Håkan Olausson

The skin as a social organ

In general, social neuroscience research tends to focus on visual and auditory channels as routes for social information. However, because the skin is the site of events and processes crucial to the way we think about, feel about, and interact with one another, touch can mediate social perceptions in various ways. This review situates cutaneous perception within a social neuroscience framework by discussing evidence for considering touch (and to some extent pain) as a channel for social information. Social information conveys features of individuals or their interactions that have potential bearing on future interactions, and attendant mental and emotional states. Here, we discuss evidence for an affective dimension of touch and explore its wider implications for the exchange of social information. We consider three important roles for this affective dimension of the cutaneous senses in the transmission and processing of social information: first, through affiliative behavior and communication; second, via affective processing in skin–brain pathways; and third, as a basis for intersubjective representation.

Somatotopic organization of gentle touch processing in the posterior insular cortex.

A network of thin (C and Aδ) afferents relays various signals related to the physiological condition of the body, including sensations of gentle touch, pain, and temperature changes. Such afferents project to the insular cortex, where a somatotopic organization of responses to noxious and cooling stimuli was recently observed. To explore the possibility of a corresponding body-map topography in relation to gentle touch mediated through C tactile (CT) fibers, we applied soft brush stimuli to the right forearm and thigh of a patient (GL) lacking Aβ afferents, and six healthy subjects during functional magnetic resonance imaging (fMRI). For improved fMRI analysis, we used a highly sensitive multivariate voxel clustering approach. A somatotopic organization of the left (contralateral) posterior insular cortex was consistently demonstrated in all subjects, including GL, with forearm projecting anterior to thigh stimulation. Also, despite denying any sense of touch in daily life, GL correctly localized 97% of the stimuli to the forearm or thigh in a forced-choice paradigm. The consistency in activation patterns across GL and the healthy subjects suggests that the identified organization reflects the central projection of CT fibers. Moreover, substantial similarities of the presently observed insular activation with that described for noxious and cooling stimuli solidify the hypothesized sensory-affective role of the CT system in the maintenance of physical well-being as part of a thin-afferent homeostatic network.

A system of unmyelinated afferents for innocuous mechanoreception in the human skin

It is generally held that tactile mechanisms in the human skin are served by fast-conducting myelinated nerve fibres, whereas touch-sensitive afferents with unmyelinated axons are lacking in man, in contrast to other mammals. In the present study we found evidence that sensitive mechanoreceptive afferents with unmyelinated fibres are quite common and widespread in the hairy skin of human subjects. Their biological role remains an enigma which might attract more attention now that their existence in man has been demonstrated.

Receptive field characteristics of tactile units with myelinated afferents in hairy skin of human subjects.

1. Impulses in single nerve fibres from the lateral antebrachial cutaneous nerve were recorded using the microneurography technique in human subjects. 2. In a sample of fifty‐five mechanoreceptive units with fast‐conducting nerve fibres, five types were identified, i.e. SAI (slowly adapting type I, Merkel), SAII (slowly adapting type II, Ruffini), hair units, field units and Pacinian‐type units. The latter three unit types were all rapidly adapting. 3. The detailed structure of thirty‐five receptive fields of SAI, SAII, hair and field units was explored with a method which was objective and independent of the experimenters skill and experience. A lightweight probe was used to scan the receptive field area in a series of tracks 0.23 mm apart while single‐unit activity was recorded. 4. SAI fields were small and composed of two to four well‐separated high‐sensitivity spots and often, in addition, one minor spot of lower sensitivity. SAII units typically fired spontaneously at a low and regular rate. Most fields consisted of one single spot of high sensitivity with diffuse borders. The hair units innervated ten to thirty‐three (or more) hairs, which were evenly distributed over a large area. The field units were characterized by a number of small and closely packed high‐sensitivity spots with diffuse borders. A conservative estimate indicated eleven spots per unit. 5. The findings indicate that the sheet of mechanoreceptors on the skin of the forearm is distinctly different from that on the dorsum of the hand and in the face. It seems reasonable to assume that the former is more representative for the hairy skin covering the main parts of the body.

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.

Unmyelinated tactile afferents have opposite effects on insular and somatosensory cortical processing

A previous functional magnetic resonance imaging (fMRI) study of an A-beta deafferented subject (GL) showed that stimulation of tactile C afferents (CT) activates insular cortex whereas no activation was seen in somatosensory cortices. Psychophysical studies suggested that CT afferents contribute to affective but not to discriminative aspects of tactile stimulation. We have now examined cortical processing following CT stimulation in a second similarly deafferented subject (IW), as well as revisited the data from GL. The results in IW showed similar activation of posterior insular cortex following CT stimulation as in GL and so strengthen the view that CT afferents underpin emotional aspects of touch. In addition, CT stimulation evoked significant fMRI deactivation in somatosensory cortex in both subjects supporting the notion that CT is not a system for discriminative touch.

Tactile directional sensibility: peripheral neural mechanisms in man

Tactile directional sensibility, i.e. the ability to tell the direction of an objects motion across the skin, is an easily observed sensory function that is highly sensitive to disturbances of the somatosensory system. Based on previous psychophysical experiments on healthy subjects it was concluded that directional sensibility depends on two kinds of information from cutaneous mechanoreceptors; spatio-temporal information and information about friction-induced changes in skin stretch. In the present study responses to similar probe movements as in the psychophysical experiments were recorded from human single mechanoreceptors in the forearm skin. All slowly adapting type 2 (SA2) units were spontaneously active, and with increasing force of friction their discharge rates were modified by probe movements at increasing distances from the Ruffini end-organ, reflecting the high stretch-sensitivity of these units. Slowly adapting type 1 (SA1) and field units responded to the moving probe within well-defined skin areas directly overlying the individual receptor terminals, and compared to the SA2 units their response properties were less dependent on the force of friction. The results suggest that SA1 and field units have the capacity to signal spatio-temporal information, whereas a population of SA2 units have the capacity to signal direction-specific information about changes in lateral skin stretch.

Feeling good: on the role of C fiber mediated touch in interoception

The human skin is innervated by a network of thin, slow-conducting afferent (C and Aδ) fibers, transmitting a diverse range of information. Classically, these fibers are described as thermo-, noci- or chemoreceptive, whereas mechanoreception is attributed exclusively to thick, fast-conducting (Aβ) afferents. A growing body of evidence, however, supports the notion that C tactile afferents comprise a second anatomically and functionally distinct system signaling touch in humans. This review discusses established as well as recent findings which highlight fundamental differences in peripheral and central information coding and processing between Aβ and C mechanoreception. We conclude that from the skin through the brain, C touch shares more characteristics with interoceptive modalities (e.g. pain, temperature, and itch) than exteroceptive Aβ touch, vision or hearing. In this light, we discuss the motivational-affective role of C touch as an integral part of a thin-fiber afferent homeostatic network for the maintenance of physical and social well-being.

Placebo improves pleasure and pain through opposite modulation of sensory processing

Significance Placebo effects illustrate the power of the human brain; simply expecting an improvement can alter pain processing and produce analgesia. We induced placebo improvement of both negative and positive feelings (painful and pleasant touch) in healthy humans, and compared the brain processing using functional MRI. Pain reduction dampened sensory processing in the brain, whereas increased touch pleasantness increased sensory processing. Neurocircuitry associated with emotion and reward underpinned improvement of both pain and pleasant touch. Our findings suggest that expectation of improvement can recruit common neurocircuitry, which up- or down-regulates sensory processing, depending on whether the starting point is painful or pleasant. These results promote widening the scope of medical research to improvement of positive experiences and pleasure. Placebo analgesia is often conceptualized as a reward mechanism. However, by targeting only negative experiences, such as pain, placebo research may tell only half the story. We compared placebo improvement of painful touch (analgesia) with placebo improvement of pleasant touch (hyperhedonia) using functional MRI and a crossover design. Somatosensory processing was decreased during placebo analgesia and increased during placebo hyperhedonia. Both placebo responses were associated with similar patterns of activation increase in circuitry involved in emotion appraisal, including the pregenual anterior cingulate, medial orbitofrontal cortex, amygdala, accumbens, and midbrain structures. Importantly, placebo-induced coupling between the ventromedial prefrontal cortex and periaqueductal gray correlated with somatosensory decreases to painful touch and somatosensory increases to pleasant touch. These findings suggest that placebo analgesia and hyperhedonia are mediated by activation of shared emotion appraisal neurocircuitry, which down- or up-regulates early sensory processing, depending on whether the expectation is reduced pain or increased pleasure.

Unmyelinated tactile afferents underpin detection of low-force monofilaments

Human hairy but not glabrous skin has unmyelinated (C) tactile (CT) afferents that project to insular cortex. We studied two subjects with the rare sensory neuronopathy syndrome who lack A‐beta fibers but have relatively preserved C‐fiber function. Weak monofilaments were detected on hairy skin alone. Hence, the ability to detect light touch does not depend entirely on the A‐beta somatosensory system; CT afferents may contribute to the detection of weak monofilaments. Muscle Nerve, 2006