Materials and methods
Participants, stimuli and procedure, and statistical analyses
Twelve participants (right-handed = 11; mean age = 25 ± 3 years; 11 females), selected using the same criteria of Experiment 1, entered Experiment 2.
The tasks, the experimental setting and the statistical analysis were the same as those of Experiment 1, the only difference relating to the visual stimuli. In the Human-to-Object Touch task, the video clips depicted the right or the left index finger moving downward and touching the stick below, or simply approaching the stick, without touching it (target and catch trials, respectively). In the Object-to-Human Touch task, the video clips shows the left or the right stick moving downward and touching the hand below, or approaching without touching it (target and catch trials, respectively) (see Fig. 1A).
The TMS procedure was identical to Experiment 1, but now only SI cortex was stimulated. Mean individual MT at rest was 58% (SD = 7.8%) of the maximal output of the stimulator. Analyses of errors, sensitivity and response bias were performed via a 2 (Task – Human-to-Object, Object-to-Human) by 2 (Session – Baseline, SI-rTMS) by 2 (Side – Left-, Right-sided stimuli) anova.
The questionnaire for Experiment 2 comprised the following items: (1) ‘The tactile stimulation looked like to be very intense’. (2) ‘The tactile stimulation looked like to be very unpleasant’. (3) ‘The hand being touched could depict my hand’. (4) ‘The touching finger could depict my finger’. Items 1 and 2 were given for both Human-to-Object and Object-to-Human Touch tasks, item 3 was given for the Object-to-human Touch task, and item 4 was given for the Human-to-object Touch task. For every item, participants rated their agreement using a five-point scale (see Experiment 1).
Analysis of the errors revealed a significant effect of Task (F1,11 = 7.88, P < 0.02, pη2 = 0.71), showing that subjects made more errors in the Human-to-Object Touch task (19%) than in the Object-to-Human Touch task (15%) (Fig. 2B). The main effect of Session (F1,11 = 6.76, P < 0.02, pη2 = 0.31) showed that the errors were slightly higher in the Baseline (18%) as compared with the SI-rTMS session (16%). Other effects did not reach significance – Side (F1,11 = 0.06, P = 0.8), Task by Session (F1,11 = 0.03, P = 0.9), Task by Side (F1,11 = 0.95, P = 0.4), Session by Side (F1,11 = 0.26, P = 0.6), Task by Session by Side (F1,11 = 1.29, P = 0.3) (Fig. 2B).
Sensitivity analysis did not show any significant main effect – Task (F1,11 = 2.67, P = 0.1), Session (F1,11 = 4.67, P = 0.07), Side (F1,11 = 0.01, P = 0.9), Task by Session (F1,11 = 0.58, P = 0.5), Task by Side (F1,11 = 1.33, P = 0.3), Session by Side (F1,11 = 1.71, P = 0.2), Task by Session by Side (F1,11 = 0.16, P = 0.7).
Similarly, analysis of the response bias did not show any significant main effect – Task (F1,11 = 1.94, P = 0.2), Session (F1,11 = 0.15, P = 0.7), Side (F1,11 = 0.56, P = 0.5), Task by Session (F1,11 = 3.07, P = 0.1), Task by Side (F1,11 = 0.77, P = 0.4), Session by Side (F1,11 = 0.93, P = 0.4), Task by Session by Side (F1,11 = 0.39, P = 0.5) (Fig. 2D).
To control for whether the four tasks differed for the level of difficulty, we analysed the d′ values of the baseline session via a three-way anova with Experiment as between-subjects factor, and Task and Side as within-subjects factors. No significant effect emerged (P > 0.09), suggesting that the four tasks were equally sensitive.
Participants disagreed that the Human-to-Object Touch was unpleasant (−0.72, t11 = −2.18, P < 0.05) and that the touching index finger could depict their own finger (−1.18, t11 = −3.13, P < 0.01); their scores did not differ from 0 with respect to VAS intensity (−0.27, t11 = −0.55, P = 0.5).
The Object-to-Human Touch was not rated as intense (0.5, t11 = 2.17, P = 0.07) nor as unpleasant (−0.64, t11 = −2.05, P = 0.07), but participants agreed that the touched hand could represent their own hand (0.72, t11 = 2.66, P < 0.02).
The aim of the present study was to uncover the selectivity of the causal involvement of SI in the visual processing of tactile events, with respect to the type of observed touching and touched stimuli. In particular, in the first experiment we compared the effect of rTMS interference of SI and VI on the ability to detect visual stimuli depicting a touch between body-parts (i.e. an index finger touching the back of a hand) and between objects (i.e. a leaf touching a wooden stick). rTMS delivered to SI selectively reduced visual perceptual sensitivity (i.e. decreased d′ values) for detecting contralateral visual events comprising a tactile component. The SI-rTMS interference was selective in two ways – it was specific for the task, namely for discrimination of human bodily touch, as well as for the side of the touching stimuli, as it affected only the perception of the contralateral (left-sided) stimuli. Moreover, the SI disruption was evident only at the perceptual level (as assessed by d′), as no significant change in the response criterion or in the error rate emerged in the SI-rTMS session.
Notably, the SI-rTMS interference correlated with the intensity, but not with the unpleasantness, of the observed touch (i.e. the more intense the touch was rated, the greater was the visual impairment induced by SI stimulation), and with the report that the touched hand could represent the participant’s own hand (i.e. more the touched hand was rated as depicting the participant’s own hand, the greater was the SI interference). Moreover, subjects interpreted the touching and touched hands as belonging to different persons, hence representing an interpersonal (social) touch. These findings are in line with previous evidence suggesting the existence of specific relationships between the sensory qualities of the bodily touch, the embodiment of the observed sensations and the visual recruitment of somatosensory areas (e.g. Blakemore et al., 2005; Bufalari et al., 2007; Ebisch et al., 2008).
With respect to the effect of VI stimulation, the interference induced in this area did not affect visual processing of human bodily touch or object contact, in line with evidence showing that biological and non-biological moving stimuli are preferentially processed outside VI (Walsh et al., 1998; Proverbio et al., 2009).
The second experiment further explored the role of SI in the visual processing of tactile interactions between body-parts and objects. There was no SI-rTMS disruption of visual perception in the Human-to-Object Touch task or in the Object-to-Human Touch task.
Overall, the present findings indicate that SI is causally involved in the visual processing of signals pertaining only to the domain of body-parts contact, suggesting that an important factor for the mirror activation of SI is that the recipient of the touched and the touching agent are both actually capable of feeling touch. This in turn suggests that the visuo-tactile mirroring mechanism of SI does not apply to the sight of ‘any’ touch, but rather is strongly restricted to the sight of body-related experiences.
In broad agreement with this, previous studies have shown a preferential activation of SI when viewing a human touch, as compared with the sight of a no-touch event (Schaefer et al., 2005; Bolognini et al., 2011b), or with the view of an object being touched (Blakemore et al., 2005). Ebisch et al. (2008) showed a significant difference in the mirror activation of SI by the sight of intentional touch by a human agent, as compared with accidental touch by an inanimate agent. Moreover, SI activity was positively correlated with the degree of intentionality of the observed touch, as rated by the observers. However, the authors did not observe any difference in SI between animate (i.e. a hand touched the back of another hand) and inanimate (i.e. a hand touched a wooden chair) intentional touch, at odds with our findings. On the other hand, equal overlapping activation for different tactile experiences, namely intentional and accidental touch between human body-parts and/or objects, emerged in the bilateral SII (Keysers et al., 2004). This evidence has led to the proposal that the mirror activity in SI might specifically reflect an automatic simulation of the proprioceptive aspects of the observed touch when intentionality is assumed by the observer; instead, SII activation by the sight of touch seems to underpin an abstract notion of touch (Ebisch et al., 2008).
The selectivity of SI activity for touch observation is also in line with evidence in people with mirror-touch synaesthesia, the phenomenon by which watching touch to another person triggers consciously reported tactile experiences on their own body. By using a visuo-tactile interference task, it was shown that the synaesthetes were slower to report a real touch when there was simultaneously felt synaesthetic touch in another location. This effect was restricted to the sight of touch to a human body, being absent if bodies were replaced by objects, consistent with the subjective reports of synaesthetes that observed touch to an object is normally not felt (Banissy & Ward, 2007).
Other psychophysical studies have shown that seeing a body-part, but not an object, can increase the accuracy with which one can localize a tactile stimulus on that body part. It has been proposed that viewing a body-part induces a top-down visual modulation of SI activity corresponding to the viewed body-part (Kennett et al., 2001). Because the sense of touch has a close and interactive relationship with higher cognitive representations of the human body (Cardini et al., 2010; Serino & Haggard, 2010), the sight of body-parts touching each other’s, at variance with the sight of object contact, may amplify the mirror recruitment of SI.
We did not find any effect of rTMS interference over SI for the visual processing of human-to-object and/or object-to-human contacts. Different factors may explain this null result. First, there is an ‘intensity coding’ effect (Keysers et al., 2010) – the touching inanimate stimulus we used, i.e. a wooden stick, may be not enough intense to trigger SI activity, as suggested by participants’ reports (see VAS intensity). Indeed, for objects touching the body, activations in SI appears stronger when the visual stimulus suggests intense pain, such as when a needle is shown penetrating a hand deeply as opposed to pricking it, or if participants imagine that they are in a painful situation themselves (Bufalari et al., 2007; Keysers et al., 2010). The intensity of observed tactile stimulus can also modulate the intensity of the synaesthesic experience – touching the face with a knife tip or finger elicits a stronger synaesthetic sensation than using a feather (Holle et al., 2011).
Second, SI is more active when viewing hands manipulating objects (e.g. grasping a cup) (Pierno et al., 2009); given the role of SI in haptic exploration, it has been proposed that SI might be particularly important for inferring the properties of objects from the way we see other people manipulate them (Keysers et al., 2010). In this view, in our study the sight of an index finger merely touching a neutral object, without any goal-directed action, might be not sufficient to trigger a mirror engagement of SI.
Finally, the sight of a touch between human body-parts may also amplify the somatosensory activation, as compared with a touch between a body-part and an object, because SI would respond to both the observed touching and touched hands.
On a broader perspective, the somatosensory mirror system seems highly malleable, and susceptible to factors such as intensity of the stimuli, passive vs. active stimulation, intentionality, self-oriented experience, perspective-taking and attention (Fitzgibbon et al., 2011). Such modulatory factors may determine the visual recruitment of SI by touch observation.
Our second finding was the lateralization of the SI-rTMS disruptive effect, which was specific for the processing of a contralateral (to the rTMS site) bodily touch. There are two explanations for this side-effect. The first rests on the assumption that visual stimuli presented in the left hemifield should be related to contralateral, right hemisphere processing; this hemifield effect should be independent of the type (left or right) of viewed hands. The alternative interpretation is related more to ‘mirroring’ theories, as our left hemifield stimuli depicted a left hand (egocentric perspective) being touched by a left index finger (allocentric perspective), as also confirmed by subjective reports. In this view, the side-specific rTMS effect might suggest a ‘resonance’ with the experience of the person being touched. Indeed, the SI-rTMS effect correlated with the interpretation of the touched hand as depicting the observer’s own hand. Moreover, each hemisphere is more strongly activated when viewing actions conducted by a model’s contralateral hand than when viewing actions conducted by an ipsilateral hand (Aziz-Zadeh et al. 2002 and mirror activations by the sight of touch are somatotopically organized, following the sensory homunculus magnification in SI (Blakemore et al., 2005; Schaefer, et al. 2009). Even in synaesthesic patients there is often an anatomical mapping in which, for instance, the observed touch to a left cheek is felt on their left cheek and activates the right SI (Blakemore et al., 2005; Holle et al., 2011). Through this anatomical mapping, SI may convey a simulation of the precise body location at which the touch occurred, hence providing somatotopically specific representations of other people’s somatosensations. Our experimental design does not allow us to discern whether it is the view of the contralateral left-sided touch, the view of left hands or the combination of both factors (i.e. left hands in the left hemifield) that determines the lateralization of the rTMS-SI effect.
From a neurophysiological perspective, SI exhibits properties that may be relevant for visual functions related to tactile events. First, some SI neurons code for arbitrary visual–tactile associations. Animal studies have shown that SI neurons in monkeys may fire both in response to a tactile stimulus and in response to a visual stimulus that may have previously been associated with the tactile stimulus (Zhou & Fuster, 1997, 2000). This evidence suggests that the mirror activation of SI may involve a local mechanism within SI. On the other hand, the caudal part of SI features multimodal receptive fields and direct connections with multisensory regions of the posterior parietal cortex (PPC) that contain bimodal neurons that combine visual and somatosensory information. These visuo-tactile neurons respond both when the animal is touched and when observing touch to someone else on the same body part, contributing to spatial matching between the bodies of the self and others in both action recognition and imitation (Ishida et al., 2010; Keysers et al., 2010; Macaluso & Maravita, 2010). As parietal areas are thought to constitute the main source of crossmodal information for the mirror system (e.g. Keysers et al., 2010), the connectivity between SI and PPC may provide a potential substrate for the visual activation of SI by touch observation. Recent neuropsychological evidence from our lab supports this view – the sight of touch seems to affect visual perception through intra-hemispheric interactions between the visual input and the tactile input within PPC, with the tactile input probably provided by SI through a simulation process (Bolognini et al., 2011a).