Functional and structural brain differences associated with mirror-touch synaesthesia

Observing touch is known to activate regions of the somatosensory cortex but the interpretation of this finding is controversial (e.g. does it reflect the simulated action of touching or the simulated reception of touch?). For most people, observing touch is not linked to reported experiences of feeling touch but in some people it is (mirror-touch synaesthetes). We conducted an fMRI study in which participants (mirror-touch synaesthetes, controls) watched movies of stimuli (face, dummy, object) being touched or approached. In addition we examined whether mirror touch synaesthesia is associated with local changes of grey and white matter volume in the brain using VBM (voxel-based morphometry). Both synaesthetes and controls activated the somatosensory system (primary and secondary somatosensory cortices, SI and SII) when viewing touch, and the same regions were activated (by a separate localiser) when feeling touch — i.e. there is a mirror system for touch. However, when comparing the two groups, we found evidence that SII seems to play a particular important role in mirror-touch synaesthesia: in synaesthetes, but not in controls, posterior SII was active for watching touch to a face (in addition to SI and posterior temporal lobe); activity in SII correlated with subjective intensity measures of mirror-touch synaesthesia (taken outside the scanner), and we observed an increase in grey matter volume within the SII of the synaesthetes' brains. In addition, the synaesthetes showed hypo-activity when watching touch to a dummy in posterior SII. We conclude that the secondary somatosensory cortex has a key role in this form of synaesthesia

The cutaneous 'rabbit' illusion affects human primary sensory cortex somatopically

We used functional magnetic resonance imaging (fMRI) to study neural correlates of a robust somatosensory illusion that can dissociate tactile perception from physical stimulation. Repeated rapid stimulation at the wrist, then near the elbow, can create the illusion of touches at intervening locations along the arm, as if a rabbit hopped along it. We examined brain activity in humans using fMRI, with improved spatial resolution, during this version of the classic cutaneous rabbit illusion. As compared with control stimulation at the same skin sites (but in a different order that did not induce the illusion), illusory sequences activated contralateral primary somatosensory cortex, at a somatotopic location corresponding to the filled-in illusory perception on the forearm. Moreover, the amplitude of this somatosensory activation was comparable to that for veridical stimulation including the intervening position on the arm. The illusion additionally activated areas of premotor and prefrontal cortex. These results provide direct evidence that illusory somatosensory percepts can affect primary somatosensory cortex in a manner that corresponds somatotopically to the illusory percept

More than skin deep: body representation beyond primary somatosensory cortex

The neural circuits underlying initial sensory processing of somatic information are relatively well understood. In contrast, the processes that go beyond primary somatosensation to create more abstract representations related to the body are less clear. In this review, we focus on two classes of higher-order processing beyond somatosensation. Somatoperception refers to the process of perceiving the body itself, and particularly of ensuring somatic perceptual constancy. We review three key elements of somatoperception: (a) remapping information from the body surface into an egocentric reference frame (b) exteroceptive perception of objects in the external world through their contact with the body and (c) interoceptive percepts about the nature and state of the body itself. Somatorepresentation, in contrast, refers to the essentially cognitive process of constructing semantic knowledge and attitudes about the body, including: (d) lexical-semantic knowledge about bodies generally and one’s own body specifically, (e) configural knowledge about the structure of bodies, (f) emotions and attitudes directed towards one’s own body, and (g) the link between physical body and psychological self. We review a wide range of neuropsychological, neuroimaging and neurophysiological data to explore the dissociation between these different aspects of higher somatosensory function

"Feeling" others' painful actions: the sensorimotor integration of pain and action information.

Sensorimotor regions of the brain have been implicated in simulation processes such as action understanding and empathy, but their functional role in these processes remains unspecified. We used functional magnetic resonance imaging (fMRI) to demonstrate that postcentral sensorimotor cortex integrates action and object information to derive the sensory outcomes of observed hand-object interactions. When subjects viewed others' hands grasping or withdrawing from objects that were either painful or nonpainful, distinct sensorimotor subregions emerged as showing preferential responses to different aspects of the stimuli: object information (noxious vs. innocuous), action information (grasps vs. withdrawals), and painful action outcomes (painful grasps vs. all other conditions). Activation in the latter region correlated with subjects' ratings of how painful each object would be to touch and their previous experience with the object. Viewing others' painful grasps also biased behavioral responses to actual tactile stimulation, a novel effect not seen for auditory control stimuli. Somatosensory cortices, including primary somatosensory areas 1/3b and 2 and parietal area PF, may therefore subserve somatomotor simulation processes by integrating action and object information to anticipate the sensory consequences of observed hand-object interactions

The Cutaneous Rabbit Illusion Affects Human Primary Sensory Cortex Somatotopically

We used functional magnetic resonance imaging (fMRI) to study neural correlates of a robust somatosensory illusion that can dissociate tactile perception from physical stimulation. Repeated rapid stimulation at the wrist, then near the elbow, can create the illusion of touches at intervening locations along the arm, as if a rabbit hopped along it. We examined brain activity in humans using fMRI, with improved spatial resolution, during this version of the classic cutaneous rabbit illusion. As compared with control stimulation at the same skin sites (but in a different order that did not induce the illusion), illusory sequences activated contralateral primary somatosensory cortex, at a somatotopic location corresponding to the filled-in illusory perception on the forearm. Moreover, the amplitude of this somatosensory activation was comparable to that for veridical stimulation including the intervening position on the arm. The illusion additionally activated areas of premotor and prefrontal cortex. These results provide direct evidence that illusory somatosensory percepts can affect primary somatosensory cortex in a manner that corresponds somatotopically to the illusory percept

Tactile Modulation of the Sensory and Cortical Responses Elicited by Focal Cooling in Humans and Mice

Distinct sensory receptors transduce thermal and mechanical energies, but we have unified, coherent thermotactile experiences of the objects we touch. These experiences must emerge from the interaction of thermal and tactile signals within the nervous system. How do thermal and mechanical signals modify each other as they interact along the pathway from skin to conscious experience? In this thesis, we study how mechanical touch modulates cooling responses by combining psychophysics in humans and neural recordings in rodents. For this, we developed a novel stimulator to deliver focal, temperature-controlled cooling without touch. First, we used this method to study in humans the sensitivity to focal cooling with and without touch. We found that touch reduces the sensitivity to near-threshold cooling, which is perhaps analogous to the well-established ‘gating’ of pain by touch. Second, we studied the perceived intensity of cooling with and without touch. We found that tactile input enhances the perceived intensity of cooling. Third, we measured the responses of the mouse primary somatosensory cortex to cooling and mechanical stimuli using imaging and electrophysiological methods. We found multisensory stimuli elicited non-linear cortical responses at both the population and cellular level. Altogether, in this thesis, we show perceptual and cortical responses to non-tactile cooling for the first time. Based on our observations, we propose a new model to explain the interactions between cooling and mechanical signals in the nervous system. This thesis advances our understanding of how touch modulates cold sensations during thermotactile stimulation

The Tactile Motion Aftereffect

The tactile motion aftereffect (tMAE) is a perceptual phenomenon in which illusory motion is reported following adaptation to a unidirectionally moving tactile stimulus. Unlike its visual counterpart, relatively little is known about the tMAE. For that reason, the purpose of this dissertation was to gain a better understanding of the tMAE using both psychophysical and neuroimaging techniques. In a series of five experiments the skin was adapted using a plastic cylinder with a square-wave patterned surface. Chapter 2 consists of two experiments, both of which adapted the glabrous surface of the right hand. Experiment 1 showed that the prevalence, duration, and vividness of the tMAE did not differ between the fingers (thumb excluded), palm and fingers (thumb included), and palm and fingers (thumb excluded). Thus, the divergent prevalence rates of two previous studies (Hollins & Favorov, 1994; Lerner & Craig, 1994) cannot be explained by the inclusion of the thumb in the latter study. Experiment 2 showed that as adapting speed increased from 15 to 75 rpm so did the prevalence, duration, and vividness of the tMAE. Previously it has been shown that the tMAE duration increases with adapting duration (Hollins & Favorov, 1994). Given that speed * duration = distance, increasing either adapting speed or duration also increases distance. As such, it was unclear which parameter(s) caused the observed increase in prevalence, duration, and vividness. Chapter 3 manipulated adapting duration (1, 2, and 4 min) and speed (30 and 60 rpm) in the same experiment, thereby allowing the effect of distance to be assessed in the interaction. The results showed that the prevalence, duration, and vividness of the tMAE increased with adapting speed. There was also a positive relationship between adapting duration and prevalence, but not duration or vividness, of the illusion. Distance was only a factor when it came to the tMAE duration. To gain insight into the peripheral neural basis of the tMAE, Chapter 4 measured the prevalence, duration, and vividness of the tMAE on skin areas that differ in their composition of fast adapting (FA) mechanoreceptive units, namely the right cheek, volar surface of the forearm, and glabrous surface of the hand. While there was no difference in duration or vividness between the skin surfaces tested, the tMAE was reported twice as often on the hand than the cheek and forearm, which did not differ significantly from one another. This finding suggests that the tMAE can be induced by adapting FA type I (FA I) units in the glabrous skin (hand) and the hair follicle units (cheek and forearm) and/or the FA I (cheek) and field (forearm) units in the hairy skin. Chapter 5 investigated the central neural basis of the tMAE using functional magnetic resonance imaging (fMRI). Of the areas shown to be responsive to tactile motion on the glabrous surface of the right hand, namely the contralateral (left) thalamus, postcentral gyrus (PCG), and parietal operculum, only the PCG showed evidence of the tMAE; that is, there was a sustained fMRI response following the offset of the illusion trials (cylinder rotating at 60 rpm), but not the control trials (cylinder rotating at 15 rpm), presumably reflecting illusory motion perception. Taken together, the experiments described herein expand our knowledge of the tMAE. Using a cylinder adapting apparatus, it was shown that: prevalence is the best measure of tMAE strength; the tMAE is not as robust as its visual counterpart; adapting duration and speed positively affect the prevalence of the tMAE; the tMAE is twice as prevalent on the glabrous than the hairy skin; the FAI and hair follicle units likely underlie the tMAE; the tMAE is likely caused by adapting direction selective neurons in the contralateral PCG

Mirror-touch synaesthesia: the role of shared representations in social cognition

Synaesthesia is a condition in which one property of a stimulus results in conscious experiences of an additional attribute. In mirror-touch synaesthesia, the synaesthete experiences a tactile sensation on their own body simply when observing touch to another person. This thesis investigates the prevalence, neurocognitive mechanisms, and consequences of mirror-touch synaesthesia. Firstly, the prevalence and neurocognitive mechanisms of synaesthesia were assessed. This revealed that mirrortouch synaesthesia has a prevalence rate of 1.6%, a finding which places mirror-touch synaesthesia as one of the most common variants of synaesthesia. It also indicated a number of characteristics of the condition, which led to the generation of a neurocognitive model of mirror-touch synaesthesia. An investigation into the perceptual consequences of synaesthesia revealed that the presence of synaesthesia is linked with heightened sensory perception - mirror-touch synaesthetes showed heightened tactile perception and grapheme-colour synaesthetes showed heightened colour perception. Given that mirror-touch synaesthesia has been shown to be linked to heightened sensorimotor simulation mechanisms, the impact of facilitated sensorimotor activity on social cognition was then examined. This revealed that mirror-touch synaesthetes show heightened emotional sensitivity compared with control participants. To compliment this, two transcranial magnetic stimulation (TMS) studies were then conducted to assess the impact of suppressing sensorimotor activity on the expression recognition abilities of healthy adults. Consistent with the findings of superior emotion sensitivity in mirror-touch synaesthesia (where there is facilitated sensorimotor activity), suppressing sensorimotor resources resulted in impaired expression recognition across modalities. The findings of the thesis are discussed in relation to neurocognitive models of synaesthesia and of social cognition