The impact of C-tactile low-threshold mechanoreceptors on affective touch and social interactions in mice.
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ABSTRACT:
SUBMITTER: Huzard D
PROVIDER: S-EPMC9242590 | biostudies-literature |
REPOSITORIES: biostudies-literature
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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.
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Project description:Mechanical pain contributes to the morbidity associated with inflammation and trauma, but primary sensory neurons that convey the sensation of acute and persistent mechanical pain have not been identified. Dorsal root ganglion (DRG) neurons transmit sensory information to the spinal cord using the excitatory transmitter glutamate, a process that depends on glutamate transport into synaptic vesicles for regulated exocytotic release. Here we report that a small subset of cells in the DRG expresses the low abundance vesicular glutamate transporter VGLUT3 (also known as SLC17A8). In the dorsal horn of the spinal cord, these afferents project to lamina I and the innermost layer of lamina II, which has previously been implicated in persistent pain caused by injury. Because the different VGLUT isoforms generally have a non-redundant pattern of expression, we used Vglut3 knockout mice to assess the role of VGLUT3(+) primary afferents in the behavioural response to somatosensory input. The loss of VGLUT3 specifically impairs mechanical pain sensation, and in particular the mechanical hypersensitivity to normally innocuous stimuli that accompanies inflammation, nerve injury and trauma. Direct recording from VGLUT3(+) neurons in the DRG further identifies them as a poorly understood population of unmyelinated, low threshold mechanoreceptors (C-LTMRs). The analysis of Vglut3(-/-) mice now indicates a critical role for C-LTMRs in the mechanical hypersensitivity caused by injury.
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Project description:Innocuous mechanical stimuli acting on the skin are detected by sensory neurons, known as low-threshold mechanoreceptors (LTMRs). LTMRs are classified based on their response properties, action potential conduction velocity, rate of adaptation to static indentation of the skin, and terminal anatomy. Here, we report organizational properties of the cutaneous and central axonal projections of the five principal hairy skin LTMR subtypes. We find that axons of neurons within a particular LTMR class are largely nonoverlapping with respect to their cutaneous end organs (e.g., hair follicles), with Aβ rapidly adapting-LTMRs being the sole exception. Individual neurons of each LTMR class are mostly nonoverlapping with respect to their associated hair follicles, with the notable exception of C-LTMRs, which exhibit multiple branches that redundantly innervate individual hair follicles. In the spinal cord, LTMR central projections exhibit rostrocaudal elongation and mediolateral compression, compared with their cutaneous innervation patterns, and these central projections also exhibit a fine degree of homotypic topographic adjacency. These findings thus reveal homotypic tiling of LTMR subtype axonal projections in hairy skin and a remarkable degree of spatial precision of spinal cord axonal termination patterns, suggesting a somatotopically precise tactile encoding capability of the mechanosensory dorsal horn.
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Project description:The mammalian need for social proximity, attachment and belonging may have an adaptive and evolutionary value in terms of survival and reproductive success. Consequently, ostracism may induce strong negative feelings of social exclusion. Recent studies suggest that slow, affective touch, which is mediated by a separate, specific C tactile neurophysiological system than faster, neutral touch, modulates the perception of physical pain. However, it remains unknown whether slow, affective touch, can also reduce feelings of social exclusion, a form of social pain. Here, we employed a social exclusion paradigm, namely the Cyberball task (N = 84), to examine whether the administration of slow, affective touch may reduce the negative feelings of ostracism induced by the social exclusion manipulations of the Cyberball task. As predicted, the provision of slow-affective, as compared to fast-neutral, touch led to a specific decrease in feelings of social exclusion, beyond general mood effects. These findings point to the soothing function of slow, affective touch, particularly in the context of social separation or rejection, and suggest a specific relation between affective touch and social bonding.
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Project description:Another person's caress is one of the most powerful of all emotional social signals. How much the primary somatosensory cortices (SIs) participate in processing the pleasantness of such social touch remains unclear. Although ample empirical evidence supports the role of the insula in affective processing of touch, here we argue that SI might be more involved in affective processing than previously thought by showing that the response in SI to a sensual caress is modified by the perceived sex of the caresser. In a functional MRI study, we manipulated the perceived affective quality of a caress independently of the sensory properties at the skin: heterosexual males believed they were sensually caressed by either a man or woman, although the caress was in fact invariantly delivered by a female blind to condition type. Independent analyses showed that SI encoded, and was modulated by, the visual sex of the caress, and that this effect is unlikely to originate from the insula. This suggests that current models may underestimate the role played by SI in the affective processing of social touch.
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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.
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Project description:The roles of Aβ low-threshold mechanoreceptors (LTMRs) in transmitting mechanical hyperalgesia and in alleviating chronic pain have been of great interest but remain contentious. Here we utilized intersectional genetic tools, optogenetics, and high-speed imaging to specifically examine functions of SplitCre labeled mouse Aβ-LTMRs in this regard. Genetic ablation of SplitCre-Aβ-LTMRs increased mechanical nociception but not thermosensation in both acute and chronic inflammatory pain conditions, indicating a modality-specific role in gating mechanical nociception. Local optogenetic activation of SplitCre-Aβ-LTMRs triggered nociception after tissue inflammation, whereas their broad activation at the dorsal column still alleviated mechanical hypersensitivity of chronic inflammation. Taking all data into consideration, we propose a model, in which Aβ-LTMRs play distinctive local and global roles in transmitting or alleviating mechanical hyperalgesia of chronic pain, respectively. Our model suggests a strategy of global activation plus local inhibition of Aβ-LTMRs for treating mechanical hyperalgesia.
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Project description:The roles of Aβ low-threshold mechanoreceptors (LTMRs) in transmitting mechanical hyperalgesia and in alleviating chronic pain have been of great interest but remain contentious. Here we utilized intersectional genetic tools, optogenetics, and high-speed imaging to specifically examine functions of Split Cre labeled Aβ-LTMRs in this regard. Genetic ablation of Split Cre - Aβ-LTMRs increased mechanical pain but not thermosensation in both acute and chronic inflammatory pain conditions, indicating their modality-specific role in gating mechanical pain transmission. Local optogenetic activation of Split Cre -Aβ-LTMRs triggered nociception after tissue inflammation, whereas their broad activation at the dorsal column still alleviated mechanical hypersensitivity of chronic inflammation. Taking all data into consideration, we propose a new model, in which Aβ-LTMRs play distinctive local and global roles in transmitting and alleviating mechanical hyperalgesia of chronic pain, respectively. Our model suggests a new strategy of global activation plus local inhibition of Aβ-LTMRs for treating mechanical hyperalgesia.
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Project description:Previous research points to two major hypotheses regarding the mechanisms by which touch can be experienced as erotogenic. The first concerns the body part to which touch is applied (erogenous zones) and the second the modality of touch (sensual touch optimal in activating C Tactile afferents). In this study, we explored for the first time the relation between those two mechanisms in actual and imagined social touch. In a first experiment, we randomly assigned "Giver" and "Receiver" roles within 19 romantic couples (20 females, 18 males, age 32.34 ± 8.71SD years) and asked the "Giver" to apply CT-optimal (3 cm/s) vs. CT-suboptimal (18 cm/s) touch on an erogenous (neck) vs. non-erogenous zone (forehead) of their partner. We then obtained ratings of pleasantness and sexual arousal from both "Receivers" and "Givers". In a second experiment, 32 healthy females (age 25.16 ± 5.91SD years) were asked to imagine CT-optimal vs. CT-suboptimal stimulation (stroking vs. patting) and velocity (3 cm/s vs. 18 cm/s) on different erogenous vs. non-erogenous zones and rate pleasantness. While both erogenous body part and CT-optimal, sensual touch were found to increase pleasant and erotic sensations, the results showed a lack of an interaction. Furthermore, pleasantness was induced by mere imagination of touch without any tactile stimulation, and touch that was sexually arousing for the receiver was rated as more sexually arousing for the giver as well, pointing to top-down, learned expectations of sensory pleasure and erogeneity. Taken together, these studies provide the first direct evidence that while both the body location to which touch is applied and the mode of touch contribute to pleasant and erotic sensations, these two factors appear to mediate subjective pleasantness and erogeneity by, at least partly, independent mechanisms.
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Project description:The sense of touch develops early in life and becomes a determinant aspect of our personal narratives, providing crucial information about the world around us and playing a prominent role in affective and social interactions. In this study we aimed to explore whether individual differences in touch experiences across the lifespan are related to adult attachment styles and to perceived touch deprivation. For this we first developed an instrument, namely the Tactile Biography, to quantify individual differences in affective touch experiences throughout life. Secondly, we performed a set of regressions models and a mediation analysis to investigate the role of attachment in relation to both the tactile history and perceived touch deprivation. We found that experiences of affective touch during childhood and adolescence seem to be closely associated with adult attachment styles and adult social touch experiences. Avoidant attachment appears to serve as a mediator in the relationship between earlier (childhood/adolescent) and later (adult) affective touch experiences, as well as between earlier affective touch experiences and perceived touch deprivation. These findings offer further support to existing literature, providing novel insights for the fields of social affective touch and attachment research.
| S-EPMC7592771 | biostudies-literature