimal distance in swarms. However, little is known about their perceptual mechanisms and executive neural circuits. Here we trace the neuronal response to self-like biological motion, a visual trigger for affiliation in developing zebrafish. 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 function. 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.

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