Rochelle Ackerley

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.

The development and validation of sensory and emotional scales of touch perception

No comprehensive language exists that describes the experience of touch. Three experiments were conducted to take steps toward establishing a touch lexicon. In Experiment I, 49 participants rated how well 262 adjectives described sensory, emotional and evaluative aspects of touch. In Experiment II, participants rated pairwise dissimilarities of the most descriptive words of the set. Multidimensional scaling (MDS) solutions representing semantic–perceptual spaces underlying the words resulted in a touch perception task (TPT) consisting of 26 ‘sensory’ attributes (e.g., bumpiness) and 14 ‘emotional’ attributes (e.g., pleasurable). In Experiment III, 40 participants used the TPT to rate unseen textured materials that were moved actively or received passively against the index fingerpad, volar forearm, and two underarm sites. MDS confirmed similar semantic–perceptual structures in Experiments II and III. Factor analysis of Experiment III data decomposed the sensory attribute ratings into factors labeled Roughness, Slip, Pile and Firmness, and the emotional attribute ratings into Comfort and Arousal factors. Factor scores varied among materials and sites. Greater intensity of sensory and emotional responses were reported when participants passively, as opposed to actively, received stimuli. The sensitivity of the TPT in identifying body site and mode of touch-related perceptual differences affirms the validity and utility of this novel linguistic/perceptual tool.

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.

Pontine Maps Linking Somatosensory and Cerebellar Cortices Are in Register with Climbing Fiber Somatotopy

The cerebropontocerebellar mossy fiber system is a major CNS sensorimotor pathway. We used a double-retrograde axonal tracing technique (red and green beads) to chart in rats the pontocerebellar projection to different electrophysiologically defined climbing fiber zones in the posterior lobe (face-receiving A2 zone and forelimb- and hindlimb-receiving parts of the C1 zone in the paramedian lobule and copula pyramidis, respectively). Individual cortical injection sites were verified as located in a given zone by mapping the pattern of cell labeling in the inferior olive, whereas labeled cells in the pontine nuclei were mapped using computer-aided three-dimensional reconstruction techniques. A number of topographical differences were found for the pontine projection to the individual zones. Projections to the A2 zone were bilateral, whereas to both parts of the C1 zone, the inputs were mainly contralateral. Furthermore, the A2 (face), C1 (forelimb), and C1 (hindlimb) zone projections were centered in progressively more caudal parts of the pontine nuclei with little or no overlap between them. The areas occupied by cell labeling for each zone corresponded closely to territories in the pontine nuclei shown previously to receive projections from somatotopically equivalent regions of the somatosensory cortex. This precise cerebropontocerebellar topography, defined by climbing fiber somatotopy, is a new principle of organization for linking somatosensory and cerebellar cortices. The convergence of direct and indirect sensory projections is likely to have important implications for cerebellar cortical processing.

An fMRI study on cortical responses during active self-touch and passive touch from others

Active, self-touch and the passive touch from an external source engage comparable afferent mechanoreceptors on the touched skin site. However, touch directed to glabrous skin compared to hairy skin will activate different types of afferent mechanoreceptors. Despite perceptual similarities between touch to different body sites, it is likely that the touch information is processed differently. In the present study, we used functional magnetic resonance imaging (fMRI) to elucidate the cortical differences in the neural signal of touch representations during active, self-touch and passive touch from another, to both glabrous (palm) and hairy (arm) skin, where a soft brush was used as the stimulus. There were two active touch conditions, where the participant used the brush in their right hand to stroke either their left palm or arm. There were two similar passive, touch conditions where the experimenter used an identical brush to stroke the same palm and arm areas on the participant. Touch on the left palm elicited a large, significant, positive blood-oxygenation level dependence (BOLD) signal in right sensorimotor areas. Less extensive activity was found for touch to the arm. Separate somatotopical palm and arm representations were found in Brodmann area (BA) 3 of the right primary somatosensory cortex (SI) and in both these areas, active stroking gave significantly higher signals than passive stroking. Active, self-touch elicited a positive BOLD signal in a network of sensorimotor cortical areas in the left hemisphere, compared to the resting baseline. In contrast, during passive touch, a significant negative BOLD signal was found in the left SI. Thus, each of the four conditions had a unique cortical signature despite similarities in afferent signaling or evoked perception. It is hypothesized that attentional mechanisms play a role in the modulation of the touch signal in the right SI, accounting for the differences found between active and passive touch.

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.

Touch Satiety: Differential Effects of Stroking Velocity on Liking and Wanting Touch Over Repetitions

A slow, gentle caress of the skin is a salient hedonic stimulus. Low threshold, unmyelinated C-tactile afferents fire preferentially to this type of touch, where slow (<1 cm/s) and fast (>10 cm/s) stroking velocities produce lower firing frequencies and are rated as less pleasant. The current aim was to investigate how the experience of tactile pleasantness changes with repeated exposure (satiety to touch). A further aim was to determine whether tactile satiety varied with different stroking velocities. The experimental paradigm used a controlled brush stroke to the forearm that was delivered repeatedly for ∼50 minutes. In Experiment 1, brush strokes were administered at three different velocities (0.3 cm/s, 3 cm/s and 30 cm/s), which were presented in a pseudo-randomised order. In Experiment 2, brush strokes were applied using only one velocity (either 3 or 30 cm/s). After each stroke, the participants rated both subjective pleasantness (liking) and wanting (the wish to be further exposed to the same stimulus) for each tactile sensation. In Experiment 1, both pleasantness and wanting showed a small, but significant, decrease over repetitions during stroking at 3 cm/s only, where the mean values for pleasantness and wanting were similar. Conversely, slower (0.3 cm/s) and faster (30 cm/s) stroking showed no decrease in ratings over time, however pleasantness was rated higher than wanting. In Experiment 2, both pleasantness and wanting showed a significant decrease over repetitions for both applied velocities, with a larger decrease in ratings for stroking at 3 cm/s. In conclusion, satiety to touch occurred with a slow onset and progression, where pleasantness and wanting ratings to stroking at 3 cm/s were affected more than at the slower or faster velocities. Tactile satiety appears to differ compared to appetitive and olfactory satiety, because the hedonic and rewarding aspects of touch persist for some time.

The role of tactile afference in shaping motor behaviour and implications for prosthetic innovation

The present review focusses on how tactile somatosensory afference is encoded and processed, and how this information is interpreted and acted upon in terms of motor control. We relate the fundamental workings of the sensorimotor system to the rehabilitation of amputees using modern prosthetic interventions. Our sense of touch is central to our everyday lives, from allowing us to manipulate objects accurately to giving us a sense of self-embodiment. There are a variety of specialised cutaneous mechanoreceptive afferents, which differ in terms of type and density according to the skin site. In humans, there is a dense innervation of our hands, which is reflected in their vast over-representation in somatosensory and motor cortical areas. We review the accumulated evidence from animal and human studies about the precise interplay between the somatosensory and motor systems, which is highly integrated in many brain areas and often not separable. The glabrous hand skin provides exquisite, discriminative detail about touch, which is useful for refining movements. When these signals are disrupted, such as through injury or amputation, the consequences are considerable. The development of sensory feedback in prosthetics offers a promising avenue for the full integration of a missing body part. Real-time touch feedback from motor intentions aids in grip control and the ability to distinguish different surfaces, even introducing the possibility of pleasure in artificial touch. Thus, our knowledge from fundamental research into sensorimotor interactions should be used to develop more realistic and integrative prostheses.

Covert tracking: A combined ERP and fixational eye movement study

Attention can be directed to particular spatial locations, or to objects that appear at anticipated points in time. While most work has focused on spatial or temporal attention in isolation, we investigated covert tracking of smoothly moving objects, which requires continuous coordination of both. We tested two propositions about the neural and cognitive basis of this operation: first that covert tracking is a right hemisphere function, and second that pre-motor components of the oculomotor system are responsible for driving covert spatial attention during tracking. We simultaneously recorded event related potentials (ERPs) and eye position while participants covertly tracked dots that moved leftward or rightward at 12 or 20°/s. ERPs were sensitive to the direction of target motion. Topographic development in the leftward motion was a mirror image of the rightward motion, suggesting that both hemispheres contribute equally to covert tracking. Small shifts in eye position were also lateralized according to the direction of target motion, implying covert activation of the oculomotor system. The data addresses two outstanding questions about the nature of visuospatial tracking. First, covert tracking is reliant upon a symmetrical frontoparietal attentional system, rather than being right lateralized. Second, this same system controls both pursuit eye movements and covert tracking.

A novel site of synaptic relay for climbing fibre pathways relaying signals from the motor cortex to the cerebellar cortical C1 zone

The climbing fibre projection from the motor cortex to the cerebellar cortical C1 zone in the posterior lobe of the rat cerebellum was investigated using a combination of physiological, anatomical and neuropharmacological techniques. Electrical stimulation of the ipsilateral fore‐ or hindimbs or somatotopically corresponding parts of the contralateral motor cortex evoked climbing fibre field potentials at the same cerebellar recording sites. Forelimb‐related responses were located in the C1 zone in the paramedian lobule or lobulus simplex and hindlimb‐related responses were located in the C1 zone in the copula pyramidis. Microinjections of anterograde axonal tracer (Fluoro‐Ruby or Fluoro‐Emerald) were made into the fore‐ or hindlimb parts of the motor cortex where stimulation evoked the largest cerebellar responses. After a survival period of 7–10 days, the neuraxis was examined for anterograde labelling. No terminal labelling was ever found in the inferior olive, but labelled terminals were consistently found in a well‐localized site in the dorso‐medial medulla, ventral to the gracile nucleus, termed the matrix region. Pharmacological inactivation of the matrix region (2 mm caudal to the obex) selectively reduced transmission in descending (cerebro‐olivocerebellar) but not ascending (spino‐olivocerebellar) paths targeting fore‐ or hindlimb‐receiving parts of the C1 zone. Transmission in spino‐olivocerebellar paths was either unaffected, or in some cases increased. The identification of a novel pre‐olivary relay in cerebro‐olivocerebellar paths originating from fore‐ and hindlimb motor cortex has implications for the regulation of transmission in climbing fibre pathways during voluntary movements and motor learning.