Shared response neurons in anterior cingulate and insular cortices engage in empathy-like behaviors of the rat
Date Issued
2016
Date
2016
Author(s)
Wu, Wen-Yi
Abstract
Studies have shown prosocial behaviors, including empathy-like acts, in rodents, but its neural substrates remain elusive. Evidence from human studies implicates the anterior cingulate (ACC) and insular cortices (InC) in pain empathy and thus predicts that certain neurons in these regions might be engaged by a subject’s sensing itself in pain as well as by its sensing others in pain. The present study addressed this issue by recording behavioral and single unit responses of the ACC and InC while noxious radiant heat was applied to a rat or its nearby companion (Chapter 2). Results showed that rats increased freezing behavior not only when receiving noxious stimuli but also when observing a companion being hurt. The observer rats also increased social approach to the companion. We found that 14.7% neurons in the ACC and 13.7% neurons in the InC responded to the pain stimuli applied to a nearby rat. These ratios were significantly higher than those responding to air radiation (7.6% and 5.5% in the ACC and InC, respectively). Furthermore, such behavioral and neuronal changes were absent in the visual-deprived control group. Interestingly, among these vicarious pain responsive units, 53.9% and 66.3% in the ACC and InC also responded, with the same or opposite direction (denoted as shared- or anti-response, respectively), to its own pain. Percentage of shared-response neurons in the ACC and InC also decreased from 40.8% to 30.8% by blocking the companion rat from observer with an opaque divider. To investigate the functional significance of the shared- and anti-response neurons, we examined the correlation between neuronal activity and social approach or freezing behaviors. We found enhanced activities in both shared- and anti-response neurons prior to and during the social approach behavior. Such enhancement was not seen for those neurons responding to laser heat pulses directed to the air. Inhibited activities were shown specifically in anti-response neurons. Furthermore, to test the pro-social significance of the shared- and anti-response neurons, we applied a behavioral paradigm relevant to empathy, in which a freely moving rat was trained to rescue a conspecific from a restraining trap (Bartal et al., Science 334: 1427, 2011) (Chapter 3). 48.9%, 58.8% and 51.8% of neurons responding to vicarious pain in the ACC, InC and primary motor cortex (MI) respectively, were either shared- or anti-response neurons. The shared-response neurons showed changes in the ensemble activity just prior to rescue behavior and did not show any change in the control conditions in which the restrainer was empty or had a toy rat in it. In addition, the neuronal activity recorded in the rescuing behavior showed that a group (25.9%) of ACC and InC neurons changed their activity at 0 to 5s prior to the specific rescue action for a rat which we called rescuing-related neurons, whereas the activity of MI ensembles increased around the gate-opening acts no matter they subserved rescue or not. Coherently, these rescuing-related neurons also responded with their ensemble activity to both other’s pain and self’s pain. These findings suggest that observation of a conspecific in pain may engage the shared-response neurons in rat’s cortex and their activity may be related to social approach behaviors and contribute to prosocial rescuing acts.
Subjects
prosocial behavior
single-unit recording
behavioral neurophysiology
limbic cortex
primary motor cortex
Type
thesis
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