Contributions of associative and non-associative learning to the dynamics of defensive ethograms

Abstract

AbstractDefensive behavior changes based on threat intensity, proximity, and context of exposure, and learning about danger-predicting stimuli is critical for survival. However, the contributions of associative and non-associative mechanisms to dynamic defensive responses are currently unclear given the reductionist behavior elicited by most Pavlovian fear conditioning paradigms. To investigate defensive ethograms more thoroughly, we subjected male and female adult C57BL/6J mice to a Pavlovian threat conditioning paradigm that pairs footshock with a serial compound stimulus (SCS) consisting of distinct tone and white noise (WN) stimulus periods. To investigate how associative and non-associative mechanisms affect defensive responses, we compared the paired SCS-footshock group with control groups that either received randomly presented SCS and footshock presentations (unpaired) or received only footshocks during conditioning (shock-only). After conditioning, only the paired group exhibited robust freezing during the tone period with switching to explosive flight responses comprised of jumping and darting behavior during the WN period. The unpaired group expressed no cue-induced freezing and significantly less freezing overall. Furthermore, the unpaired group reduced freezing but rarely showed jumping or darting during WN. Following conditioning, we observed how defensive behavior changed over two extinction sessions. During extinction, only the paired group decreased tone-induced freezing. During WN, the paired group rapidly transitioned from escape jumping to freezing and darting. Comparatively, the unpaired and shock-only groups displayed stress-induced tail rattling to SCS, eschewing freezing and jumping. These findings demonstrate that while non-associative factors promote some defensive responsiveness, associative pairings are required for robust cue-induced freezing and flight expression.