Helena Backlund Wasling

Human C-Tactile Afferents Are Tuned to the Temperature of a Skin-Stroking Caress

Human C-tactile (CT) afferents respond vigorously to gentle skin stroking and have gained attention for their importance in social touch. Pharmacogenetic activation of the mouse CT equivalent has positively reinforcing, anxiolytic effects, suggesting a role in grooming and affiliative behavior. We recorded from single CT axons in human participants, using the technique of microneurography, and stimulated a units receptive field using a novel, computer-controlled moving probe, which stroked the skin of the forearm over five velocities (0.3, 1, 3, 10, and 30 cm s−1) at three temperatures (cool, 18°C; neutral, 32°C; warm, 42°C). We show that CTs are unique among mechanoreceptive afferents: they discharged preferentially to slowly moving stimuli at a neutral (typical skin) temperature, rather than at the cooler or warmer stimulus temperatures. In contrast, myelinated hair mechanoreceptive afferents proportionally increased their firing frequency with stroking velocity and showed no temperature modulation. Furthermore, the CT firing frequency correlated with hedonic ratings to the same mechano-thermal stimulus only at the neutral stimulus temperature, where the stimuli were felt as pleasant at higher firing rates. We conclude that CT afferents are tuned to respond to tactile stimuli with the specific characteristics of a gentle caress delivered at typical skin temperature. This provides a peripheral mechanism for signaling pleasant skin-to-skin contact in humans, which promotes interpersonal touch and affiliative behavior.

Touch perceptions across skin sites: differences between sensitivity, direction discrimination and pleasantness

Human skin is innervated with different tactile afferents, which are found at varying densities over the body. We investigate how the relationships between tactile pleasantness, sensitivity and discrimination differ across the skin. Tactile pleasantness was assessed by stroking a soft brush over the skin, using five velocities (0.3, 1, 3, 10, 30 cm s−1), known to differentiate hedonic touch, and pleasantness ratings were gained. The ratings velocity-profile is known to correlate with firing in unmyelinated C-tactile (CT) afferents. Tactile sensitivity thresholds were determined using monofilament force detection and the tactile discrimination level was obtained in the direction discrimination of a moving probe; both tasks readily activate myelinated touch receptors. Perceptions were measured over five skin sites: forehead, arm, palm, thigh and shin. The assessment of tactile pleasantness over the skin resulted in a preference for the middle velocities (1–10 cm s−1), where higher ratings were gained compared to the slowest and fastest velocities. This preference in tactile pleasantness was found across all the skin sites, apart from at the palm, where no decrease in pleasantness for the faster stroking velocities was seen. We find that tactile sensitivity and discrimination vary across the skin, where the forehead and palm show increased acuity. Tactile sensitivity and discrimination levels also correlated significantly, although the tactile acuity did not relate to the perceived pleasantness of touch. Tactile pleasantness varied in a subtle way across skin sites, where the middle velocities were always rated as the most pleasant, but the ratings at hairy skin sites were more receptive to changes in stroking velocity. We postulate that although the mechanoreceptive afferent physiology may be different over the skin, the perception of pleasant touch can be interpreted using all of the available incoming somatosensory information in combination with central processing.

Roughness Encoding in Human and Biomimetic Artificial Touch: Spatiotemporal Frequency Modulation and Structural Anisotropy of Fingerprints

The influence of fingerprints and their curvature in tactile sensing performance is investigated by comparative analysis of different design parameters in a biomimetic artificial fingertip, having straight or curved fingerprints. The strength in the encoding of the principal spatial period of ridged tactile stimuli (gratings) is evaluated by indenting and sliding the surfaces at controlled normal contact force and tangential sliding velocity, as a function of fingertip rotation along the indentation axis. Curved fingerprints guaranteed higher directional isotropy than straight fingerprints in the encoding of the principal frequency resulting from the ratio between the sliding velocity and the spatial periodicity of the grating. In parallel, human microneurography experiments were performed and a selection of results is included in this work in order to support the significance of the biorobotic study with the artificial tactile system.

Quantifying the sensory and emotional perception of touch: differences between glabrous and hairy skin.

The perception of touch is complex and there has been a lack of ways to describe the full tactile experience quantitatively. Guest et al. (2011) developed a Touch Perception Task (TPT) in order to capture such experiences, and here we used the TPT to examine differences in sensory and emotional aspects of touch at different skin sites. We compared touch on three skin sites: the hairy arm and cheek, and the glabrous palm. The hairy skin contains C-tactile (CT) afferents, which play a role in affective touch, whereas glabrous skin does not contain CT afferents and is involved in more discriminative touch. In healthy volunteers, three different materials (soft brush, sandpaper, fur) were stroked across these skin sites during self-touch or experimenter-applied touch. After each stimulus, participants rated the tactile experience using descriptors in the TPT. Sensory and emotional descriptors were analyzed using factor analyses. Five sensory factors were found: Texture, Pile, Moisture, Heat/Sharp and Cold/Slip, and three emotional factors: Positive Affect, Arousal, and Negative Affect. Significant differences were found in the use of descriptors in touch to hairy vs. glabrous skin: this was most evident in touch on forearm skin, which produced higher emotional content. The touch from another was also judged as more emotionally positive then self-touch, and participants readily discriminated between the materials on all factors. The TPT successfully probed sensory and emotional percepts of the touch experience, which aided in identifying skin where emotional touch was more pertinent. It also highlights the potentially important role for CTs in the affective processing of inter-personal touch, in combination with higher-order influences, such as through cultural belonging and previous experiences.

Unmyelinated tactile cutaneous nerves signal erotic sensations.

INTRODUCTIONnIntrapersonal touch is a powerful tool for communicating emotions and can among many things evoke feelings of eroticism and sexual arousal. The peripheral neural mechanisms of erotic touch signaling have been less studied. C tactile afferents (unmyelinated low-threshold mechanoreceptors), known to underpin pleasant aspects of touch processing, have been posited to play an important role.nnnMETHODnIn two studies, we investigated the relationship between C tactile activation and the perception of erotic and pleasant touch, using tactile brushing stimulation. In total, 66 healthy subjects (37 women, age range 19-51 years) were examined. In study 1 (n = 20), five different stroking velocities were applied to the forearm and the inner thigh. The participants answered questions about partnership, mood, and touch. In study 2 (n = 46), the same five stroking velocities were applied to the forearm. The participants answered questions about partnership, touch, and sexuality.nnnRESULTSnBoth touch eroticism and pleasantness were rated significantly higher for C tactile optimal velocities compared with suboptimal velocities. No difference was found between the ratings of the thigh and the forearm. The velocity-dependent rating curves of pleasantness, intensity, and eroticism differed from each other. Pleasantness was best explained by a quadratic fit, intensity by a linear fit, and eroticism by both. A linear transformation of pleasantness and intensity predicted the observed eroticism ratings reliably. Eroticism ratings were negatively correlated with length of relationship.nnnCONCLUSIONnTouch was rated most erotic when perceived as pleasant and weak. In human hairy skin, perception of pleasantness is correlated with the firing rate of C tactile afferents, and perception of intensity is correlated with the firing rate of Aβ afferents. Accordingly, eroticism may be perceived most readily for touch stimuli that induce high activity in C tactile fibers and low activity in Aβ fibers.

Tactile directional sensitivity and postural control

People are good at telling the direction of a moving tactile stimulus and this capacity provides a sensitive clinical test of somatosensory disturbances. Tactile directional sensitivity depends on two different kinds of somatosensory information, i.e. spatiotemporal information and information about friction-induced changes in skin stretch. The objective of this study was to compare the relative contribution to postural control of these two types of information for both glabrous and hairy skin. Postural sway amplitudes and sway paths were recorded, with or without access to tactile and/or visual stabilizing stimuli. Subjects were standing on two types of surface, either solid metal or 50xa0mm foam plastic. Two types of stimulus were used to generate sway-related tactile information. One was a thin air-stream that was used to assess the contribution by spatiotemporal information, and the second was a narrow steel rod that was glued to the skin to assess the contribution by skin-stretch information. The stimuli were applied to the hairy skin of the forearm and to the glabrous skin of the fingertip. In addition, we studied the ability to tell the direction of movement of an air-stream stimulus on glabrous and hairy skin. The air-stream caused significant sway reductions when applied to glabrous, but not hairy skin. The weak effect on hairy skin reflected the perceptually poor directional sensitivity for the air-stream stimulus in this cutaneous area. In contrast, the glued rod reduced sway when applied to both glabrous and hairy skin reflecting the tactile afferents’ high sensitivity to skin stretch in these areas. Both types of tactile stimulus reduced sway amplitudes more than sway paths for both hairy and glabrous skin. The visual cue, on the other hand, tended to reduce sway paths more than amplitudes. The two types of tactile receptive surface seem to influence postural control in the same manner, despite anatomical and physiological differences. The results invite speculation that patients with poor directional sensitivity might have reduced postural stability compared with healthy individuals.

Gentle touch perception across the lifespan.

Pleasant, affective touch provides various health benefits, including stress and depression relief. There is a dichotomy between mechanoreceptive afferents that predominantly signal discriminative (myelinated A-beta) and affective (unmyelinated C-tactile) aspects of touch. It is well documented that discriminative abilities of touch decline with age. However, a thorough investigation of how the pleasant aspects of touch develop with age has not been previously attempted. Here, we investigated the relationship between age and psychophysical ratings in response to gentle stroking touch. One hundred twenty participants (60 males, 60 females) ages 13-82 years were presented with C-tactile optimal and suboptimal stroking velocities, and rated pleasantness and intensity. Moreover, to examine the specificity of age effects on touch perception, we used olfactory stimuli as a cross-sensory comparison. For all ages, we found that C-tactile optimal stimuli were rated significantly more pleasant than C-tactile suboptimal stimuli. Although, both touch and olfactory intensity ratings were negatively correlated with age, a positive correlation between pleasantness ratings of touch (but not olfactory stimuli) and age was found. We conclude that the affective, but not the discriminative, aspects of touch are enhanced with increasing age. The increase of pleasantness of all touch stimuli in late adulthood is discussed in relation to cognitive modulations.

Cortical processing of tactile direction discrimination based on spatiotemporal cues in man

Tactile direction discrimination (TDD), the ability to determine the direction of an objects movement across the skin, is used clinically to detect and quantify tactile dysfunction. We have previously identified a cortical network for TDD based on skin stretch information that includes the second somatosensory, anterior insular and dorsolateral prefrontal cortices. In the present study we investigated cortical processing of TDD based on spatiotemporal cues. Sixteen healthy subjects (8 females; mean age, 25.5 years; range, 23-32 years) were stimulated with a low-friction, spatiotemporal rolling wheel on the right thigh during functional magnetic resonance imaging (fMRI). The subjects were instructed to indicate the distal or proximal rolling direction of the stimulus. The fMRI contrast between rolling wheel stimulation and rest showed activations in several areas which included the left (contralateral) primary somatosensory, bilateral second somatosensory, bilateral anterior insular, and bilateral dorsolateral prefrontal cortices. We conclude that, spatiotemporal TDD is processed in a largely similar distributed cortical network as skin stretch TDD. Further, spatiotemporal TDD activated primary somatosensory cortex whereas a role for this area in processing of skin stretch TDD has not been demonstrated.

Cortical processing of lateral skin stretch stimulation in humans

Direction discrimination of a moving tactile stimulus requires intact dorsal columns and provides a sensitive clinical test of somatosensory dysfunction. Cortical mechanisms are poorly understood. We have applied tangential skin pulls to the right lower leg during functional magnetic resonance imaging. Healthy subjects judged the direction of the skin pulls (task experiment, nxa0=xa07) or received skin pulls passively (no task experiment, nxa0=xa08). Second somatosensory cortex (S2) was activated in the task as well as no task experiment, and there was no significant difference in cortical activation between the two experiments. Within S2 nearly all subjects had prominent activations in the caudal and superficial part, i.e., in the opercular parietal (OP) area 1. S1 was activated in only one of the subjects. Thus, S2 and especially OP 1 seems to be important for processing of lateral skin stretch stimulation. The finding suggests that a lesion of this area might cause a disturbance in tactile direction discrimination which should be relevant for clinical testing.

Affective and non-affective touch evoke differential brain responses in 2-month-old infants

ABSTRACT Caressing touch is an effective way to communicate emotions and to create social bonds. It is also one of the key mediators of early parental bonding. The caresses are generally thought to represent a social form of touching and indeed, slow, gentle brushing is encoded in specialized peripheral nerve fibers, the C‐tactile (CT) afferents. In adults, areas such as the posterior insula and superior temporal sulcus are activated by affective, slow stroking touch but not by fast stroking stimulation. However, whether these areas are activated in infants, after social tactile stimulation, is unknown. In this study, we compared the total hemoglobin responses measured with diffuse optical tomography (DOT) in the left hemisphere following slow and fast stroking touch stimulation in 16 2‐month‐old infants. We compared slow stroking (optimal CT afferent stimulation) to fast stroking (non‐optimal CT stimulation). Activated regions were delineated using two methods: one based on contrast between the two conditions, and the other based on voxel‐based statistical significance of the difference between the two conditions. The first method showed a single activation cluster in the temporal cortex with center of gravity in the middle temporal gyrus where the total hemoglobin increased after the slow stroking relative to the fast stroking (p = 0.04 uncorrected). The second method revealed a cluster in the insula with an increase in total hemoglobin in the insular cortex in response to slow stroking relative to fast stroking (p = 0.0005 uncorrected; p = 0.04 corrected for multiple comparisons). These activation clusters encompass areas that are involved in processing of affective, slow stroking touch in the adult brain. We conclude that the infant brain shows a pronounced and adult‐like response to slow stroking touch compared to fast stroking touch in the insular cortex but the expected response in the primary somatosensory cortex was not found at this age. The results imply that emotionally valent touch is encoded in the brain in adult‐like manner already soon after birth and this suggests a potential for involvement of touch in bonding with the caretaker.