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      Emotional Mirror Neurons in the Rat’s Anterior Cingulate Cortex

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          Summary

          How do the emotions of others affect us? The human anterior cingulate cortex (ACC) responds while experiencing pain in the self and witnessing pain in others, but the underlying cellular mechanisms remain poorly understood. Here we show the rat ACC (area 24) contains neurons responding when a rat experiences pain as triggered by a laser and while witnessing another rat receive footshocks. Most of these neurons do not respond to a fear-conditioned sound (CS). Deactivating this region reduces freezing while witnessing footshocks to others but not while hearing the CS. A decoder trained on spike counts while witnessing footshocks to another rat can decode stimulus intensity both while witnessing pain in another and while experiencing the pain first-hand. Mirror-like neurons thus exist in the ACC that encode the pain of others in a code shared with first-hand pain experience. A smaller population of neurons responded to witnessing footshocks to others and while hearing the CS but not while experiencing laser-triggered pain. These differential responses suggest that the ACC may contain channels that map the distress of another animal onto a mosaic of pain- and fear-sensitive channels in the observer. More experiments are necessary to determine whether painfulness and fearfulness in particular or differences in arousal or salience are responsible for these differential responses.

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          Highlights

          • Rat ACC contains mirror-like neurons responding to pain experience and observation

          • Most do not respond to another salient negative emotion: fear

          • One can decode pain intensity in the self from a pattern decoding pain in others

          • Deactivating this region (area 24) impairs the social transmission of distress

          Abstract

          Carrillo et al. show the rat anterior cingulate cortex contains emotional mirror neurons that respond when a rat experiences pain and witnesses another rat in pain but not while experiencing another salient emotion, fear. After cingulate deactivation, rats show reduced distress when witnessing another receive a shock.

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          Most cited references34

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          Empathy for pain involves the affective but not sensory components of pain.

          Our ability to have an experience of another's pain is characteristic of empathy. Using functional imaging, we assessed brain activity while volunteers experienced a painful stimulus and compared it to that elicited when they observed a signal indicating that their loved one--present in the same room--was receiving a similar pain stimulus. Bilateral anterior insula (AI), rostral anterior cingulate cortex (ACC), brainstem, and cerebellum were activated when subjects received pain and also by a signal that a loved one experienced pain. AI and ACC activation correlated with individual empathy scores. Activity in the posterior insula/secondary somatosensory cortex, the sensorimotor cortex (SI/MI), and the caudal ACC was specific to receiving pain. Thus, a neural response in AI and rostral ACC, activated in common for "self" and "other" conditions, suggests that the neural substrate for empathic experience does not involve the entire "pain matrix." We conclude that only that part of the pain network associated with its affective qualities, but not its sensory qualities, mediates empathy.
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            Switching on and off fear by distinct neuronal circuits.

            Switching between exploratory and defensive behaviour is fundamental to survival of many animals, but how this transition is achieved by specific neuronal circuits is not known. Here, using the converse behavioural states of fear extinction and its context-dependent renewal as a model in mice, we show that bi-directional transitions between states of high and low fear are triggered by a rapid switch in the balance of activity between two distinct populations of basal amygdala neurons. These two populations are integrated into discrete neuronal circuits differentially connected with the hippocampus and the medial prefrontal cortex. Targeted and reversible neuronal inactivation of the basal amygdala prevents behavioural changes without affecting memory or expression of behaviour. Our findings indicate that switching between distinct behavioural states can be triggered by selective activation of specific neuronal circuits integrating sensory and contextual information. These observations provide a new framework for understanding context-dependent changes of fear behaviour.
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              Empathy and pro-social behavior in rats.

              Whereas human pro-social behavior is often driven by empathic concern for another, it is unclear whether nonprimate mammals experience a similar motivational state. To test for empathically motivated pro-social behavior in rodents, we placed a free rat in an arena with a cagemate trapped in a restrainer. After several sessions, the free rat learned to intentionally and quickly open the restrainer and free the cagemate. Rats did not open empty or object-containing restrainers. They freed cagemates even when social contact was prevented. When liberating a cagemate was pitted against chocolate contained within a second restrainer, rats opened both restrainers and typically shared the chocolate. Thus, rats behave pro-socially in response to a conspecific's distress, providing strong evidence for biological roots of empathically motivated helping behavior.
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                Author and article information

                Contributors
                Journal
                Curr Biol
                Curr. Biol
                Current Biology
                Cell Press
                0960-9822
                1879-0445
                22 April 2019
                22 April 2019
                : 29
                : 8
                : 1301-1312.e6
                Affiliations
                [1 ]Social Brain Lab, Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, Meibergdreef 47, 1105 BA Amsterdam, the Netherlands
                [2 ]Department of Psychology, University of Amsterdam, Nieuwe Achtergracht 166, 1018 WV Amsterdam, the Netherlands
                Author notes
                []Corresponding author c.keysers@ 123456nin.knaw.nl
                [3]

                These authors contributed equally

                [4]

                Deceased

                [5]

                Present address: Cognitive Psychology Unit, Institute of Psychology, Leiden University, Wassenaarseweg 52, 2333 AK Leiden, the Netherlands

                [6]

                Lead Contact

                Article
                S0960-9822(19)30322-7
                10.1016/j.cub.2019.03.024
                6488290
                30982647
                2a41c013-d120-4199-9f63-444e19a8f8e1
                © 2019 The Author(s)

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 1 December 2018
                : 11 March 2019
                : 14 March 2019
                Categories
                Article

                Life sciences
                empathy,mirror neurons,emotional contagion,vicarious activity,causality,fear,pain,social behavior,rodent

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