Fear conditioning by-proxy: social transmission of fear during memory retrieval

Abstract

After fear conditioning (e.g., by pairing a tone to a shock), memory retrieval typically leads to fear expression (e.g., freezing to the tone). Here, we examined the effect of a conditioned rat's fear memory retrieval on a naïve cage-mate's behavior to the conditioned stimulus. We show that rats exposed to a novel tone in the presence of a cage-mate previously conditioned to that same tone selectively showed increased freezing to the stimulus the next day (fear conditioning by-proxy). In addition, fear conditioning by-proxy experienced prior to pairing the tone to a mild shock increased freezing during presentation of that tone the next day. Our results suggest that, during memory retrieval, fear of a stimulus can be socially transmitted to a cage-mate. These findings may have implications for models of phobias.

Figure 1

(A) Experimental design diagram illustrating the fear conditioning by-proxy paradigm. One rat from the triad was conditioned to 3 tone-shock pairings (0.7 mA footshock) (Blue). The next day, the conditioned rat and one of his cage-mates (FCbP rat, red) were placed in the conditioning chamber and 3 tones were played. No shock US was delivered at this time. Twenty-four hours later, all rats were tested for their freezing response to the CS (FCbP rat is shown here). (B) Effect of fear conditioning by proxy (FCbP) on freezing to a tone. FCbP rats showed significantly (p<0.05) more freezing to the tone than their naïve control cagemates when tested in the context in which they observed conditioned fear responses 24 h earlier.

Figure 2

FCbP median split shows that only half of FCbP rats displayed freezing behavior when tested 24 h after the FCbP training session. The upper half of the FCbP rats (FCbP+) froze more than the lower half (FCbP-) of the FCbP and the naïve control rats (p<.05). Fear-conditioned rats froze significantly (p < 0.05) more than either FCbP or naïve rats.

Figure 3

Social interaction duration and type between the FC and FCbP rats before and during CS exposure. (3A) Relationship between social interaction duration with an FC cagemate during CS, and FCbP freezing the next day. A multiple regression analysis revealed that the duration of social interactions between the FC and FCbP rats significantly accounted for the variance accounted for in FCbP freezing the next day, R(12)=.533, p<.05. (3B) Qualitative depiction of social interaction types between the FC and FCbP rats during each CS, and for 20 seconds prior to the first CS presentation.

Figure 4

(A) Experimental design diagram illustrating methodology for experiment 2. First, one rat from the triad was conditioned to 3 tone-shock pairings (0.7 mA footshock). The next day, the conditioned rat and one of his cage-mates (FCbP rat) were placed in the conditioning chamber and 3 tones were played. No shock US was present at this time. Four hours later, the third rat (until then, naive), as well as the FCbP rat, individually received 3 CS-US pairing (0.4 mA US). All rats (FC-0.7 mA [Blue], FC-0.4 mA [black], and FCbP+FC-0.4 mA [Red]) were tested 24 h later for their freezing response to the CS. (B) Effect of fear conditioning by proxy (FCbP) on subsequent conditioning. Rats conditioned using 0.7 mA shock US (Blue) froze significantly more than the rats conditioned using 0.4 mA shock US (Black) (p<0.05). Rats that were fear-conditioned by-proxy (Red) prior to being conditioned to tone shock pairings (0.4 mA US) froze significantly (p<0.05) more than the previously naïve rats conditioned using the same parameters. There was no significant difference between the rats conditioned with 0.7 mA shock US and the rats conditioned with a milder shock US (0.4 mA) who underwent FCbP prior to the CS-US pairing (p>.05).