Social modulation of learning in rats

Abstract

It is well known that emotions participate in the regulation of social behaviors and that the emotion displayed by a conspecific influences the behavior of other animals. In its simplest form, empathy can be characterized as the capacity to be affected by and/or share the emotional state of another. However, to date, relatively little is known about the mechanisms by which animals that are not in direct danger share emotions. In the present study, we used a model of between-subject transfer of fear to characterize the social interaction during which fear is transmitted, as well as the behavioral effects of socially transmitted fear. We found that (1) during social interaction with a recently fear-conditioned partner, observers and demonstrators exhibit social exploratory behaviors rather than aggressive behaviors; (2) learning and memory in a shock-motivated shuttle avoidance task are facilitated in rats that underwent a social interaction with a partner that had been fear conditioned; and (3) a brief social interaction with a recently fear-conditioned partner immediately before fear conditioning increases conditioned freezing measured on the next day. The observed effects were not due to a stress-induced increase in pain sensitivity or analgesia. Collectively, these data suggest that a brief social interaction with a cage mate that has undergone an aversive learning experience promotes aversive learning in an otherwise naïve animal. We argue that socially transferred fear is an adaptation that promotes defensive behavior to potentially dangerous situations in the environment.

Figure 1.

Interaction with a recently fear-conditioned partner improves acquisition and retention of two-way avoidance response. All behavioral parameters presented were registered during two consecutive 50-trial sessions of two-way avoidance training. (A) Scheme of the experiment. (B) Percentage of avoidance response in five 10-trial blocks. (C) Cumulated distribution of latency of avoidance (shorter than 5 sec) and escape responses (longer than 5 sec). (D) Frequency of crossings during the adaptation period (before the first CS and US were delivered) in the first (a1) and the second (a2) session and during intertrial intervals (ITRs) in five 10-trial blocks. (So) Observers paired with fear-conditioned demonstrators; (NSo) observers paired with demonstrators exposed to a novel cage; (SINGLE) animals trained and tested without any social interaction; (*) P < 0.05; (**) P < 0.01; (***) P < 0.001.

Figure 2.

Interaction with a recently fear-conditioned partner improves fear memory. (A) Scheme of the experiment. (B) Familiar rats: Percentage of freezing measured during 3 min preceding a footshock during the training day (TRAIN) and 3 min during exposure to the experimental cage on the test day (TEST). (So) Observers paired with fear-conditioned demonstrators; (NSo) observers paired with demonstrators merely exposed to a novel cage; (SINGLE) animals trained and tested without any social interaction; (*) P < 0.05.

Figure 3.

Interaction with a recently fear-conditioned partner improves fear memory also in unfamiliar rats. Percentage of freezing measured during 3 min preceding a footshock during the training day (TRAIN) and 3 min during exposure to the experimental cage on the test day (TEST). (So) Observers paired with fear-conditioned demonstrators; (NSo) observers paired with demonstrators merely exposed to a novel cage; (*) P < 0.05.

Figure 4.

Interaction with recently fear-conditioned partner causes neither increase in pain sensitivity nor analgesia. Both hot plate (A) and tail-flick (B) tests showed no differences in response to acute pain between the observers paired with either shocked (So) or non-shocked (NSo) demonstrators. Pain sensitivity thresholds were measured (A) before the social interaction (baseline level), (B) immediately after the social interaction, and (C) 24 h after the social interaction.