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The impact of C-tactile low-threshold mechanoreceptors on affective touch and social interactions in mice.

ABSTRACT: Affective touch is necessary for proper neurodevelopment and sociability. However, it remains unclear how the neurons innervating the skin detect affective and social behaviors. The C low-threshold mechanoreceptors (C-LTMRs), a specific population of somatosensory neurons in mice, appear particularly well suited, physiologically and anatomically, to perceive affective and social touch. However, their contribution to sociability has not been resolved yet. Our observations revealed that C-LTMR functional deficiency induced social isolation and reduced tactile interactions in adulthood. Conversely, transient increase in C-LTMR excitability in adults, using chemogenetics, was rewarding, promoted touch-seeking behaviors, and had prosocial influences on group dynamics. This work provides the first empirical evidence that specific peripheral inputs alone can drive complex social behaviors. It demonstrates the existence of a specialized neuronal circuit, originating in the skin, wired to promote interactions with other individuals.

SUBMITTER: Huzard D

PROVIDER: S-EPMC9242590 | biostudies-literature | 2022 Jul

REPOSITORIES: biostudies-literature

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The impact of C-tactile low-threshold mechanoreceptors on affective touch and social interactions in mice.

Huzard Damien D Martin Miquel M Maingret François F Chemin Jean J Jeanneteau Freddy F Mery Pierre-François PF Fossat Pascal P Bourinet Emmanuel E François Amaury A

Science advances 20220629 26

Affective touch is necessary for proper neurodevelopment and sociability. However, it remains unclear how the neurons innervating the skin detect affective and social behaviors. The C low-threshold mechanoreceptors (C-LTMRs), a specific population of somatosensory neurons in mice, appear particularly well suited, physiologically and anatomically, to perceive affective and social touch. However, their contribution to sociability has not been resolved yet. Our observations revealed that C-LTMR fun ...[more]

PMID: 35767616

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Project description:The rewarding sensation of touch in affiliative interactions is hypothesized to be underpinned by a specialized system of nerve fibers called C-Tactile afferents (CTs), which respond optimally to slowly moving, gentle touch, typical of a caress. However, empirical evidence to support the theory that CTs encode socially relevant, rewarding tactile information in humans is currently limited. While in healthy participants, touch applied at CT optimal velocities (1-10cm/sec) is reliably rated as subjectively pleasant, neuronopathy patients lacking large myelinated afferents, but with intact C-fibres, report that the conscious sensation elicited by stimulation of CTs is rather vague. Given this weak perceptual impact the value of self-report measures for assessing the specific affective value of CT activating touch appears limited. Therefore, we combined subjective ratings of touch pleasantness with implicit measures of affective state (facial electromyography) and autonomic arousal (heart rate) to determine whether CT activation carries a positive affective value. We recorded the activity of two key emotion-relevant facial muscle sites (zygomaticus major-smile muscle, positive affect & corrugator supercilii-frown muscle, negative affect) while participants evaluated the pleasantness of experimenter administered stroking touch, delivered using a soft brush, at two velocities (CT optimal 3cm/sec & CT non-optimal 30cm/sec), on two skin sites (CT innervated forearm & non-CT innervated palm). On both sites, 3cm/sec stroking touch was rated as more pleasant and produced greater heart rate deceleration than 30cm/sec stimulation. However, neither self-report ratings nor heart rate responses discriminated stimulation on the CT innervated arm from stroking of the non-CT innervated palm. In contrast, significantly greater activation of the zygomaticus major (smiling muscle) was seen specifically to CT optimal, 3cm/sec, stroking on the forearm in comparison to all other stimuli. These results offer the first empirical evidence in humans that tactile stimulation that optimally activates CTs carries a positive affective valence that can be measured implicitly.

Project description:This study investigated whether communication via mediated hand pressure during a remotely shared experience (watching an amusing video) can (1) enhance recovery from sadness, (2) enhance the affective quality of the experience, and (3) increase trust towards the communication partner. Thereto participants first watched a sad movie clip to elicit sadness, followed by a funny one to stimulate recovery from sadness. While watching the funny clip they signaled a hypothetical fellow participant every time they felt amused. In the experimental condition the participants responded by pressing a hand-held two-way mediated touch device (a Frebble), which also provided haptic feedback via simulated hand squeezes. In the control condition they responded by pressing a button and they received abstract visual feedback. Objective (heart rate, galvanic skin conductance, number and duration of joystick or Frebble presses) and subjective (questionnaires) data were collected to assess the emotional reactions of the participants. The subjective measurements confirmed that the sad movie successfully induced sadness while the funny movie indeed evoked more positive feelings. Although their ranking agreed with the subjective measurements, the physiological measurements confirmed this conclusion only for the funny movie. The results show that recovery from movie induced sadness, the affective experience of the amusing movie, and trust towards the communication partner did not differ between both experimental conditions. Hence, feedback via mediated hand touching did not enhance either of these factors compared to visual feedback. Further analysis of the data showed that participants scoring low on Extraversion (i.e., persons that are more introvert) or low on Touch Receptivity (i.e., persons who do not like to be touched by others) felt better understood by their communication partner when receiving mediated touch feedback instead of visual feedback, while the opposite was found for participants scoring high on these factors. The implications of these results for further research are discussed, and some suggestions for follow-up experiments are presented.

Dataset Information

The impact of C-tactile low-threshold mechanoreceptors on affective touch and social interactions in mice.

Publications

The impact of C-tactile low-threshold mechanoreceptors on affective touch and social interactions in mice.

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