Rapid Spatial Learning Controls Instinctive Defensive Behavior in Mice

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.

Environmental Enrichment Rescues Visually-Mediated Behavior in Ten-m3 Knockout Mice During an Early Critical Period

“…The response to the looming stimulus is considered innate (Yilmaz and Meister, 2013), and was chosen here to minimize any potential effects of altered learning in Ten-m3 KOs. Nevertheless, the flight response can be affected by changes in spatial acquisition (Vale et al, 2017). The hippocampus is well-known for its important roles in spatial learning and navigation (reviewed in Moser et al, 2017;Rolls, 2018).…”

Ultrastructural and optogenetic dissection of V1 corticotectal terminal synaptic properties

“…Looming visual stimuli have been shown to preferentially activate the human SC and pulvinar (Billington, Wilkie, Field, & Wann, 2011) or homologous structures across species (Liu, Niu, & Wang, 2008;Sun & Frost, 1998;Wu et al, 2005;Zhao et al, 2014). When mice are presented with overhead visual stimuli, they respond with escape or freezing behavior, dependent on the stimulus, the presence of a shelter during testing, as well as previous colony housing conditions (De Franceschi, Vivattanasarn, Saleem, & Solomon, 2016;Vale, Evans, & Branco, 2017;Yilmaz & Meister, 2013). Our results suggest that V1 corticotectal projections may enhance these behavioral responses via a combination of a relatively weak influence on GABAergic interneurons, and sustained excitation of WFV cells.…”

Mice use robust and common strategies to discriminate natural scenes

“…We analyzed the residuals of the fits by computing the root mean squared error (RMSE) between a predictor and the actual data. The RMSE for the simple case where the correct rate for each mouse 8 was predicted by the mean correct rate of the other mice (mean ± S.E.M. : 0.047 ± 0.0046) were significantly smaller than the RMSE values for the SSIM-based psychometric curve fits (mean ± S.E.M.…”

“…Mammalian visual systems including primates and rodents evolved to efficiently process natural stimuli [1][2][3][4][5] . Mice use vision to hunt prey 6 , avoid danger [7][8][9] , and navigate 10,11 .…”