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Research ArticleNew Research, Cognition and Behavior

Tactile Stimulation of the Face and the Production of Facial Expressions Activate Neurons in the Primate Amygdala

Clayton P. Mosher, Prisca E. Zimmerman, Andrew J. Fuglevand and Katalin M. Gothard
eNeuro 28 September 2016, 3 (5) ENEURO.0182-16.2016; DOI: https://doi.org/10.1523/ENEURO.0182-16.2016
Clayton P. Mosher
Department of Physiology, College of Medicine, The University of Arizona, Tucson, AZ, USA
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Prisca E. Zimmerman
Department of Physiology, College of Medicine, The University of Arizona, Tucson, AZ, USA
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Andrew J. Fuglevand
Department of Physiology, College of Medicine, The University of Arizona, Tucson, AZ, USA
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Katalin M. Gothard
Department of Physiology, College of Medicine, The University of Arizona, Tucson, AZ, USA
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  • Figure 1.
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    Figure 1.

    Example tactile neurons. Each panel shows the firing rate of a neuron during somatosensory stimulation of the face. The receptive fields are shaded in gray on the schematic drawing of the monkey face. The small arrows inside the receptive fields indicate the preferred direction of stimulation, if any. Raw traces of single-unit activity are shown to the right of the receptive fields. The red segments in the lines above the neural traces delineate periods of tactile stimulation; blue segments mark periods of production of a facial expression. The rasters and histograms are aligned to the start of stimulation (red dotted lines) or the start of the active facial expressions (blue dotted lines). The rasters are sorted by the duration of stimulation; for each trial the end of tactile stimulation is marked by a red dot. A, A neuron with a sustained (tonic) excitatory response during stimulation of the mouth and muzzle. During bared teeth displays (fear grimaces) produced by the monkey, this neuron showed patterns of activity that resembled the external stimulation of the muzzle. B, Transient, (phasic) excitatory responses to bilateral stimulation of the ears, forehead, and upper lip. This neuron also increased its firing rate during fear grimacing. C, Tonic inhibitory response elicited by touching the lips and during the production of fear grimaces and in preparation to receive food or accept a nonfood item in the mouth. Other facial expressions that involved lip movements did not elicit changes in neural activity. D, Tonic excitatory response to tactile stimulation anywhere on the face. This neuron did not respond during the production of facial expressions.

  • Figure 2.
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    Figure 2.

    Population activity and bilateral receptive fields. A, The colors in this illustration indicate the proportion of cells that responded to tactile stimulation on each facial region. Note that these values add up to more than 100% because the majority of cells responded to the touch of multiple facial regions. B, Mean normalized firing rate of the population of tactile cells during stimulation of the left and right sides of the face (no significant difference, α = 0.05). C, D, Example neurons with bilateral (C) and unilateral (D) receptive fields. Rasters (top) and PSTHs (bottom) indicate the firing rate of the two neurons before and after tactile stimulation (zero on the x axis corresponds to the onset of stimulation). Trials shown in black and red correspond to stimulation of the left and right face, respectively. E, Mean normalized population firing rate of all tactile cells. F, Histogram showing the number of tactile cells that responded with a significant change in firing rate at each time bin following stimulation (bin size = 100 ms with 20-ms sliding window). Tactile cells modulate their firing rate throughout stimulation. The time bin at which the highest number of cells responded was 270–370 ms after stimulation onset.

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    Figure 3.

    The combined effects of tactile stimulation and facial movement. The top three panels show rasters (top) and PSTHs (bottom) for the three example cells. Neural activity elicited by touch alone is shown in black, whereas neural activity elicited by touch and movement is shown in gray. On each raster, the end of the tactile stimulation is indicated by the red dot. The touch events are sorted by duration. A, no difference in firing rate during touch alone and touch that elicited facial movement. B, increased response duration for touches that elicited facial movement. C, increased firing rate for touches that elicited facial movment. D, Comparison of the normalized firing elicited in the same population of neurons by touch alone (black) and touch combined with facial movements (gray). In general, tactile stimulation combined with facial expressions led to higher firing rates. The red bar above the population histogram indicated the bins in which the firing rates are significantly different (Wilcoxon rank-sum test, α = 0.001)

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    Figure 4.

    MRI-based reconstruction of recording sites. Filled circles mark the location of tactile neurons on a representative coronal section through the amygdala and are color-coded for the location of their receptive fields (yellow = nose, blue = eye region, green = muzzle, red = mouth, gray = chin, purple = ear, orange = cheek). Open circles represent neurons with large receptive fields that covered the entire face and are shown on every panel. Neurons with multiple receptive fields are shown in each panel that corresponds to their receptive fields. Histological verification of electrode location in the amygdala is from monkey Q. The arrowhead indicates an electrolytic lesion applied to the site where the neuron shown in Figure 1C was recorded. opt, optic tract; ent, entorhinal cortex; L, lateral nucleus; B, basal nucleus; AB, accessory basal nucleus; Ce, central nucleus; M, medial nucleus).

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Tactile Stimulation of the Face and the Production of Facial Expressions Activate Neurons in the Primate Amygdala
Clayton P. Mosher, Prisca E. Zimmerman, Andrew J. Fuglevand, Katalin M. Gothard
eNeuro 28 September 2016, 3 (5) ENEURO.0182-16.2016; DOI: 10.1523/ENEURO.0182-16.2016

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Tactile Stimulation of the Face and the Production of Facial Expressions Activate Neurons in the Primate Amygdala
Clayton P. Mosher, Prisca E. Zimmerman, Andrew J. Fuglevand, Katalin M. Gothard
eNeuro 28 September 2016, 3 (5) ENEURO.0182-16.2016; DOI: 10.1523/ENEURO.0182-16.2016
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Keywords

  • emotion
  • face
  • monkey
  • social communication
  • somatosensory
  • Touch

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