The majority of neurophysiological studies that explored the role of the primate amygdala in the evaluation of social signals relied on visual stimuli such as images of facial expressions. Vision, however, is not the only sensory modality that carries social signals. Both humans and non-human primates exchange emotionally meaningful social signals through touch. Indeed, social grooming in non-human primates and caressing touch in humans is critical for building lasting and reassuring social bonds. To determine the role of the amygdala in processing touch, we recorded the responses of single neurons in the macaque amygdala while we applied tactile stimuli to the face. We found that 1/3 of the recorded neurons responded to tactile stimulation. Although we recorded exclusively from the right amygdala, the receptive fields of 98% of the neurons were bilateral. A fraction of these tactile neurons were monitored during the production of facial expressions and during facial movements elicited occasionally by touch stimuli. Firing rates arising during the production of facial expressions were similar to those elicited by tactile stimulation. In a subset of cells combining tactile stimulation with facial movement further augmented the firing rates. This suggests that tactile neurons in the amygdala receive input from skin mechanoceptors that are activated by touch and by compressions and stretches of the facial skin during the contraction of the underlying muscles. Tactile neurons in the amygdala may play a role in extracting the valence of touch stimuli and/or in monitoring the facial expressions of self during social interactions.
Significance Statement: The primate amygdala receives sensory inputs of all modalities, yet remarkably little is known about how the amygdala may process touch. Here we report for the first time that neurons in the monkey amygdala respond to touching the face. Similar to visually responsive neurons, tactile neurons in the amygdala may be involved in extracting the positive or negative valence of touch stimuli. The activity of these neurons was modulated during the production of facial expressions and the contraction of facial muscles suggesting that these neurons can also signal the expressive status of the face. The presence of touch-sensitive neurons in the primate amygdala expands the known functions of this important structure for emotion and social communication with facial expressions.
Authors report no conflict of interest.
R21NIMH 086065; P50MH 100023; NSF Graduate Fellowship.