Neuronal detection of social actions directs collective escape behavior

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Abstract

Animals in groups obtain information from their social partners to engage in collective behavior 1–4 . Social information transmission has been observed amongst individuals in fish schools 5–8 , bird flocks 9,10 , and human groups 11,12 , but the neural mechanisms for detecting socially transmitted information are poorly understood 4,13–15 . By studying the schooling glassfish Danionella cerebrum 16–18 , here we demonstrate that escape from danger is enhanced by visual perception of other escaping fish. We found that neural populations in the midbrain optic tectum 19–21 and dorsal thalamus 22,23 are activated by the rapid escape of social partners. These neurons are also driven by the sudden disappearance of virtual social partners, yet unaffected by disappearing stimuli without social relevance. Virtual fish schools that escape or disappear were sufficient to cause observers to escape, even in the absence of direct threats. These results demonstrate that rapid “social-off” detection in visual circuits enables the detection of socially transmitted threat information, which may be a particularly effective strategy for animals capable of rapid movement but limited visual range 17,24 . These results show how neural computations in individuals enables rapid information sharing in animal collectives 4,15 .
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Abstract Animals in groups obtain information from their social partners to engage in collective behavior1–4. Social information transmission has been observed amongst individuals in fish schools5–8, bird flocks9,10, and human groups11,12, but the neural mechanisms for detecting socially transmitted information are poorly understood4,13–15. By studying the schooling glassfish Danionella cerebrum16–18, here we demonstrate that escape from danger is enhanced by visual perception of other escaping fish. We found that neural populations in the midbrain optic tectum19–21 and dorsal thalamus22,23 are activated by the rapid escape of social partners. These neurons are also driven by the sudden disappearance of virtual social partners, yet unaffected by disappearing stimuli without social relevance. Virtual fish schools that escape or disappear were sufficient to cause observers to escape, even in the absence of direct threats. These results demonstrate that rapid “social-off” detection in visual circuits enables the detection of socially transmitted threat information, which may be a particularly effective strategy for animals capable of rapid movement but limited visual range17,24. These results show how neural computations in individuals enables rapid information sharing in animal collectives4,15. Competing Interest Statement The authors have declared no competing interest. Footnotes Revision has corrections to Figs. 3A,E, 5J

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License: CC-BY-NC-ND-4.0