Modulating vicarious tactile perception with transcranial electrical current stimulation

Our capacity to share the experiences of others is a critical part of social behaviour. One process thought to be important for this is vicarious perception. Passively viewing touch activates some of the same network of brain regions as the direct experience of touch. This vicarious experience is usually implicit, but for some people, viewing touch evokes conscious tactile sensations (mirror‐touch synaesthesia). Recent work has attempted to induce conscious vicarious touch in those that do not normally experience these sensations, using transcranial direct current stimulation (tDCS). Anodal tDCS applied to primary somatosensory cortex (SI) was found to induce behavioural performance akin to mirror‐touch synaesthesia on a visuotactile interference task. Here, we conducted two experiments that sought to replicate and extend these findings by examining: (i) the effects of tDCS and high‐frequency transcranial random noise stimulation (tRNS) targeted at SI and temporo‐parietal junction (TPJ) on vicarious tactile perception, (ii) the extent to which any stimulation effects were specific to viewing touch to humans vs. inanimate agents and (iii) the influence of visual perspective (viewing touch from one's own vs. another's perspective) on vicarious perception. In Experiment 1, tRNS targeted at SI did not modulate vicarious perception. In Experiment 2, tDCS targeted at SI, but not TPJ, resulted in some modulation of vicarious perception, but there were important caveats to this effect. Implications regarding mechanisms of vicarious perception are discussed. Collectively, the findings do not provide convincing evidence for the potential to modulate vicarious tactile perception with transcranial electrical current stimulation.     

Distinct fine‐scale fMRI activation patterns of contra‐ and ipsilateral somatosensory areas 3b and 1 in humans

Inter‐areal and ipsilateral cortical responses to tactile stimulation have not been well described in human S1 cortex. By taking advantage of the high signal‐to‐noise ratio at 7 T, we quantified blood oxygenation level dependent (BOLD) response patterns and time courses to tactile stimuli on individual distal finger pads at a fine spatial scale, and examined whether there are inter‐areal (area 3b versus area 1) and interhemispheric response differences to unilateral tactile stimulation in healthy human subjects. We found that 2‐Hz tactile stimulation of individual fingertips evoked detectable BOLD signal changes in both contralateral and ipsilateral area 3b and area 1. Contralateral digit activations were organized in an orderly somatotopic manner, and BOLD responses in area 3b were more digit selective than those in area 1. However, the area of cortex that was responsive to stimulation of a single digit (stimulus–response field) was similar across areas. In the ipsilateral hemisphere, response magnitudes in both areas 3b and 1 were significantly weaker than those of the contralateral hemisphere. Digit activations exhibited no clear somatotopic organizational pattern in either area 3b or area 1, yet digit selectivity was retained in area 1 but not in area 3b. The observation of distinct digit‐selective responses of contralateral area 3b versus area 1 supports a higher order function of contralateral area 1 in spatial integration. In contrast, ipsilateral cortices may play a less discriminative role in the perception of unilateral tactile sensation in humans. Hum Brain Mapp 35:4841–4857, 2014. © 2014 Wiley Periodicals, Inc.     

Short communication: mapping of somatosensory cortices with functional magnetic resonance imaging in anaesthetized macaque monkeys

Functional magnetic resonance imaging (fMRI) in macaque monkeys is emerging as a potent candidate to bridge the gap between data from human fMRI studies and data from anatomy, electrophysiology and lesion studies in monkeys. The primary (SI) and secondary (SII) somatosensory cortices are the principal regions for somatosensory information processing and contain systematic representations of the body surface map (somatotopy). To examine the functional organization of the somatosensory cortices in anaesthetized macaque monkeys with fMRI, we asked whether focal and differential activation could be observed in SI and SII in response to tactile stimulation with two parameters: body sides (right and left) and body regions (hand and face). We found that changes in stimulus parameters elicited differential focal activation in both SI and SII in two ways. First, the hand and face stimulation activated SI and SII in the contralateral, but not in the ipsilateral, hemisphere. Second, the hand and face stimulation differentially activated two adjacent regions in both SI and SII. These fMRI results appear to correlate with previous mapping studies by other methods in the macaque somatosensory cortices. This study shows the feasibility of fMRI studies in mapping multiple sensory areas in monkeys by which we can distinguish between adjacent functionally distinct regions.     

Altered somatosensory processing in trigeminal neuralgia

Trigeminal neuralgia (TN) is a pain state characterized by intermittent unilateral pain attacks in one or several facial areas innervated by the trigeminal nerve. The somatosensory cortex is heavily involved in the perception of sensory features of pain, but it is also the primary target for thalamic input of nonpainful somatosensory information. Thus, pain and somatosensory processing are accomplished in overlapping cortical structures raising the question whether pain states are associated with alteration of somatosensory function itself. To test this hypothesis, we used functional magnetic resonance imaging to assess activation of primary (SI) and secondary (SII) somatosensory cortices upon nonpainful tactile stimulation of lips and fingers in 18 patients with TN and 10 patients with TN relieved from pain after successful neurosurgical intervention in comparison with 13 healthy subjects. We found that SI and SII activations in patients did neither depend on the affected side of TN nor differ between operated and nonoperated patients. However, SI and SII activations, but not thalamic activations, were significantly reduced in patients as compared to controls. These differences were most prominent for finger stimulation, an area not associated with TN. For lip stimulation SI and SII activations were reduced in patients with TN on the contra‐ but not on the ipsilateral side to the stimulus. These findings suggest a general reduction of SI and SII processing in patients with TN, indicating a long‐term modulation of somatosensory function and pointing to an attempt of cortical adaptation to potentially painful stimuli. Hum Brain Mapp, 2009. © 2009 Wiley‐Liss, Inc.     

Localization of pain‐related brain activation: A meta‐analysis of neuroimaging data

A meta‐analysis of 140 neuroimaging studies was performed using the activation‐likelihood‐estimate (ALE) method to explore the location and extent of activation in the brain in response to noxious stimuli in healthy volunteers. The first analysis involved the creation of a likelihood map illustrating brain activation common across studies using noxious stimuli. The left thalamus, right anterior cingulate cortex (ACC), bilateral anterior insulae, and left dorsal posterior insula had the highest likelihood of being activated. The second analysis contrasted noxious cold with noxious heat stimulation and revealed higher likelihood of activation to noxious cold in the subgenual ACC and the amygdala. The third analysis assessed the implications of using either a warm stimulus or a resting baseline as the control condition to reveal activation attributed to noxious heat. Comparing noxious heat to warm stimulation led to peak ALE values that were restricted to cortical regions with known nociceptive input. The fourth analysis tested for a hemispheric dominance in pain processing and showed the importance of the right hemisphere, with the strongest ALE peaks and clusters found in the right insula and ACC. The fifth analysis compared noxious muscle with cutaneous stimuli and the former type was more likely to evoke activation in the posterior and anterior cingulate cortices, precuneus, dorsolateral prefrontal cortex, and cerebellum. In general, results indicate that some brain regions such as the thalamus, insula and ACC have a significant likelihood of activation regardless of the type of noxious stimuli, while other brain regions show a stimulus‐specific likelihood of being activated. Hum Brain Mapp, 2013. © 2011 Wiley Periodicals, Inc.     

Effects of different viewing perspectives on somatosensory activations during observation of touch

Previous studies showed that neurons in the monkey premotor cortex became active when performing a particular action and also when observing the same action performed by others. These findings suggest a mirror system for action observation. Recently, bimodal neurons, sensitive both to visual and tactile stimulation, were reported in the parietal cortex, suggesting a potential mirror neuron system for observing and experiencing tactile stimulation. Subsequently, a mirror neuron system for observed touch has been suggested. The current study was designed to determine whether the activation of a sensory mirror system during touch observation is affected by possible attributions of the observed touch to oneself (subjective view) or to somebody else (objective view). In the study, healthy volunteers observed video clips of a touched or nontouched hand either in an egocentric or in an allocentric perspective during functional magnetic resonance imaging. Results showed activation of somatosensory cortices when observing the hand being touched in egocentric as well as in the allocentric perspectives. Moreover, somatosensory responses differed depending on the perspective of the observed touch. We discuss the results in terms of a possible mirror neuron system for observed and experienced touch. Hum Brain Mapp 2009. © 2009 Wiley‐Liss, Inc.     

Maternal sensitivity and infant neural response to touch: an fNIRS study

The mother’s attunement to her infant’s emotional needs influences her use of touching behaviors during mother–infant interactions. Moreover, maternal touch appears to modulate infants’ physiological responses to affective touch. However, little is known about the impact of maternal sensitivity on infants’ touch processing at a brain level. This study explored the association between maternal sensitivity when infants (N = 24) were 7 months old and their patterns of cortical activation to touch at 12 months. Brain activation was measured using functional near-infrared spectroscopy. Changes in oxy-hemoglobin (HbO₂) and deoxy-hemoglobin (HHb) concentrations were measured in the left somatosensory cortex and right temporal cortex while infants received two types of tactile stimulation—affective and discriminative touch. Results showed that a lower maternal sensitivity was associated with a higher HbO₂ response for discriminative touch over the temporal region. Additionally, infants of less sensitive mothers tended to present a higher response in HbO₂ for affective touch over the somatosensory region. These findings suggest that less sensitive interactions might result in a lower exposure to maternal touch, which can be further related to infants’ neural processing of touch.     

Seeing touch in the somatosensory cortex: a TMS study of the visual perception of touch

Recent studies suggest the existence of a visuo-tactile mirror system, comprising the primary (SI) and secondary (SII) somatosensory cortices, which matches observed touch with felt touch. Here, repetitive transcranial magnetic stimulation (rTMS) was used to determine whether SI or SII play a functional role in the visual processing of tactile events. Healthy participants performed a visual discrimination task with tactile stimuli (a finger touching a hand) and a control task (a finger moving without touching). During both tasks, rTMS was applied over either SI or SII, and to the occipital cortex. rTMS over SI selectively reduced subject performance for interpreting whether a contralateral visual tactile stimulus contains a tactile event, whereas SII stimulation impaired visual processing regardless of the tactile component. These findings provide evidence for a multimodal sensory-motor system with mirror properties, where somatic and visual properties of action converge. SI, a cortical area traditionally viewed as modality-specific, is selectively implicated in the visual processing of touch. These results are in line with the existence of a sensory mirror system mediating the embodied simulation concept.     

Neural correlates of an illusory touch experience investigated with fMRI

When asked to judge the presence or absence of near-threshold tactile stimuli, participants often report touch experiences when no tactile stimulation has been delivered (‘false alarms’). The simultaneous presentation of a light flash during the stimulation period can increase the frequency of touch reports, both when touch is and is not present. Using fMRI, we investigated the BOLD response during both light-present and light-absent false alarms, testing predictions concerning two possible neural mechanisms underlying these illusory touch experiences: activation of a tactile representation in primary somatosensory cortex (SI) and/or activation of a tactile representation in late processing areas outside of sensory-specific cortex, such as medial prefrontal cortex (MPC). Our behavioural results showed that participants made false alarms in light-present and light-absent trials, both of which activated regions of the medial parietal and medial prefrontal cortex including precuneus, posterior cingulate and paracingulate cortex, suggesting the same underlying mechanism. However, only a non-significant increase in SI activity was measured in response to false alarm vs. correct rejection trials. We argue that our results provide evidence for the role of top-down regions in somatic misperception, consistent with findings from studies in humans and non-human primates.     

Prominent activation of the intraparietal and somatosensory areas during angle discrimination by intra-active touch

Intra‐active touch (IAT) is a process that involves a body part doing the touching (active touch [AT]) and another body part being touched (passive touch [PT]) simultaneously. The brain representation related to IAT is still unclear. A total of 23 subjects carried out angle discrimination under PT, AT and IAT conditions with functional magnetic resonance imaging. All of the tasks were strictly dependent on cutaneous feedback from the finger(s). As the subjects were able to perceive the angle stimuli from the right (touching) and left (touched) sides during the IAT condition, we expected there would be greater brain activation with the IAT condition than for the AT or PT condition. Therefore, we hypothesized that the region within and/or around the intraparietal sulcus (IPS) and the part of the primary somatosensory cortex (SI) that is associated with high‐level tactile spatial processing would be more active during the IAT task than during the AT and PT tasks. Compared with the areas activated by the motor somatosensory control task, the most prominent activation areas evoked by the three‐angle discrimination tasks were in the SI and secondary somatosensory cortex areas in the bilateral parietal operculum, IPS, lateral occipital complex, insula and cerebellum. Finally, we directly compared IAT with AT and PT, and the results suggest that the contralateral part of IPS and part of the SI are more active under IAT conditions than under either AT or PT conditions. These results suggest that both hemispheres contribute to angle discrimination during IAT. Hum Brain Mapp, 2012. © 2011 Wiley Periodicals, Inc.     

Autistic traits modulate cortical responses to affective but not discriminative touch

The sense of touch is primarily considered a discriminative and exteroceptive sense, facilitating the detection, manipulation and exploration of objects, via an array of low‐threshold mechanoreceptors and fast conducting A‐beta (Aβ) afferents. However, a class of unmyelinated, low‐threshold mechanoreceptors identified in the hairy skin of mammals have been proposed to constitute a second, anatomically distinct system coding the affective qualities of touch. Unlike Aβs, which increase their firing rate linearly with the velocity of a stimulus moving across their receptive field, the response of these C‐tactile afferents (CTs) is described by an inverted ‘U’ curve fit, responding optimally to a skin temperature stimulus moving at between 1 and 10 cm/s. Given the distinct velocity tuning of these fast and slow touch fibres, here we used event‐related potentials to compare the time course of neural responses to 1st (fast) and 2nd (slow) touch systems. We identified a higher amplitude P300 in response to fast, Aβ‐targeted, versus slow CT‐targeted, stroking touch. In contrast, we identified a previously described, C‐fibre specific, ultra‐late potential (ULP) associated with CT‐targeted input. Of special note as regards the function of CTs is that the amplitude of the ULP was negatively correlated with self‐reported levels of autistic traits, which is consistent with the hypothesized affective and social significance of this response. Taken together, these findings provide further support for distinct discriminative and affective touch systems and suggests the temporal resolution of EEG provides an as yet underutilized tool for exploring individual differences in response sensitivity to CT‐targeted touch.     

Activation of somatosensory cortical areas varies with attentional state: an fMRI study

The differing roles of SI and SII areas in the somatosensory system have received relatively little interest in previous research. In the present study fMRI was applied to determine possible changes in activations of these areas as a function of attentional modulation (attending vs. not attending to the stimulation of a finger). The results showed that attention induced larger regional changes, mostly enlargements of activated areas, at SII than at SI. The number of instances where new, emerging activations, not present in the non-attend condition, were observed was larger at SII than at SI. These differential attentional effects indicate that SII areas may have a role in more complex tactile functions such as tactile working memory mechanisms.     

Neural correlates of gentle skin stroking in early infancy

Physical expressions of affection play a foundational role in early brain development, but the neural correlates of affective touch processing in infancy remain unclear. We examined brain responses to gentle skin stroking, a type of tactile stimulus associated with affectionate touch, in young infants. Thirteen term-born infants aged 11–36 days, recruited through the FinnBrain Birth Cohort Study, were included in the study. Soft brush strokes, which activate brain regions linked to somatosensory as well as socio-affective processing in children and adults, were applied to the skin of the right leg during functional magnetic resonance imaging. We examined infant brain responses in two regions-of-interest (ROIs) known to process gentle skin stroking – the postcentral gyrus and posterior insular cortex – and found significant responses in both ROIs. These results suggest that the neonate brain is responsive to gentle skin stroking within the first weeks of age, and that regions linked to primary somatosensory as well as socio-affective processing are activated. Our findings support the notion that social touch may play an important role in early life sensory processing. Future research will elucidate the significance of these findings for human brain development.     

Early integration of bilateral touch in the primary somatosensory cortex

Animal, as well as behavioural and neuroimaging studies in humans have documented integration of bilateral tactile information at the level of primary somatosensory cortex (SI). However, it is still debated whether integration in SI occurs early or late during tactile processing, and whether it is somatotopically organized. To address both the spatial and temporal aspects of bilateral tactile processing we used magnetoencephalography in a tactile repetition‐suppression paradigm. We examined somatosensory evoked‐responses produced by probe stimuli preceded by an adaptor, as a function of the relative position of adaptor and probe (probe always at the left index finger; adaptor at the index or middle finger of the left or right hand) and as a function of the delay between adaptor and probe (0, 25, or 125 ms). Percentage of response‐amplitude suppression was computed by comparing paired (adaptor + probe) with single stimulations of adaptor and probe. Results show that response suppression varies differentially in SI and SII as a function of both spatial and temporal features of the stimuli. Remarkably, repetition suppression of SI activity emerged early in time, regardless of whether the adaptor stimulus was presented on the same and the opposite body side with respect to the probe. These novel findings support the notion of an early and somatotopically organized inter‐hemispheric integration of tactile information in SI. Hum Brain Mapp 36:1506–1523, 2015. © 2014 Wiley Periodicals, Inc.     

Rough primes and rough conversations: evidence for a modality-specific basis to mental metaphors

How does our brain organize knowledge? Traditional theories assume that our knowledge is represented abstractly in an amodal conceptual network of formal logic symbols. The theory of embodied cognition challenges this view and argues that conceptual representations that constitute our knowledge are grounded in sensory and motor experiences. We tested this hypothesis by examining how the concept of social coordination is grounded metaphorically in the tactile sensation of roughness. Participants experienced rough or smooth touch before being asked to judge an ambiguous social interaction. Results revealed that rough touch made social interactions appear more difficult and adversarial, consistent with the rough metaphor. This impact of tactile cues on social impressions was accompanied by a network including primary and secondary somatosensory cortices, amygdala, hippocampus and inferior prefrontal cortex. Thus, the roughness of tactile stimulation affected metaphor-relevant (but not metaphor-irrelevant) behavioral and neural responses. Receiving touch from a rough object seems to trigger the application of associated ontological concepts (or scaffolds) even for unrelated people and situations (but not to unrelated or more general feelings). Since this priming was based on somatosensory brain areas, our results provide support for the theory that sensorimotor grounding is intrinsic to cognitive processes.     

Stability of tactile- and pain-related fMRI brain activations: an examination of threshold-dependent and threshold-independent methods

Functional MRI can be used to assess brain plasticity over time. To confidently attribute changes in activation patterns to cortical plasticity, it is important to establish the stability of cortical activation patterns. Because little is known concerning the stability of somatosensory-evoked brain responses, we assessed the reproducibility of within-subject responses in key somatosensory regions [thalamus, primary and secondary cortex (S1, S2)] to tactile and painful stimuli using threshold-dependent and threshold-independent analyses. Six subjects underwent four biweekly scanning sessions during which tactile and painful stimuli were applied to the hand. Standard thresholding and voxel counting techniques were compared with a novel threshold-independent method utilizing percent signal change within the regions of interest. Contralateral S1 and S2 were qualitatively reproducible during tactile stimulation, with overlapping activations >85% of the time. S2 was also highly reproducible during painful stimulation (88%), whereas S1 was less reproducible (44%). However, activation in the thalamus to both tactile and painful stimulation was highly variable. Ipsilateral activation was consistent within S2 but sparse within S1 and thalamus. Deactivations within ipsilateral S1 occurred 48% of the time with tactile stimuli, and 90% of the time with painful stimuli. Within contralaterally activated regions intraclass correlations (ICCs) were very high using the unthresholded method regardless of the type of stimulation, whereas much lower ICCs arose from the thresholded analyses. These data indicate that a threshold-independent analysis can produce more reproducible outcomes than a standard threshold-dependent analysis.     

Seeing the hand boosts feeling on the cheek

Tactile acuity improves when subjects look at the stimulated body part, even when vision does not provide any information relevant to touch. This “visual enhancement of touch” (VET), might involve modulation of primary somatosensory cortex (SI) processing by multimodal information related to the body. SI shows a characteristic somatotopic organization, with the face and hand represented laterally and adjacent to each other, and the foot represented more medially.The aim of this study was to investigate whether VET is limited to the viewed body part, spreads to all body parts, or generalizes only to body parts represented in SI closely to the viewed body part. Tactile acuity was assessed in healthy subjects on the hand, face and foot, while subjects viewed either their stimulated hand, their foot or were blindfolded: viewing the hand, compared to blindfold condition, enhanced tactile sensitivity on the hand and also on the face, but not on the foot. Conversely, viewing the foot, compared to blindfold condition, improved touch only on the foot. Two control experiments assured this effect was due to viewing the body and not to directing visuo-spatial attention toward the location of tactile stimulation. The present results show that VET acts accordingly to a somatotopic gradient based on SI organization, suggesting that this multisensory effect may occur within SI. This finding might have a possible application to facilitate the recovery of tactile deficits in patients with a lesion of somatosensory cortices.     

Effects of acute tryptophan depletion on central processing of CT‐targeted and discriminatory touch in humans

C‐tactile afferents (CTs) are slowly conducting nerve fibres, present only in hairy skin. They are optimally activated by slow, gentle stroking touch, such as those experienced during a caress. CT stimulation activates affective processing brain regions, alluding to their role in affective touch perception. We tested a theory that CT‐activating touch engages the pro‐social functions of serotonin, by determining whether reducing serotonin, through acute tryptophan depletion, diminishes subjective pleasantness and affective brain responses to gentle touch. A tryptophan depleting amino acid drink was administered to 16 healthy females, with a further 14 receiving a control drink. After 4 h, participants underwent an fMRI scan, during which time CT‐innervated forearm skin and CT non‐innervated finger skin was stroked with three brushes of differing texture, at CT‐optimal force and velocity. Pleasantness ratings were obtained post scanning. The control group showed a greater response in ipsilateral orbitofrontal cortex to CT‐activating forearm touch compared to touch to the finger where CTs are absent. This differential response was not present in the tryptophan depleted group. This interaction effect was significant. In addition, control participants showed a differential primary somatosensory cortex response to brush texture applied to the finger, a purely discriminatory touch response, which was not observed in the tryptophan depleted group. This interaction effect was also significant. Pleasantness ratings were similar across treatment groups. These results implicate serotonin in the differentiation between CT‐activating and purely discriminatory touch responses. Such effects could contribute to some of the social abnormalities seen in psychiatric disorders associated with abnormal serotonin function.     

Visual perception of bodily interactions in the primary somatosensory cortex

Brain imaging studies in humans have revealed the existence of a visuo-tactile system, which matches observed touch with felt touch. In this system, the primary somatosensory cortex (SI) appears to play a causal role in the visual processing of tactile events. Whether this visuo-tactile mechanism for touch in SI applies to the sight of 'any' touch, or whether it is restricted to the domain of body-related tactile experiences remains unresolved. To address this issue, repetitive transcranial magnetic stimulation (rTMS) was used to determine whether activity in SI is strictly related to the visual processing of human body-part interactions, or is also involved in processing the contact between inanimate objects, or between human body-parts and objects. The results show that rTMS over SI selectively impaired the processing of a contralateral visual stimulus depicting a human body-part being touched by a human agent, while it did not affect the visual perception of contact between objects, or between human body-parts and objects. Correlation analysis shows that this effect was associated with the intensity and embodiment of the observed touched. This result suggests that SI is more suited to represent social touch, contributing to our understanding of the effect of interpersonal tactile interactions between people.