Context Shapes Fear: Habituation of Innate Defensive Behaviours Depends on Environmental Context

Abstract

The capacity of animals to rapidly and appropriately respond to potential threats is critical for survival. In many species, this involves innate defensive behaviours, such as escape or freezing. But not all threats are dangerous. Habituation - a form of non-associative learning - allows animals to filter out irrelevant stimuli and thereby avoid unnecessary energy expenditure. While it is well known that context can influence behavioural responses to associative learning, whether non-associative forms of learning, such as habituation, are also context-dependent is unclear. Here, we address this issue in mice by examining the role of environmental context on habituation of defensive behaviours to threatening visual stimuli. We first developed a protocol leading to rapid (within minutes) and stable (at least one week) habituation of freezing responses to slowly sweeping visual stimuli, resembling an aerial predator moving across the sky. Using this protocol, we tested the impact of environmental context on habituation of freezing responses, finding that changing the environmental context led to a significant and reversible reduction in habituation. In summary, we find that environmental context plays a critical role in determining the impact of habituation on visually evoked innate defensive behaviours. These findings reveal a previously unrecognised flexibility in defensive responses to visual threats, extending the influence of environmental context to non-associative learning. HighlightsO_LIMice freeze in response to sweeping visual stimuli, resembling an aerial predator. C_LIO_LIHabituation to sweeping visual stimuli could be induced rapidly and remained stable over time. C_LIO_LIHabituation to sweeping visual stimuli depended on environmental context. C_LIO_LIContext-specific habituation was reversible. C_LI