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      Primate Amygdala Neurons Simulate Decision Processes of Social Partners

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          Summary

          By observing their social partners, primates learn about reward values of objects. Here, we show that monkeys’ amygdala neurons derive object values from observation and use these values to simulate a partner monkey’s decision process. While monkeys alternated making reward-based choices, amygdala neurons encoded object-specific values learned from observation. Dynamic activities converted these values to representations of the recorded monkey’s own choices. Surprisingly, the same activity patterns unfolded spontaneously before partner’s choices in separate neurons, as if these neurons simulated the partner’s decision-making. These “simulation neurons” encoded signatures of mutual-inhibitory decision computation, including value comparisons and value-to-choice conversions, resulting in accurate predictions of partner’s choices. Population decoding identified differential contributions of amygdala subnuclei. Biophysical modeling of amygdala circuits showed that simulation neurons emerge naturally from convergence between object-value neurons and self-other neurons. By simulating decision computations during observation, these neurons could allow primates to reconstruct their social partners’ mental states.

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          Highlights

          • Amygdala neurons derive object values from own experience and social observation

          • Simulation neurons convert object values to predictions of social partner’s choices

          • Simulation neurons code signatures of decision computation during social observation

          • Simulation signals can emerge from converging value signals and self-other signals

          Abstract

          When monkeys observe and learn from each other’s choices, neurons in the amygdala spontaneously encode decision computations to simulate the social partner’s choices.

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          Most cited references39

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          Decision making in recurrent neuronal circuits.

          Decision making has recently emerged as a central theme in neurophysiological studies of cognition, and experimental and computational work has led to the proposal of a cortical circuit mechanism of elemental decision computations. This mechanism depends on slow recurrent synaptic excitation balanced by fast feedback inhibition, which not only instantiates attractor states for forming categorical choices but also long transients for gradually accumulating evidence in favor of or against alternative options. Such a circuit endowed with reward-dependent synaptic plasticity is able to produce adaptive choice behavior. While decision threshold is a core concept for reaction time tasks, it can be dissociated from a general decision rule. Moreover, perceptual decisions and value-based economic choices are described within a unified framework in which probabilistic choices result from irregular neuronal activity as well as iterative interactions of a decision maker with an uncertain environment or other unpredictable decision makers in a social group.
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            The primate amygdala represents the positive and negative value of visual stimuli during learning.

            Visual stimuli can acquire positive or negative value through their association with rewards and punishments, a process called reinforcement learning. Although we now know a great deal about how the brain analyses visual information, we know little about how visual representations become linked with values. To study this process, we turned to the amygdala, a brain structure implicated in reinforcement learning. We recorded the activity of individual amygdala neurons in monkeys while abstract images acquired either positive or negative value through conditioning. After monkeys had learned the initial associations, we reversed image value assignments. We examined neural responses in relation to these reversals in order to estimate the relative contribution to neural activity of the sensory properties of images and their conditioned values. Here we show that changes in the values of images modulate neural activity, and that this modulation occurs rapidly enough to account for, and correlates with, monkeys' learning. Furthermore, distinct populations of neurons encode the positive and negative values of visual stimuli. Behavioural and physiological responses to visual stimuli may therefore be based in part on the plastic representation of value provided by the amygdala.
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              The human amygdala in social judgment.

              Studies in animals have implicated the amygdala in emotional and social behaviours, especially those related to fear and aggression. Although lesion and functional imaging studies in humans have demonstrated the amygdala's participation in recognizing emotional facial expressions, its role in human social behaviour has remained unclear. We report here our investigation into the hypothesis that the human amygdala is required for accurate social judgments of other individuals on the basis of their facial appearance. We asked three subjects with complete bilateral amygdala damage to judge faces of unfamiliar people with respect to two attributes important in real-life social encounters: approachability and trustworthiness. All three subjects judged unfamiliar individuals to be more approachable and more trustworthy than did control subjects. The impairment was most striking for faces to which normal subjects assign the most negative ratings: unapproachable and untrustworthy looking individuals. Additional investigations revealed that the impairment does not extend to judging verbal descriptions of people. The amygdala appears to be an important component of the neural systems that help retrieve socially relevant knowledge on the basis of facial appearance.
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                Author and article information

                Contributors
                Journal
                Cell
                Cell
                Cell
                Cell Press
                0092-8674
                1097-4172
                02 May 2019
                02 May 2019
                : 177
                : 4
                : 986-998.e15
                Affiliations
                [1 ]Department of Physiology, Development and Neuroscience, University of Cambridge, Downing Street, Cambridge CB2 3DY, UK
                [2 ]Center for Brain and Cognition, Department of Technology and Information, Universitat Pompeu Fabra, Carrer Tànger, 122-140, 08018 Barcelona, Spain
                [3 ]Institució Catalana de la Recerca i Estudis Avançats, Universitat Barcelona, Passeig Lluís Companys 23, 08010 Barcelona, Spain
                Author notes
                []Corresponding author fg292@ 123456cam.ac.uk
                [4]

                Present address: Department of Neurosurgery, Massachusetts General Hospital, Harvard Medical School, 55 Fruit Street, Boston, MA 02114, USA

                [5]

                Lead Contact

                Article
                S0092-8674(19)30225-9
                10.1016/j.cell.2019.02.042
                6506276
                30982599
                d89d82b7-72dd-40d7-bf58-fb94e6da8c2e
                © 2019 The Author(s)

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

                History
                : 17 October 2018
                : 22 January 2019
                : 25 February 2019
                Categories
                Article

                Cell biology
                reward,decision-making,observational learning,social cognition,mirror neuron,autism,theory of mind,attractor network

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