Anterior cingulate inputs to nucleus accumbens control the social transfer of pain and analgesia

• Published in: Science (American Association for the Advancement of Science) Vol. 371; no. 6525; pp. 153 - 159
• Main Authors: Smith, Monique L., Asada, Naoyuki, Malenka, Robert C.
• Format: Journal Article
• Language: English
• Published: United States The American Association for the Advancement of Science 08.01.2021
• Subjects: Amygdala; Analgesia; Analgesia - psychology; Animal behavior; Animal models; Animals; Basolateral Nuclear Complex - physiology; Brain; Circuits; Cognitive ability; Communication; Cortex (cingulate); Emotional behavior; Emotional factors; Emotions; Empathy; Empathy - physiology; Fear; Fear - physiology; Female; Gyrus Cinguli - physiology; Hyperalgesia; Inflammation; Information processing; Interpersonal Relationship; Lyssavirus; Male; Mental disorders; Mice; Morphine; Morphine - administration & dosage; Nervous system; Neural networks; Neurons; Nucleus accumbens; Nucleus Accumbens - physiology; Optogenetics; Pain; Pain - drug therapy; Pain - psychology; Pain perception; Pain sensitivity; Rabies; Rodents; Social behavior; Social factors; Social interaction; Social interactions; Somatosensory cortex
• ISSN: 0036-8075; 1095-9203; 1095-9203
• DOI: 10.1126/science.abe3040

In mice, both pain and fear can be transferred by short social contact from one animal to a bystander. Neurons in a brain region called the anterior cingulate cortex in the bystander animal mediate these transfers. However, the specific anterior cingulate projections involved in such empathy-related behaviors are unknown. Smith et al. found that projections from the anterior cingulate cortex to the nucleus accumbens are necessary for the social transfer of pain in mice (see the Perspective by Klein and Gogolla). Fear, however, was mediated by projections from the anterior cingulate cortex to the basolateral amygdala. Interestingly, in animals with pain, analgesia can also be transferred socially. Science , this issue p. 153 ; see also p. 122 In mice, distinct neuronal circuits are involved in empathy for companion animals who are observed to be experiencing pain or pain relief versus fear. Empathy is an essential component of social communication that involves experiencing others’ sensory and emotional states. We observed that a brief social interaction with a mouse experiencing pain or morphine analgesia resulted in the transfer of these experiences to its social partner. Optogenetic manipulations demonstrated that the anterior cingulate cortex (ACC) and its projections to the nucleus accumbens (NAc) were selectively involved in the social transfer of both pain and analgesia. By contrast, the ACC→NAc circuit was not necessary for the social transfer of fear, which instead depended on ACC projections to the basolateral amygdala. These findings reveal that the ACC, a brain area strongly implicated in human empathic responses, mediates distinct forms of empathy in mice by influencing different downstream targets.