Projection from the Anterior Cingulate Cortex to the Lateral Part of Mediodorsal Thalamus Modulates Vicarious Freezing B
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ORIGINAL ARTICLE
Projection from the Anterior Cingulate Cortex to the Lateral Part of Mediodorsal Thalamus Modulates Vicarious Freezing Behavior Chaowen Zheng1,2 • Yanwang Huang1,2 • Binshi Bo1 • Lei Wei1 • Zhifeng Liang1 Zuoren Wang1,2,3
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Received: 11 March 2019 / Accepted: 26 May 2019 Ó Shanghai Institutes for Biological Sciences, CAS 2019
Abstract Emotional contagion, a primary form of empathy, is present in rodents. Among emotional contagion behaviors, social transmission of fear is the most studied. Here, we modified a paradigm used in previous studies to more robustly assess the social transmission of fear in rats that experienced foot-shock. We used resting-state functional magnetic resonance imaging to show that foot-shock experience enhances the regional connectivity of the anterior cingulate cortex (ACC). We found that lesioning the ACC specifically attenuated the vicarious freezing behavior of foot-shock-experienced observer rats. Furthermore, ablation of projections from the ACC to the mediodorsal thalamus (MDL) bilaterally delayed the vicarious freezing responses, and activation of these projections decreased the vicarious freezing responses. Overall, our results demonstrate that, in rats, the ACC modulates vicarious freezing behavior via a projection to the MDL and provide clues to understanding the mechanisms underlying empathic behavior in humans. Keywords Rat Empathy Vicarious freezing Neuronal circuit
& Zuoren Wang [email protected] 1
Institute of Neuroscience, State Key Laboratory of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai 200031, China
2
University of Chinese Academy of Sciences, Beijing 100049, China
3
School of Future Technology, University of Chinese Academy of Sciences, Beijing 100049, China
Introduction Empathy refers to the capability of a subject to stand in another individual’s situation and experience the feelings of the latter [1]. It is a sophisticated psychological process vital for individuals to live in society. In addition, abnormalities in this ability are closely associated with mental diseases, such as autism spectrum disorder [2, 3] and schizophrenia [4–6]. Thus, defining the neuronal mechanisms underlying empathy could enable understanding and lead to cures for psychiatric disorders. Currently, these mechanisms in humans remain unknown, in part due to limited research methods. Initially, researchers defined empathy as unique to humans and apes [7, 8]. Now, increasing evidence has shown that empathy is evolutionarily conserved from rodents to humans [1, 9]. Although advanced empathic behaviors such as perspective-taking have not been defined in rodents, many studies support the idea that rodents exhibit emotional contagion [10, 11], a primary form of empathic behavior. In the hierarchy of empathic behaviors, emotional contagion refers to an individual’s ability to unconsciously mimic the emotional state of a conspecific [7] and is tho
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