Johan Wessberg

Real-time prediction of hand trajectory by ensembles of cortical neurons in primates.

Signals derived from the rat motor cortex can be used for controlling one-dimensional movements of a robot arm. It remains unknown, however, whether real-time processing of cortical signals can be employed to reproduce, in a robotic device, the kind of complex arm movements used by primates to reach objects in space. Here we recorded the simultaneous activity of large populations of neurons, distributed in the premotor, primary motor and posterior parietal cortical areas, as non-human primates performed two distinct motor tasks. Accurate real-time predictions of one- and three-dimensional arm movement trajectories were obtained by applying both linear and nonlinear algorithms to cortical neuronal ensemble activity recorded from each animal. In addition, cortically derived signals were successfully used for real-time control of robotic devices, both locally and through the Internet. These results suggest that long-term control of complex prosthetic robot arm movements can be achieved by simple real-time transformations of neuronal population signals derived from multiple cortical areas in primates.

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.

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.

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.

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.