Abstract
SummaryInstinctive defensive behaviors are essential for animal survival. Across the animal kingdom, there are sensory stimuli that innately represent threat and trigger stereotyped behaviors such as escape or freezing [1, 2, 3, 4]. While innate behaviors are considered to be hard-wired stimulus-responses [5], they act within dynamic environments, and factors such as the properties of the threat [6, 7, 8, 9] and its perceived intensity [1, 10, 11], access to food sources [12, 13, 14], and expectations from past experience [15, 16] have been shown to influence defensive behaviors, suggesting that their expression can be modulated. However, despite recent work [2, 4, 17, 18, 19, 20, 21], little is known about how flexible mouse innate defensive behaviors are and how quickly they can be modified by experience. To address this, we have investigated the dependence of escape behavior on learned knowledge about the spatial environment and how the behavior is updated when the environment changes acutely. Using behavioral assays with innately threatening visual and auditory stimuli, we show that the primary goal of escape in mice is to reach a previously memorized shelter location. Memory of the escape target can be formed in a single shelter visit lasting less than 20 s, and changes in the spatial environment lead to a rapid update of the defensive action, including changing the defensive strategy from escape to freezing. Our results show that although there are innate links between specific sensory features and defensive behavior, instinctive defensive actions are surprisingly flexible and can be rapidly updated by experience to adapt to changing spatial environments.
Highlights
To further test this hypothesis, we reasoned that presentation of the threat while the animal is in the shelter should not cause escape behavior. Auditory stimuli delivered both in the Barnes maze and in a modified version with a surface shelter did not cause escape behavior, despite the sound pressure level inside the shelter being within 2dB of the arena outside, indicating that the perception of safety can veto escape from innately aversive threats. These results show that instinctive escape behavior in the mouse is not a simple stimulus reaction, but a generic action in response to threat with the goal of reaching a safe area, the location of which is computed before the onset of the escape
Mice stayed in the vicinity of the pre-rotation location for 4.6 ± 0.2 s, which is 2.5 times longer than the time mice spent in the wrong location during missed flights in control conditions (Figure 2E; p < 0.001, t test for time in the wrong location between control and post-rotation), further indicating goal directedness toward this location. These data suggest that landmarks proximal to the shelter are not required for the computation of shelter location, and this is further supported by threat presentation in complete darkness, which evokes perfectly accurate escape responses (Figures S2A and S2B; Movie S2)
We found that animals escaped to the new shelter location in less than two trials, with four out of nine mice escaping to the new location on the first trial
Summary
These results show that instinctive escape behavior in the mouse is not a simple stimulus reaction, but a generic action in response to threat with the goal of reaching a safe area, the location of which is computed before the onset of the escape.
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