Håkan Olausson

Unmyelinated tactile afferents signal touch and project to insular cortex.

There is dual tactile innervation of the human hairy skin: in addition to fast-conducting myelinated afferent fibers, there is a system of slow-conducting unmyelinated (C) afferents that respond to light touch. In a unique patient lacking large myelinated afferents, we found that activation of C tactile (CT) afferents produced a faint sensation of pleasant touch. Functional magnetic resonance imaging (fMRI) analysis during CT stimulation showed activation of the insular region, but not of somatosensory areas S1 and S2. These findings identify CT as a system for limbic touch that may underlie emotional, hormonal and affiliative responses to caress-like, skin-to-skin contact between individuals.

Coding of pleasant touch by unmyelinated afferents in humans

Pleasant touch sensations may begin with neural coding in the periphery by specific afferents. We found that during soft brush stroking, low-threshold unmyelinated mechanoreceptors (C-tactile), but not myelinated afferents, responded most vigorously at intermediate brushing velocities (1−10 cm s−1), which were perceived by subjects as being the most pleasant. Our results indicate that C-tactile afferents constitute a privileged peripheral pathway for pleasant tactile stimulation that is likely to signal affiliative social body contact.

The neurophysiology of unmyelinated tactile afferents.

CT (C tactile) afferents are a distinct type of unmyelinated, low-threshold mechanoreceptive units existing in the hairy but not glabrous skin of humans and other mammals. Evidence from patients lacking myelinated tactile afferents indicates that signaling in these fibers activate the insular cortex. Since this system is poor in encoding discriminative aspects of touch, but well-suited to encoding slow, gentle touch, CT fibers in hairy skin may be part of a system for processing pleasant and socially relevant aspects of touch. CT fiber activation may also have a role in pain inhibition. This review outlines the growing evidence for unique properties and pathways of CT afferents.

Touching and feeling: differences in pleasant touch processing between glabrous and hairy skin in humans

Previous functional magnetic resonance imaging studies in two rare patients, together with microneurography and psychophysical observations in healthy subjects, have demonstrated a system of mechanosensitive C‐fiber tactile (CT) afferents sensitive to slowly moving stimuli. They project to the posterior insular cortex and signal pleasant aspects of touch. Importantly, CTs have not been found in the glabrous skin of the hand, yet it is commonly observed that glabrous skin touch is also perceived as pleasant. Here we asked if the brain processing of pleasant touch differs between hairy and glabrous skin by stroking the forearm and glabrous skin of the hand during positron emission tomography. The data showed that, when contrasting slow brush stroking on the forearm with slow brush stroking on the palm, there were significant activations of the posterior insular cortex and mid‐anterior orbitofrontal cortex. The opposite contrast showed a significant activation of the somatosensory cortices. Although concurrent psychophysical ratings showed no differences in intensity or pleasantness ratings, a subsequent touch questionnaire in which subjects used a newly developed ‘touch perception task’ showed significant difference for the two body sites. Emotional descriptors received higher ratings on the forearm and sensory descriptors were rated more highly on the palm. The present findings are consistent with the hypothesis that pleasant touch from hairy skin, mediated by CT afferents, is processed in the limbic‐related cortex and represents an innate non‐learned process. In contrast, pleasant touch from glabrous skin, mediated by A‐beta afferents, is processed in the somatosensory cortex and represents an analytical process dependent on previous tactile experiences.

Functional role of unmyelinated tactile afferents in human hairy skin: sympathetic response and perceptual localization

In addition to A-beta fibres the human hairy skin has unmyelinated (C) fibres responsive to light touch. Previous functional magnetic resonance imaging (fMRI) studies in a subject with a neuronopathy who specifically lacks A-beta afferents indicated that tactile C afferents (CT) activate insular cortex, whereas no response was seen in somatosensory areas 1 and 2. Psychophysical tests suggested that CT afferents give rise to an inconsistent perception of weak and pleasant touch. By examining two neuronopathy subjects as well as control subjects we have now demonstrated that CT stimulation can elicit a sympathetic skin response. Further, the neuronopathy subjects’ ability to localize stimuli which activate CT afferents was very poor but above chance level. The findings support the interpretation that the CT system is well suited to underpin affective rather than discriminative functions of tactile sensations.

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.

Development of brain mechanisms for processing affective touch

Affective tactile stimulation plays a key role in the maturation of neural circuits, but the development of brain mechanisms processing touch is poorly understood. We therefore used functional magnetic resonance imaging (fMRI) to study brain responses to soft brush stroking of both glabrous (palm) and hairy (forearm) skin in healthy children (5–13 years), adolescents (14–17 years), and adults (25–35 years). Adult-defined regions-of-interests in the primary somatosensory cortex (SI), secondary somatosensory cortex (SII), insular cortex and right posterior superior temporal sulcus (pSTS) were significantly and similarly activated in all age groups. Whole-brain analyses revealed that responses in the ipsilateral SII were positively correlated with age in both genders, and that responses in bilateral regions near the pSTS correlated significantly and strongly with age in females but not in males. These results suggest that brain mechanisms associated with both sensory-discriminative and affective-motivational aspects of touch are largely established in school-aged children, and that there is a general continuing maturation of SII and a female-specific increase in pSTS sensitivity with age. Our work establishes a groundwork for future comparative studies of tactile processing in developmental disorders characterized by disrupted social perception such as autism.

Tactile directional sensibility and diabetic neuropathy.

Five different procedures used to diagnose neuropathy were compared in a “blind” study with diabetic patients. The aim was to evaluate tests of tactile directional sensibility. Three matched groups were examined, two groups with type I diabetes, either with or without suspected neuropathy, and one of healthy controls. Testing consisted of: (1) examination by a specialist in neurology, (2) electrophysiologic measurement of nerve conduction velocity and determination of cool sensitivity, and (3) determination of directional sensibility in two stages, with categorical and quantitative techniques. Abnormal test results were obtained for both groups of diabetic patients. Quantitatively measured directional sensibility had the highest sensitivity (89%) and specificity (85%) when calculated for patients who had received a diagnosis of neuropathy from the neurologist, despite one case of abnormal directional sensibility among the healthy controls. Conduction velocity testing was almost comparably sensitive (80%) and cool sensitivity, comparably specific (85%) when calculated in the same manner.

Tactile direction discrimination and vibration detection in diabetic neuropathy

Löken LS, Lundblad LC, Elam M, Olausson HW. Tactile direction discrimination and vibration detection in diabetic neuropathy. Acta Neurol Scand: 2010: 121: 302–308.
© 2009 The Authors Journal compilation