Tactile Stimulation of the Face and the Production of Facial Expressions Activate Neurons in the Primate Amygdala (original) (raw)

The role of the amygdala in processing social and affective touch

2021

The amygdala plays a central role in socio-emotional behavior, yet its role in processing affective touch is not well established. Longitudinal studies reveal that touch-deprived infants show later in life exaggerated emotional reactivity related to structural and functional changes in the amygdala. The connectivity of the amygdala is well-suited to process the sensory features and the socio-cognitive dimensions of touch. The convergent processing of bottom-up and top-down touch-related inputs in the amygdala triggers autonomic responses. The positive hedonic value of touch in humans and grooming in non-human primates is correlated with vagal tone and the release of oxytocin and endogenous opioids. Grooming reduces vigilance that has been shown to depend critically on the amygdala. Touch-induced vagal tone and lowered vigilance alter neural activity in the amygdala. Under these circumstances neurons no longer respond to each touch stimulus, rather they appear to signal a sustained f...

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

Wiley Interdisciplinary Reviews: Cognitive Science, 2017

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.

Role of the monkey amygdala in social cognition

International Congress Series, 2003

Recent studies demonstrated the role of the primate amygdala (AM) in social cognition. In the present study, neuronal responses in the monkey amygdala were analyzed during discrimination of facial expressions and discrimination of various rewarding and aversive stimuli, such as food and objects associated with electric shock. The results indicated that activity of some amygdalar neurons preferentially increased in response to human facial expressions. Patterns of correlation coefficients between the different facial expressions indicated that facial expressions of a familiar person to the monkey were more discriminately represented than those of unfamiliar persons. Furthermore, responses of these neurons to facial expressions seemed to be independent of reward contingency. Other neurons responded to various objects that were biologically important, including food as reward and real humans. These amygdalar neurons displayed modulation of responses to the objects in various situations, including satiation and reversal, and modulation of responses to real humans who approached and withdrew from the monkey. These results suggest that there are at least two classes of amygdalar neurons: one type of neuron is involved in processes independent of one's own emotional state such as recognition of facial expression and inferring the emotional states of other persons, and the other type is involved in the ongoing evaluation of all sensory stimuli based on one's own emotional state.

Brain mechanisms for processing affective touch

Human Brain Mapping, 2013

Despite the crucial role of touch in social development, there is very little functional magnetic resonance imaging (fMRI) research on brain mechanisms underlying social touch processing. The ''skin as a social organ'' hypothesis is supported by the discovery of C-tactile (CT) nerves that are present in hairy skin and project to the insular cortex. CT-fibers respond specifically well to slow, gentle touch such as that which occurs during close social interactions. Given the social significance of such touch researchers have proposed that the CT-system represents an evolutionarily conserved mechanism important for normative social development. However, it is currently unknown whether brain regions other than the insula are involved in processing CT-targeted touch. In the current fMRI study, we sought to characterize the brain regions involved in the perception of CT-supported affective touch. Twenty-two healthy adults received manual brush strokes to either the arm or palm. A direct contrast of the blood-oxygenation-level-dependent (BOLD) response to gentle brushing of the arm and palm revealed the involvement of a network of brain regions, in addition to the posterior insula, during CTtargeted affective touch to the arm. This network included areas known to be involved in social perception and social cognition, including the right posterior superior temporal sulcus and the medial prefrontal cortex (mPFC)/dorso anterior cingulate cortex (dACC). Connectivity analyses with an mPFC/dACC seed revealed coactivation with the left insula and amygdala during arm touch. These findings characterize a network of brain regions beyond the insula involved in coding CT-targeted affective touch. Hum Brain Mapp 00:000-000,

Radiotelemetered activity from the amygdala during social interactions in the monkey

Experimental Neurology, 1979

Electrical activity from the amygdaloid nucleus in freely moving monkeys (Cercopithecus aethiops) during social interactions and alone were recorded via radiotelemetry. Spectral analysis of amygdaloid activity revealed highest power outputs occurred during behaviors related to sexual and aggressive interactions and the lowest with the tension-reducing behavior of grooming. Power output was not directly related to motor activity. These results suggest that amygdaloid activity is related to the emotional significance and degree of ambiguity of an interaction. It is hypothesized that at least two separate tierent systems, one for low frequencies and the other for fast frequencies, may be correlated with different behavioral events.

Neurons in the amygdala of the monkey with responses selective for faces

Behavioural Brain Research, 1985

To investigate the functions of the amygdala in visual information processing and in emotional and social responses, recordings were made from single neurons in the amygdala of the monkey. A population of neurons (40 of more than 1000 recorded in 4 monkeys) was investigated which responded primarily to faces. These neurons typically (1) responded to some human or monkey faces, which were presented to the monkey through a large aperture shutter so that response latencies could be measured, or were simply shown to the monkey, (2) responded to 2-dimensional representations of these faces, as well as to real 3-dimensional faces, (3) had no responses or only small (less than half maximum) responses to gratings, simple geometrical, other complex 3-D stimuli, or to arousing and aversive stimuli, (4) had response latencies of 110-200 ms, (5) were located in the basal accessory nucleus of the amygdala, (6) responded differently to different faces, as shown by measures ofd', and could thus over a population of such neurons code information useful for making different responses to different individuals, (7)could in some cases (9/11 tested) respond to parts of faces, and (8) in a few cases (4/19 tested) responded more to a face which produced an emotional response. A comparison made in three monkeys of the responses of these neurons with the responses of 77 neurons with face-selective responses recorded in the cortex of the superior temporal sulcus (STS) showed that the amygdaloid neurons had longer response latencies (110-200 compared to 90-140 ms), and were in some respects more selective in their responses to different faces. It is suggested that the deficits in social and emotional behavior produced by amygdala lesions could be due in part to damage to a neuronal system specialized in utilizing information from faces so that appropriate social and emotional responses can be made to different individuals.

Selective processing of social stimuli in the superficial amygdala

Human Brain Mapping, 2009

The human amygdala plays a pivotal role in the processing of socially significant information. Anatomical studies show that the human amygdala is not a single homogeneous structure but is composed of segregable subregions. These have recently been functionally delineated by using a combination of functional magnetic resonance imaging (fMRI) and cytoarchitectonically defined probabilistic maps. However, the response characteristics and individual contribution of these subregions to the processing of social-emotional stimuli are little understood. Here, we used this novel technique to segregate intra-amygdalar responses to facial expressions and nonsocial control stimuli. We localized facial expression-evoked signal changes bilaterally in the superficial amygdala, which suggests that this subregion selectively extracts the social value of incoming sensory information. Hum Brain Mapp 00:000-000,

Reading the mind in the touch: Neurophysiological specificity in the communication of emotions by touch

Neuropsychologia, 2017

Touch is central to interpersonal interactions. Touch conveys specific emotions about the touch provider, but it is not clear whether this is a purely socially learned function or whether it has neurophysiological specificity. In two experiments with healthy participants (N = 76 and 61) and one neuropsychological single case study, we investigated whether a type of touch characterised by peripheral and central neurophysiological specificity, namely the C tactile (CT) system, can communicate specific emotions and mental states. We examined the specificity of emotions elicited by touch delivered at CT-optimal (3cm/s) and CT-suboptimal (18cm/s) velocities (Experiment 1) at different body sites which contain (forearm) vs. do not contain (palm of the hand) CT fibres (Experiment 2). Blindfolded participants were touched without any contextual cues, and were asked to identify the touch provider's emotion and intention. Overall, CT-optimal touch (slow, gentle touch on the forearm) was s...

Bringing Touch Back to the Study of Emotions in Human and Non-Human Primates: A Theoretical Exploration

International Journal of Comparative Psychology, 2018

This paper provides a theoretical exploration of how comparative research on the expression of emotions has traditionally focused on the visual mode and argues that, given the neurophysiological, developmental, and behavioral evidence that links touch with social interactions, focusing on touch can become an ideal mode to understand the communication of emotions in human and non-human primates. This evidence shows that touch is intrinsically linked with social cognition because it motivates human and non-human animals, from birth, to form social bonds. It will be shown that touch is one of the modes of interaction used by the mother-infant or caregiver-infant dyad that facilitates the expression of emotions by the infant (and later the expression of emotions by the adult that the infant has become) in ways that are understood by other members of the group.