Patterns of neural activity in the human ventral premotor cortex reflect a whole-body multisensory percept.

Previous research has shown that the integration of multisensory signals from the body in fronto-parietal association areas underlies the perception of a body part as belonging to one's physical self. What are the neural mechanisms that enable the perception of one's entire body as a unified entity? In one behavioral and one fMRI multivoxel pattern analysis experiment, we used a full-body illusion to investigate how congruent visuo-tactile signals from a single body part facilitate the emergence of the sense of ownership of the entire body. To elicit this illusion, participants viewed the body of a mannequin from the first-person perspective via head-mounted displays while synchronous touches were applied to the hand, abdomen, or leg of the bodies of the participant and the mannequin; asynchronous visuo-tactile stimuli served as controls. The psychometric data indicated that the participants perceived ownership of the entire artificial body regardless of the body segment that received the synchronous visuo-tactile stimuli. Based on multivoxel pattern analysis, we found that the neural responses in the left ventral premotor cortex displayed illusion-specific activity patterns that generalized across all tested pairs of body parts. Crucially, a tripartite generalization analysis revealed the whole-body specificity of these premotor activity patterns. Finally, we also identified multivoxel patterns in the premotor, intraparietal, and lateral occipital cortices and in the putamen that reflected multisensory responses specific to individual body parts. Based on these results, we propose that the dynamic formation of a whole-body percept may be mediated by neuronal populations in the ventral premotor cortex that contain visuo-tactile receptive fields encompassing multiple body segments.

Rubber hands feel touch, but not in blind individuals.

Psychology and neuroscience have a long-standing tradition of studying blind individuals to investigate how visual experience shapes perception of the external world. Here, we study how blind people experience their own body by exposing them to a multisensory body illusion: the somatic rubber hand illusion. In this illusion, healthy blindfolded participants experience that they are touching their own right hand with their left index finger, when in fact they are touching a rubber hand with their left index finger while the experimenter touches their right hand in a synchronized manner (Ehrsson et al. 2005). We compared the strength of this illusion in a group of blind individuals (n = 10), all of whom had experienced severe visual impairment or complete blindness from birth, and a group of age-matched blindfolded sighted participants (n = 12). The illusion was quantified subjectively using questionnaires and behaviorally by asking participants to point to the felt location of the right hand. The results showed that the sighted participants experienced a strong illusion, whereas the blind participants experienced no illusion at all, a difference that was evident in both tests employed. A further experiment testing the participants' basic ability to localize the right hand in space without vision (proprioception) revealed no difference between the two groups. Taken together, these results suggest that blind individuals with impaired visual development have a more veridical percept of self-touch and a less flexible and dynamic representation of their own body in space compared to sighted individuals. We speculate that the multisensory brain systems that re-map somatosensory signals onto external reference frames are less developed in blind individuals and therefore do not allow efficient fusion of tactile and proprioceptive signals from the two upper limbs into a single illusory experience of self-touch as in sighted individuals.

No pain relief with the rubber hand illusion.

The sense of body ownership can be easily disrupted during illusions and the most common illusion is the rubber hand illusion. An idea that is rapidly gaining popularity in clinical pain medicine is that body ownership illusions can be used to modify pathological pain sensations and induce analgesia. However, this idea has not been empirically evaluated. Two separate research laboratories undertook independent randomized repeated measures experiments, both designed to detect an effect of the rubber hand illusion on experimentally induced hand pain. In Experiment 1, 16 healthy volunteers rated the pain evoked by noxious heat stimuli (5 s duration; interstimulus interval 25 s) of set temperatures (47°, 48° and 49°C) during the rubber hand illusion or during a control condition. There was a main effect of stimulus temperature on pain ratings, but no main effect of condition (p = 0.32), nor a condition x temperature interaction (p = 0.31). In Experiment 2, 20 healthy volunteers underwent quantitative sensory testing to determine heat and cold pain thresholds during the rubber hand illusion or during a control condition. Secondary analyses involved heat and cold detection thresholds and paradoxical heat sensations. Again, there was no main effect of condition on heat pain threshold (p = 0.17), nor on cold pain threshold (p = 0.65), nor on any of the secondary measures (p<0.56 for all). We conclude that the rubber hand illusion does not induce analgesia.

The perspective matters! Multisensory integration in ego-centric reference frames determines full-body ownership.

Recent advances in experimental science have made it possible to investigate the perceptual processes involved in generating a sense of owning an entire body. This is achieved by full-body ownership illusions which make use of specific patterns of visual and somatic stimuli integration. Here we investigate the fundamental question of the reference frames used in the process of attributing an entire body to the self. We quantified the strength of the body-swap illusion in conditions where the participants were observing this artificial body from the perspective of the first or third person. Consistent results from subjective reports and physiological recordings show that the first person visual perspective is critical for the induction of this full-body ownership illusion. This demonstrates that the multisensory integration processes producing the sense of corporeal self operates in an ego-centric reference frame.

FMRI adaptation reveals a cortical mechanism for the coding of space near the hand.

Behavioral studies in humans and electrophysiological recordings in nonhuman primates have suggested the existence of a specific representation of the space immediately surrounding the body. In macaques, neurons that have visual receptive fields limited to a region of space close around a body part have been found in premotor and parietal areas. These cells are hypothesized to encode the location of external objects in coordinate systems that are centered on individual body parts. In the present study, we used an fMRI adaptation paradigm on healthy participants to reveal areas in the anterior part of the intraparietal sulcus, the inferior parietal lobe (supramarginal gyrus), and the dorsal and ventral portions of the premotor cortex that exhibit selective BOLD adaptation to an object moving near the right hand. Crucially, these areas did not manifest adaptation if the stimulus was presented in far space (100 cm) or when the hand was retracted from the object. This hand-centered selectivity could not be detected when a traditional fMRI analysis approach was used. These findings are important as they provide the most conclusive neuroimaging evidence to date for a representation of near-personal space in the human brain. They also demonstrate a selective mechanism implemented by human perihand neurons in the premotor and posterior parietal areas and add to earlier findings from humans and nonhuman primates.

From part- to whole-body ownership in the multisensory brain.

The question of how we experience ownership of an entire body distinct from the external world is a fundamental problem in psychology and neuroscience [1-6]. Earlier studies suggest that integration of visual, tactile, and proprioceptive information in multisensory areas [7-11] mediates self-attribution of single limbs. However, it is still unknown how ownership of individual body parts translates into the unitary experience of owning a whole body. Here, we used a "body-swap" illusion [12], in which people experienced an artificial body to be their own, in combination with functional magnetic resonance imaging to reveal a coupling between the experience of full-body ownership and neural responses in bilateral ventral premotor and left intraparietal cortices, and left putamen. Importantly, activity in the ventral premotor cortex reflected the construction of ownership of a whole body from the parts, because it was stronger when the stimulated body part was attached to a body, was present irrespective of whether the illusion was triggered by stimulation of the hand or the abdomen, and displayed multivoxel patterns carrying information about full-body ownership. These findings suggest that the unitary experience of owning an entire body is produced by neuronal populations that integrate multisensory information across body segments.

The illusion of owning a third arm.

Could it be possible that, in the not-so-distant future, we will be able to reshape the human body so as to have extra limbs? A third arm helping us out with the weekly shopping in the local grocery store, or an extra artificial limb assisting a paralysed person? Here we report a perceptual illusion in which a rubber right hand, placed beside the real hand in full view of the participant, is perceived as a supernumerary limb belonging to the participant's own body. This effect was supported by questionnaire data in conjunction with physiological evidence obtained from skin conductance responses when physically threatening either the rubber hand or the real one. In four well-controlled experiments, we demonstrate the minimal required conditions for the elicitation of this "supernumerary hand illusion". In the fifth, and final experiment, we show that the illusion reported here is qualitatively different from the traditional rubber hand illusion as it is characterised by less disownership of the real hand and a stronger feeling of having two right hands. These results suggest that the artificial hand 'borrows' some of the multisensory processes that represent the real hand, leading to duplication of touch and ownership of two right arms. This work represents a major advance because it challenges the traditional view of the gross morphology of the human body as a fundamental constraint on what we can come to experience as our physical self, by showing that the body representation can easily be updated to incorporate an additional limb.

Integration of visual and tactile signals from the hand in the human brain: an FMRI study.

In the non-human primate brain, a number of multisensory areas have been described where individual neurons respond to visual, tactile and bimodal visuotactile stimulation of the upper limb. It has been shown that such bimodal neurons can integrate sensory inputs in a linear or nonlinear fashion. In humans, activity in a similar set of brain regions has been associated with visuotactile stimulation of the hand. However, little is known about how these areas integrate visual and tactile information. In this functional magnetic resonance imaging experiment, we employed tactile, visual, and visuotactile stimulation of the right hand in an ecologically valid setup where participants were looking directly at their upper limb. We identified brain regions that were activated by both visual and tactile stimuli as well as areas exhibiting greater activity in the visuotactile condition than in both unisensory ones. The posterior and inferior parietal, dorsal, and ventral premotor cortices, as well as the cerebellum, all showed evidence of multisensory linear (additive) responses. Nonlinear, superadditive responses were observed in the cortex lining the left anterior intraparietal sulcus, the insula, dorsal premotor cortex, and, subcortically, the putamen. These results identify a set of candidate frontal, parietal and subcortical regions that integrate visual and tactile information for the multisensory perception of one's own hand.

When right feels left: referral of touch and ownership between the hands.

Feeling touch on a body part is paradigmatically considered to require stimulation of tactile afferents from the body part in question, at least in healthy non-synaesthetic individuals. In contrast to this view, we report a perceptual illusion where people experience "phantom touches" on a right rubber hand when they see it brushed simultaneously with brushes applied to their left hand. Such illusory duplication and transfer of touch from the left to the right hand was only elicited when a homologous (i.e., left and right) pair of hands was brushed in synchrony for an extended period of time. This stimulation caused the majority of our participants to perceive the right rubber hand as their own and to sense two distinct touches--one located on the right rubber hand and the other on their left (stimulated) hand. This effect was supported by quantitative subjective reports in the form of questionnaires, behavioral data from a task in which participants pointed to the felt location of their right hand, and physiological evidence obtained by skin conductance responses when threatening the model hand. Our findings suggest that visual information augments subthreshold somatosensory responses in the ipsilateral hemisphere, thus producing a tactile experience from the non-stimulated body part. This finding is important because it reveals a new bilateral multisensory mechanism for tactile perception and limb ownership.

If I were you: perceptual illusion of body swapping.

The concept of an individual swapping his or her body with that of another person has captured the imagination of writers and artists for decades. Although this topic has not been the subject of investigation in science, it exemplifies the fundamental question of why we have an ongoing experience of being located inside our bodies. Here we report a perceptual illusion of body-swapping that addresses directly this issue. Manipulation of the visual perspective, in combination with the receipt of correlated multisensory information from the body was sufficient to trigger the illusion that another person's body or an artificial body was one's own. This effect was so strong that people could experience being in another person's body when facing their own body and shaking hands with it. Our results are of fundamental importance because they identify the perceptual processes that produce the feeling of ownership of one's body.