Social modulation of learning in rats

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.Human empathy can be defined as the ability to experience and share the thoughts and feelings of others (de Waal 2008). Obviously, this is a complex social phenomenon that, until recently, has received much attention from philosophers and psychologists rather than neuroscientists (Decety and Lamm 2006). However, in its simplest form, empathy can be characterized as the capacity to be affected by and/or share the emotional state of another (de Waal 2008). Tuning one''s emotional state to that of another increases the probability of similar behavior, which thereby allows rapid adaptation to environmental challenges (Hatfield et al. 1994). This social adaptation may be particularly important for emotions that signal a potential danger, such as fear. Although one can learn about potentially harmful stimuli by directly experiencing an aversive event, observation or interaction with a conspecific in danger and/or in pain may also provide information about threats in the environment. There is a vast literature on learning about direct danger (Maren 2001) as well as sharing emotions through observation (see, e.g., Church 1959; Langford et al. 2006; Olsson and Phelps 2007). However, relatively little is known about the mechanisms by which animals that are not in a direct danger share emotions.We have recently designed an experimental rat model of between-subject transfer of emotional information (Knapska et al. 2006). In this model, rats are housed in pairs and one member of the pair (the “demonstrator”) is removed and subjected to fear conditioning. After the fear-conditioning episode, the conditioned animal is allowed to interact with its naïve cage mate (the “observer”). We showed that the demonstrator''s fear is socially transferred to the observer, resulting in both rapid increase in exploratory behavior of the observer and a pattern of c-Fos activation in the observer''s amygdala that parallels that of the shocked demonstrators.These results suggest that the social interaction between the demonstrator and observer results in a transfer of information that promotes aversively motivated learning in the observer. However, the nature of the social interaction and how it comes to influence aversively motivated behavior is not known. Therefore, the present study aimed to characterize the behavior of both the demonstrators and observers during their social interaction and further characterize the nature of the influence of socially transmitted fear on aversively motivated learning and memory. We hypothesized that the social interaction between observers and demonstrators would result in a social transfer of fear that would promote learning and memory of both active defensive responses (avoidance) as well as defensive immobility (freezing). To test this hypothesis, we carried out five experiments that examined the nature of the social interaction between shocked demonstrators and observers (Experiment 1), the acquisition and retention of active avoidance (Experiment 2), and conditioned freezing (Experiment 3). Because it is not clear if social transfer effects can be observed among unfamiliar animals and to control for social buffering, we also compared the social transfer of fear in familiar and unfamiliar rats (Experiment 4). To control for the possible influence of different pain sensitivity thresholds in the observers paired with shocked demonstrators, we carried out pain tests (Experiment 5).