Social modulation of associative fear learning by pheromone communication

Abstract

Mice communicate through visual, vocal, and olfactory cues that influence innate, nonassociative behavior. We here report that exposure to a recently fear-conditioned familiar mouse impairs acquisition of conditioned fear and facilitates fear extinction, effects mimicked by both an olfactory chemosignal emitted by a recently fear-conditioned familiar mouse and by the putative stress-related anxiogenic pheromone beta-phenylethylamine (beta-PEA). Together, these findings suggest social modulation of higher-order cognitive processing through pheromone communication and support the concurrent excitor hypothesis of extinction learning.

Figure 1.

Social modulation of associative fear during (A) acquisition of conditioned fear, (B) retention of fear memory, (C) fear extinction learning (* P < 0.05 relative to social extinction; P < 0.001; # P < 0.05, ## P < 0.01 relative to Social Negative), and (D) retention of extinction memory. Observer mice exposed to recently fear-conditioned mice or an olfactory chemosignal from recently fear-conditioned mice show impaired fear learning. Observer mice exposed to recently extinction-trained mice show impaired extinction learning. Error bars ± SEM; (*) P < 0.05; (**) P < 0.01; (***) P < 0.001; n = 8–12/group.

Figure 2.

Olfactory Negative chemosignal modulation of associative fear during (A) fear extinction learning and (B) retention of extinction memory. Observer mice exposed to an olfactory chemosignal from either recently fear-conditioned mice or extinction-trained mice show enhanced extinction learning. Error bars ± SEM; (*) P < 0.05; (**) P < 0.01; (***) P < 0.001 relative to Olfactory Negative; n = 8/group.

Figure 3.

β-Phenylethylamine modulation of associative fear during (A) acquisition of conditioned fear, (B) retention of fear memory, (C) fear extinction learning, and (D) retention of extinction memory. Observer mice exposed to β-PEA show impaired fear conditioning, but enhanced extinction learning. Error bars ± SEM; (*) P < 0.05; (**) P < 0.01; (***) P < 0.001; n = 8/group.

Figure 4.

Social Negative, Olfactory Negative, and β-phenylethylamine modulation of (A) nociception and (B) locomotor activity. Contrary to our expectation, observer mice exposed to β-PEA show increased pain sensitivity. Error bars ± SEM; (*) P < 0.05; n = 6/group. There is no effect on locomotor activity.