Innate heuristics and fast learning support escape route selection in mice

Abstract

When faced with imminent danger, animals must rapidly take defensive actions to reach safety. Mice can react to threatening stimuli in ∼250 milliseconds1Evans D.A. Stempel A.V. Vale R. Ruehle S. Lefler Y. Branco T. A synaptic threshold mechanism for computing escape decisions.Nature. 2018; 558: 590-594https://doi.org/10.1038/s41586-018-0244-6Crossref PubMed Scopus (214) Google Scholar and, in simple environments, use spatial memory to quickly escape to shelter.2Vale R. Evans D.A. Branco T. Rapid Spatial Learning Controls Instinctive Defensive Behavior in Mice.Curr. Biol. 2017; 27: 1342-1349https://doi.org/10.1016/j.cub.2017.03.031Abstract Full Text Full Text PDF PubMed Scopus (53) Google Scholar,3Shamash P. Olesen S.F. Iordanidou P. Campagner D. Banerjee N. Branco T. Mice learn multi-step routes by memorizing subgoal locations.Nat. Neurosci. 2021; 24: 1270-1279https://doi.org/10.1038/s41593-021-00884-8Crossref PubMed Scopus (12) Google Scholar Natural habitats, however, often offer multiple routes to safety that animals must identify and choose from.4Cooper Jr., W. Cooper Jr., W.E. Blumstein D.T. Escaping From Predators: An Integrative View of Escape Decisions. Cambridge University Press, 2015Crossref Scopus (197) Google Scholar This is challenging because although rodents can learn to navigate complex mazes,5De Camp J.E. Relative distance as a factor in the white rat’s selection of a path.Psychobiology. 1920; 2: 245-253https://doi.org/10.1037/h0075411Crossref Scopus (10) Google Scholar,6Snygg D. Mazes in Which Rats Take the Longer Path to Food.J. Psychol. 1935; 1: 153-166https://doi.org/10.1080/00223980.1935.9917250Crossref Google Scholar learning the value of different routes through trial and error during escape could be deadly. Here, we investigated how mice learn to choose between different escape routes. Using environments with paths to shelter of varying length and geometry, we find that mice prefer options that minimize path distance and angle relative to the shelter. This strategy is already present during the first threat encounter and after only ∼10 minutes of exploration in a novel environment, indicating that route selection does not require experience of escaping. Instead, an innate heuristic assigns survival value to each path after rapidly learning the spatial environment. This route selection process is flexible and allows quick adaptation to arenas with dynamic geometries. Computational modeling shows that model-based reinforcement learning agents replicate the observed behavior in environments where the shelter location is rewarding during exploration. These results show that mice combine fast spatial learning with innate heuristics to choose escape routes with the highest survival value. The results further suggest that integrating prior knowledge acquired through evolution with knowledge learned from experience supports adaptation to changing environments and minimizes the need for trial and error when the errors are costly.

Topics & Concepts