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WIREs Cogn Sci
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New perspectives on the neurophysiology of primate amygdala emerging from the study of naturalistic social behaviors

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A major challenge of primate neurophysiology, particularly in the domain of social neuroscience, is to adopt more natural behaviors without compromising the ability to relate patterns of neural activity to specific actions or sensory inputs. Traditional approaches have identified neural activity patterns in the amygdala in response to simplified versions of social stimuli such as static images of faces. As a departure from this reduced approach, single images of faces were replaced with arrays of images or videos of conspecifics. These stimuli elicited more natural behaviors and new types of neural responses: (1) attention‐gated responses to faces, (2) selective responses to eye contact, and (3) selective responses to touch and somatosensory feedback during the production of facial expressions. An additional advance toward more natural social behaviors in the laboratory was the implementation of dyadic social interactions. Under these conditions, neurons encoded similarly rewards that monkeys delivered to self and to their social partner. These findings reinforce the value of bringing natural, ethologically valid, behavioral tasks under neurophysiological scrutiny.

Fixation‐aligned face cell activity in the human and monkey amygdala. (a) An example stimulus array that was used for neural recordings in humans and monkeys. The dotted line indicates the image that was fixated first. Note that each species fixated first on a conspecific face. (b) Cross sections through the human and monkey brain [obtained from Magnetic resonance imaging (MRI)] indicating in the component nuclei of the amygdala in different colors. To the right of these images are representative segments of raw neural recordings. Every thin vertical line is an action potential fired by a neuron. (c) The continuous black lines indicate the vertical eye movements of the subjects. The quasi‐horizontal and vertical segments of the solid black line correspond to fixations and saccades, respectively. The yellow and purple bars correspond to fixations on one or multiple faces that are shown above. The action potentials generated during these recordings are indicated by red dots at the bottom of the graph. Note the higher spike density during fixations on faces. These data show that face‐selective activity in both the human and monkey amygdala is gated by fixations, the behavioral instantiations of visual attention. (Reprinted with permission from Ref . Copyright 2017 Cell Press 2017)
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Example tactile neuron from the monkey amygdala. (a) The area shaded in gray shows the receptive field of this neuron in the monkey face. The small arrows indicate the preferred direction of stimulation. (b) Raw traces of single‐unit activity. The red lines above the raw traces indicate tactile stimulation of the face; the blue lines indicate the production of a facial expression (fear grimace). (c) Rasters and histograms aligned to the start of tactile stimulation (red dashed line) or the start of the facial expressions (blue dashed line). The rasters are sorted by the duration of stimulation; for each trial, the end of tactile stimulation is marked by a red dot. The neuron shown here responded to touch with a sustained increase in firing rate. (d) During bared‐teeth displays (fear grimaces) produced by the monkey, this neuron showed patterns of activity that resembled the external stimulation of the muzzle. (Reprinted with permission from Ref . Copyright 2016 eNeuro)
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Eye cells in the monkey amygdala. (a) Neural activity was analyzed during three types of fixations while viewing movies: fixations on the eyes that were preceded by fixations elsewhere (blue), fixations on another facial feature that were preceded by fixations on the eyes (yellow), and fixations on other features that were preceded by fixations on other areas (red). (b) Raster plots and peri‐event time histograms illustrating the activity of two example neurons during the three fixation types listed above. Rasters are sorted by fixation duration. Fixations begin at 0 second and end at the curved line. This neuron showed increased firing rate (relative to the periods preceding this fixation) as long as the viewer monkey fixated eyes of the monkey in the video. Fixations on other facial features did not have the same effect. (c) This neuron showed a brief, phasic increase in firing rate during the first 200–300 milliseconds after the onset of each fixation on the eyes. (Reprinted with permission from Ref . Copyright 2014 Elsevier)
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Facial expressions provoked by viewing of videos of conspecifics elicit distinct patterns of EMG activity. Each row shows the raw EMG from five muscles: fron., frontalis; o.ar., orbito‐auricularis; s.ar. and p.ar., superior and posterior auricularis, respectively, and zyg., zygomatic. Note the rhythmic and complementary bursting during lipsmacks. High amplitude electromyographic (EMG) signals of p.ar., zyg., and o.ar. are clipped in yawn and fear grimace.
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