Mouse alarm pheromone shares structural similarity with predator scents

Abstract

Sensing the chemical warnings present in the environment is essential for species survival. In mammals, this form of danger communication occurs via the release of natural predator scents that can involuntarily warn the prey or by the production of alarm pheromones by the stressed prey alerting its conspecifics. Although we previously identified the olfactory Grueneberg ganglion as the sensory organ through which mammalian alarm pheromones signal a threatening situation, the chemical nature of these cues remains elusive. We here identify, through chemical analysis in combination with a series of physiological and behavioral tests, the chemical structure of a mouse alarm pheromone. To successfully recognize the volatile cues that signal danger, we based our selection on their activation of the mouse olfactory Grueneberg ganglion and the concomitant display of innate fear reactions. Interestingly, we found that the chemical structure of the identified mouse alarm pheromone has similar features as the sulfur-containing volatiles that are released by predating carnivores. Our findings thus not only reveal a chemical Leitmotiv that underlies signaling of fear, but also point to a double role for the olfactory Grueneberg ganglion in intraspecies as well as interspecies communication of danger.olfaction | animal communication | behavior | calcium imaging

Intergenerational transmission of emotional trauma through amygdala-dependent mother-to-infant transfer of specific fear

“…3D), which has been shown to contain the largest NG (23). The robust activity in the c-MOB-iGl suggests that this area is involved in the transfer of fear, possibly through the Grueneberg ganglion (GG)-NG olfactory subsystem, which was recently shown to be involved in alarm odor processing (21) and which was further explored below. Within the vomeronasal organ (VNO)-AOB subsystem (20), significant differences were found for the AOB [F(2, 14) = 6.090; P < 0.02]; post hoc tests showed increased AOB activity in both groups with mothers expressing fear ( Table 1 and Table S1) compared with the no MFC-CS group (P < 0.05; Fig.…”

“…However, at birth, pups have a welldeveloped olfactory system, which supports olfactory learning and infant-mother communication (12)(13)(14)(15). Olfaction remains important throughout life in rodents, including communicating fear using an alarm odor to support social transmission of fear (20)(21)(22). Thus, we explored whether the frightened mother's odor and its ability to increase pups' CORT was important for pups' learning of socially transmitted fear.…”

“…To examine the role of the GG-NG pathway in the social transmission of fear, PND 2-3 pups underwent either GG axotomy or sham surgery (SI Materials and Methods). Previous work shows that disruption of GG axonal tracts abolishes fear responses to the alarm odor in adults (21). Twelve days following the GG axotomy/sham procedure, pups were exposed to the odor of the frightened mother paired with a neutral lemon odor CS.…”

“…Because the stress hormone CORT is increased by the alarm odor (21) and is critical for pups' fear learning (12)(13)(14), we next explored the possibility that the alarm odor induced an increase in pups' CORT and was critical for pups socially transmitted FC. It should be noted, however, that maternal presence typically socially buffers pups to suppress the US-induced CORT increase and blocks FC until PND 16, although these mothers did not express fear (15).…”

“…pups may acquire an aversion to the CS through association with the odor of the frightened mother and the potential release of a maternal alarm odor (20)(21)(22).…”