A High-Dimensional Quantification of Mouse Defensive Behaviors Reveals Enhanced Diversity and Stimulus Specificity

Instinctive defensive behaviors, consisting of stereotyped sequences of movements and postures, are an essential component of the mouse behavioral repertoire. Since defensive behaviors can be reliably triggered by threatening sensory stimuli, the selection of the most appropriate action depends on the stimulus property. However, since the mouse has a wide repertoire of motor actions, it is not clear which set of movements and postures represent the relevant action. So far, this has been empirically identified as a change in locomotion state. However, the extent to which locomotion alone captures the diversity of defensive behaviors and their sensory specificity is unknown. To tackle this problem, we developed a method to obtain a faithful 3D reconstruction of the mouse body that enabled to quantify a wide variety of motor actions. This higher dimensional description revealed that defensive behaviors are more stimulus specific than indicated by locomotion data. Thus, responses to distinct stimuli that were equivalent in terms of locomotion (e.g., freezing induced by looming and sound) could be discriminated along other dimensions. The enhanced stimulus specificity was explained by a surprising diversity. A clustering analysis revealed that distinct combinations of movements and postures, giving rise to at least 7 different behaviors, were required to account for stimulus specificity. Moreover, each stimulus evoked more than one behavior, revealing a robust one-to-many mapping between sensations and behaviors that was not apparent from locomotion data. Our results indicate that diversity and sensory specificity of mouse defensive behaviors unfold in a higher dimensional space, spanning multiple motor actions.