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Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC
Daejong Jeon1,6, Sangwoo Kim1,2, Mattu Chetana1, Daewoong Jo3, H Earl Ruley4, Shih-Yao Lin5, Dania Rabah5, Jean-Pierre Kinet5 & Hee-Sup Shin1,2
Fear can be acquired vicariously through social observation of others suffering from aversive stimuli. We found that mice (observers) developed freezing behavior by observing other mice (demonstrators) receive repetitive foot shocks. Observers had higher fear responses when demonstrators were socially related to themselves, such as siblings or mating partners. Inactivation of anterior cingulate cortex (ACC) and parafascicular or mediodorsal thalamic nuclei, which comprise the medial pain system representing pain affection, substantially impaired this observational fear learning, whereas inactivation of sensory thalamic nuclei had no effect. The ACC neuronal activities were increased and synchronized with those of the lateral amygdala attheta rhythm frequency during this learning. Furthermore, an ACC-limited deletion of Cav1.2 Ca2+ channels in mice impaired observational fear learning and reduced behavioral pain responses. These results demonstrate the functional involvement of the affective pain system and Cav1.2 channels of the ACC in observational social fear.
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Fear is a biological response to dangerous, threatening situations or stimuli. Fear can be acquired and expressed in a variety of ways1. First, fear can be learned from direct experience of an adverse situation (for example, an unconditioned stimulus in classical Pavlovian fear conditioning). In a classical conditioning experiment, pairing of a neutral, conditioned stimulus (for example, a tone) with an aversive, unconditioned stimulus (for example, a foot shock) causes an animal to express fear behaviors when the animal is later exposed to the conditioned stimulus in the absence of the unconditioned stimulus. The neural mechanism and circuitry of this fear has been well studied across species, including rodents2,3. Fear can be socially acquired from instruction by verbal information (instructed fear) or from a vicarious observation of a conspecifics distress (observational fear) in primates, including humans1,4,5. For example, a higher primate can recognize fear by observing a conspecifics distressed face or a conspecific suffering from an enemy attack1,612. Previous studies using a bar-pressing protocol found that rats seeing a distressed conspecific (by electric shocks) display fearful behavioral responses, such as crouching or...