Neural Substrates of Body Ownership and Agency during Voluntary Movement.

Body ownership and the sense of agency are two central aspects of bodily self-consciousness. While multiple neuroimaging studies have investigated the neural correlates of body ownership and agency separately, few studies have investigated the relationship between these two aspects during voluntary movement when such experiences naturally combine. By eliciting the moving rubber hand illusion with active or passive finger movements during functional magnetic resonance imaging, we isolated activations reflecting the sense of body ownership and agency, respectively, as well as their interaction, and assessed their overlap and anatomic segregation. We found that perceived hand ownership was associated with activity in premotor, posterior parietal, and cerebellar regions, whereas the sense of agency over the movements of the hand was related to activity in the dorsal premotor cortex and superior temporal cortex. Moreover, one section of the dorsal premotor cortex showed overlapping activity for ownership and agency, and somatosensory cortical activity reflected the interaction of ownership and agency with higher activity when both agency and ownership were experienced. We further found that activations previously attributed to agency in the left insular cortex and right temporoparietal junction reflected the synchrony or asynchrony of visuoproprioceptive stimuli rather than agency. Collectively, these results reveal the neural bases of agency and ownership during voluntary movement. Although the neural representations of these two experiences are largely distinct, there are interactions and functional neuroanatomical overlap during their combination, which has bearing on theories on bodily self-consciousness.SIGNIFICANCE STATEMENT How does the brain generate the sense of being in control of bodily movement (agency) and the sense that body parts belong to one's body (body ownership)? Using fMRI and a bodily illusion triggered by movement, we found that agency is associated with activity in premotor cortex and temporal cortex, and body ownership with activity in premotor, posterior parietal, and cerebellar regions. The activations reflecting the two sensations were largely distinct, but there was overlap in premotor cortex and an interaction in somatosensory cortex. These findings advance our understanding of the neural bases of and interplay between agency and body ownership during voluntary movement, which has implications for the development of advanced controllable prosthetic limbs that feel like real limbs.

Right temporoparietal junction encodes inferred visual knowledge of others.

When people make inferences about other people's minds, called theory of mind (ToM), a cortical network becomes active. The right temporoparietal junction (TPJ) is one of the most consistently responsive nodes in that network. Here we used a pictorial, reaction-time, ToM task to study brain activity in the TPJ and other cortical areas. Subjects were asked to take the perspective of a cartoon character and judge its knowledge of a visual display in front of it. The right TPJ showed evidence of encoding information about the implied visual knowledge of the cartoon head. When the subject was led to believe that the head could see a visual change take place, activity in the right TPJ significantly reflected that change. When the head could apparently not see the same visual change take place, activity in the right TPJ no longer significantly reflected that change. The subject could see the change in all cases; the critical factor that affected TPJ activity was whether the subject was led to think the cartoon character could see the change. We also found that whether the beliefs attributed to the cartoon head were true or false did not significantly affect activity in the present paradigm. These results suggest that the right TPJ may play a role in modeling the contents of the minds of others, perhaps more than it participates in evaluating the truth or falsity of that content.

Attention, awareness, and the right temporoparietal junction.

The attention schema theory posits a specific relationship between subjective awareness and attention, in which awareness is the control model that the brain uses to aid in the endogenous control of attention. In previous experiments, we developed a behavioral paradigm in human subjects to manipulate awareness and attention. The paradigm involved a visual cue that could be used to guide attention to a target stimulus. In task 1, subjects were aware of the cue, but not aware that it provided information about the target. The cue measurably drew exogenous attention to itself. In addition, implicitly, the subjects' endogenous attention mechanism used the cue to help shift attention to the target. In task 2, subjects were no longer aware of the cue. The cue still measurably drew exogenous attention to itself, yet without awareness of the cue, the subjects' endogenous control mechanism was no longer able to use the cue to control attention. Thus, the control of attention depended on awareness. Here, we tested the two tasks while scanning brain activity in human volunteers. We predicted that the right temporoparietal junction (TPJ) would be active in relation to the process in which awareness helps control attention. This prediction was confirmed. The right TPJ was active in relation to the effect of the cue on attention in task 1; it was not measurably active in task 2. The difference was significant. In our interpretation, the right TPJ is involved in an interaction in which awareness permits the control of attention.

Temporo-parietal cortex involved in modeling one's own and others' attention.

In a traditional view, in social cognition, attention is equated with gaze and people track other people's attention by tracking their gaze. Here, we used fMRI to test whether the brain represents attention in a richer manner. People read stories describing an agent (either oneself or someone else) directing attention to an object in one of two ways: either internally directed (endogenous) or externally induced (exogenous). We used multivoxel pattern analysis to examine how brain areas within the theory-of-mind network encoded attention type and agent type. Brain activity patterns in the left temporo-parietal junction (TPJ) showed significant decoding of information about endogenous versus exogenous attention. The left TPJ, left superior temporal sulcus (STS), precuneus, and medial prefrontal cortex (MPFC) significantly decoded agent type (self versus other). These findings show that the brain constructs a rich model of one's own and others' attentional state, possibly aiding theory of mind.

Visual motion assists in social cognition.

Recent evidence suggests a link between visual motion processing and social cognition. When person A watches person B, the brain of A apparently generates a fictitious, subthreshold motion signal streaming from B to the object of B's attention. These previous studies, being correlative, were unable to establish any functional role for the false motion signals. Here, we directly tested whether subthreshold motion processing plays a role in judging the attention of others. We asked, if we contaminate people's visual input with a subthreshold motion signal streaming from an agent to an object, can we manipulate people's judgments about that agent's attention? Participants viewed a display including faces, objects, and a subthreshold motion hidden in the background. Participants' judgments of the attentional state of the faces was significantly altered by the hidden motion signal. Faces from which subthreshold motion was streaming toward an object were judged as paying more attention to the object. Control experiments showed the effect was specific to the agent-to-object motion direction and to judging attention, not action or spatial orientation. These results suggest that when the brain models other minds, it uses a subthreshold motion signal, streaming from an individual to an object, to help represent attentional state. This type of social-cognitive model, tapping perceptual mechanisms that evolved to process physical events in the real world, may help to explain the extraordinary cultural persistence of beliefs in mind processes having physical manifestation. These findings, therefore, may have larger implications for human psychology and cultural belief.

Other people's gaze encoded as implied motion in the human brain.

Keeping track of other people's gaze is an essential task in social cognition and key for successfully reading other people's intentions and beliefs (theory of mind). Recent behavioral evidence suggests that we construct an implicit model of other people's gaze, which may incorporate physically incoherent attributes such as a construct of force-carrying beams that emanate from the eyes. Here, we used functional magnetic resonance imaging and multivoxel pattern analysis to test the prediction that the brain encodes gaze as implied motion streaming from an agent toward a gazed-upon object. We found that a classifier, trained to discriminate the direction of visual motion, significantly decoded the gaze direction in static images depicting a sighted face, but not a blindfolded one, from brain activity patterns in the human motion-sensitive middle temporal complex (MT+) and temporo-parietal junction (TPJ). Our results demonstrate a link between the visual motion system and social brain mechanisms, in which the TPJ, a key node in theory of mind, works in concert with MT+ to encode gaze as implied motion. This model may be a fundamental aspect of social cognition that allows us to efficiently connect agents with the objects of their attention. It is as if the brain draws a quick visual sketch with moving arrows to help keep track of who is attending to what. This implicit, fluid-flow model of other people's gaze may help explain culturally universal myths about the mind as an energy-like, flowing essence.

Implied motion as a possible mechanism for encoding other people's attention.

Recent evidence suggests that the human brain automatically constructs a rich model of other people's attention, beyond registering low-level cues such as someone else's gaze direction. This model is not a physically accurate representation of attention, but instead appears to contain simplifying and physically incoherent features. For example, without explicitly realizing it, people treat the attentive gaze of others as though it exerts a gentle force pushing on objects. Here we specify another aspect of that implicit model of attention. People treat the attentive gaze of an agent as though it were travelling through space, with an implied motion encoded literally enough that it causes a perceptual motion adaptation effect. This implicit model of other people's attention may facilitate the process of keeping track of who is attending to what, which is essential for reading and predicting the minds and behavior of social agents. This implicit model of attention may also have shaped culturally widespread ideas about mind and spirit.

Duplication of the bodily self: a perceptual illusion of dual full-body ownership and dual self-location.

Previous research has shown that it is possible to use multisensory stimulation to induce the perceptual illusion of owning supernumerary limbs, such as two right arms. However, it remains unclear whether the coherent feeling of owning a full-body may be duplicated in the same manner and whether such a dual full-body illusion could be used to split the unitary sense of self-location into two. Here, we examined whether healthy human participants can experience simultaneous ownership of two full-bodies, located either close in parallel or in two separate spatial locations. A previously described full-body illusion, based on visuo-tactile stimulation of an artificial body viewed from the first-person perspective (1PP) via head-mounted displays, was adapted to a dual-body setting and quantified in five experiments using questionnaires, a behavioural self-location task and threat-evoked skin conductance responses. The results of experiments 1-3 showed that synchronous visuo-tactile stimulation of two bodies viewed from the 1PP lying in parallel next to each other induced a significant illusion of dual full-body ownership. In experiment 4, we failed to find support for our working hypothesis that splitting the visual scene into two, so that each of the two illusory bodies was placed in distinct spatial environments, would lead to dual self-location. In a final exploratory experiment (no. 5), we found preliminary support for an illusion of dual self-location and dual body ownership by using dynamic changes between the 1PPs of two artificial bodies and/or a common third-person perspective in the ceiling of the testing room. These findings suggest that healthy people, under certain conditions of multisensory perceptual ambiguity, may experience dual body ownership and dual self-location. These findings suggest that the coherent sense of the bodily self located at a single place in space is the result of an active and dynamic perceptual integration process.

Toward a standard model of consciousness: Reconciling the attention schema, global workspace, higher-order thought, and illusionist theories.

Here we examine how people's understanding of consciousness may have been shaped by an implicit theory of mind. This social cognition approach may help to make sense of an apparent divide between the physically incoherent consciousness we think we have and the complex, rich, but mechanistic consciousness we may actually have. We suggest this approach helps reconcile some of the current cognitive neuroscience theories of consciousness. We argue that a single, coherent explanation of consciousness is available and has been for some time, encompassing the views of many researchers, but is not yet recognized. It is obscured partly by terminological differences, and partly because researchers view isolated pieces of it as rival theories. It may be time to recognize that a deeper, coherent pool of ideas, a kind of standard model, is available to explain multiple layers of consciousness and how they relate to specific networks within the brain.

Multisensory correlations-Not tactile expectations-Determine the sense of body ownership.

Can the mere expectation of a sensory event being about to occur on an artificial limb be sufficient to elicit an illusory sense of ownership over said limb? This issue is currently under debate and studies using two different paradigms have presented conflicting results. Here, we employed the two relevant paradigms, namely, the magnetic touch illusion and the "tactile expectation" version of the rubber hand illusion, to clarify the role of tactile expectations in the process of attributing ownership to limbs. The illusory senses of ownership and 'magnetic touch' were quantified using questionnaires, threat-evoked skin conductance responses and a combination of motion tracking synchronized with real-time subjective ratings and skin conductance. The results showed that the magnetic touch illusion was dependent on concurrent visual and tactile stimulation and that visually induced tactile expectations alone were insufficient. Moreover, in this study, tactile expectations were not associated with the rubber hand illusion, neither in terms of subjective ratings nor skin conductance changes. Together, these findings contradict the notion that the brain uses predictions of upcoming sensory events to determine whether or not a limb belongs to the self, and, instead, emphasize the importance of correlated multisensory information.

Direct Electrophysiological Correlates of Body Ownership in Human Cerebral Cortex.

Over the past decade, numerous neuroimaging studies based on hemodynamic markers of brain activity have examined the feeling of body ownership using perceptual body-illusions in humans. However, the direct electrophysiological correlates of body ownership at the cortical level remain unexplored. To address this, we studied the rubber hand illusion in 5 patients (3 males and 2 females) implanted with intracranial electrodes measuring cortical surface potentials. Increased high-γ (70-200 Hz) activity, an index of neuronal firing rate, in premotor and intraparietal cortices reflected the feeling of ownership. In both areas, high-γ increases were intimately coupled with the subjective illusion onset and sustained both during and in-between touches. However, intraparietal activity was modulated by tactile stimulation to a higher degree than the premotor cortex through effective connectivity with the hand-somatosensory cortex, which suggests different functional roles. These findings constitute the first intracranial electrophysiological characterization of the rubber hand illusion and extend our understanding of the dynamic mechanisms of body ownership.

Implicit model of other people's visual attention as an invisible, force-carrying beam projecting from the eyes.

As a part of social cognition, people automatically construct rich models of other people's vision. Here we show that when people judge the mechanical forces acting on an object, their judgments are biased by another person gazing at the object. The bias is consistent with an implicit perception that gaze adds a gentle force, pushing on the object. The bias was present even though the participants were not explicitly aware of it and claimed that they did not believe in an extramission view of vision (a common folk view of vision in which the eyes emit an invisible energy). A similar result was not obtained on control trials when participants saw a blindfolded face turned toward the object, or a face with open eyes turned away from the object. The findings suggest that people automatically and implicitly generate a model of other people's vision that uses the simplifying construct of beams coming out of the eyes. This implicit model of active gaze may be a hidden, yet fundamental, part of the rich process of social cognition, contributing to how we perceive visual agency. It may also help explain the extraordinary cultural persistence of the extramission myth of vision.

Tool use changes the spatial extension of the magnetic touch illusion.

Characterizing the brain mechanisms that allow humans to use tools to interact with the environment is a major goal in neuroscience. It has been proposed that handheld tools are incorporated into the multisensory representation of the body and its surrounding (peripersonal) space, underlying our remarkable tool use ability. One single-cell recording study in tool-using monkeys provided qualitative support for this hypothesis, and the results from a vast number of human studies employing different experimental paradigms have been ambiguous. Here, we made use of the recently reported magnetic touch illusion-a perceptual correlate of peripersonal space-to examine the effect of tool use on the representation of visuotactile peripersonal space. The results showed that active tool use leads to an extension of the "illusion volume" around the entire length of a tool, which was significantly greater compared with a manual control task. These findings support the notion that the multisensory representation of peripersonal space is extended to incorporate handheld tools and provide a three-dimensional estimation of this remapping process. (PsycINFO Database Record

Ownership of an artificial limb induced by electrical brain stimulation.

Replacing the function of a missing or paralyzed limb with a prosthetic device that acts and feels like one's own limb is a major goal in applied neuroscience. Recent studies in nonhuman primates have shown that motor control and sensory feedback can be achieved by connecting sensors in a robotic arm to electrodes implanted in the brain. However, it remains unknown whether electrical brain stimulation can be used to create a sense of ownership of an artificial limb. In this study on two human subjects, we show that ownership of an artificial hand can be induced via the electrical stimulation of the hand section of the somatosensory (SI) cortex in synchrony with touches applied to a rubber hand. Importantly, the illusion was not elicited when the electrical stimulation was delivered asynchronously or to a portion of the SI cortex representing a body part other than the hand, suggesting that multisensory integration according to basic spatial and temporal congruence rules is the underlying mechanism of the illusion. These findings show that the brain is capable of integrating "natural" visual input and direct cortical-somatosensory stimulation to create the multisensory perception that an artificial limb belongs to one's own body. Thus, they serve as a proof of concept that electrical brain stimulation can be used to "bypass" the peripheral nervous system to induce multisensory illusions and ownership of artificial body parts, which has important implications for patients who lack peripheral sensory input due to spinal cord or nerve lesions.

The magnetic touch illusion: A perceptual correlate of visuo-tactile integration in peripersonal space.

To accurately localize our limbs and guide movements toward external objects, the brain must represent the body and its surrounding (peripersonal) visual space. Specific multisensory neurons encode peripersonal space in the monkey brain, and neurobehavioral studies have suggested the existence of a similar representation in humans. However, because peripersonal space lacks a distinct perceptual correlate, its involvement in spatial and bodily perception remains unclear. Here, we show that applying brushstrokes in mid-air at some distance above a rubber hand-without touching it-in synchrony with brushstrokes applied to a participant's hidden real hand results in the illusory sensation of a "magnetic force" between the brush and the rubber hand, which strongly correlates with the perception of the rubber hand as one's own. In eight experiments, we characterized this "magnetic touch illusion" by using quantitative subjective reports, motion tracking, and behavioral data consisting of pointing errors toward the rubber hand in an intermanual pointing task. We found that the illusion depends on visuo-tactile synchrony and exhibits similarities with the visuo-tactile receptive field properties of peripersonal space neurons, featuring a non-linear decay at 40cm that is independent of gaze direction and follows changes in the rubber hand position. Moreover, the "magnetic force" does not penetrate physical barriers, thus further linking this phenomenon to body-specific visuo-tactile integration processes. These findings provide strong support for the notion that multisensory integration within peripersonal space underlies bodily self-attribution. Furthermore, we propose that the magnetic touch illusion constitutes a perceptual correlate of visuo-tactile integration in peripersonal space.

Decoding illusory self-location from activity in the human hippocampus.

Decades of research have demonstrated a role for the hippocampus in spatial navigation and episodic and spatial memory. However, empirical evidence linking hippocampal activity to the perceptual experience of being physically located at a particular place in the environment is lacking. In this study, we used a multisensory out-of-body illusion to perceptually 'teleport' six healthy participants between two different locations in the scanner room during high-resolution functional magnetic resonance imaging (fMRI). The participants were fitted with MRI-compatible head-mounted displays that changed their first-person visual perspective to that of a pair of cameras placed in one of two corners of the scanner room. To elicit the illusion of being physically located in this position, we delivered synchronous visuo-tactile stimulation in the form of an object moving toward the cameras coupled with touches applied to the participant's chest. Asynchronous visuo-tactile stimulation did not induce the illusion and served as a control condition. We found that illusory self-location could be successfully decoded from patterns of activity in the hippocampus in all of the participants in the synchronous (P < 0.05) but not in the asynchronous condition (P > 0.05). At the group-level, the decoding accuracy was significantly higher in the synchronous than in the asynchronous condition (P = 0.012). These findings associate hippocampal activity with the perceived location of the bodily self in space, which suggests that the human hippocampus is involved not only in spatial navigation and memory but also in the construction of our sense of bodily self-location.

Posterior cingulate cortex integrates the senses of self-location and body ownership.

The senses of owning a body and being localized somewhere in space are two key components of human self-consciousness. Despite a wealth of neurophysiological and neuroimaging research on the representations of the spatial environment in the parietal and medial temporal cortices, the relationship between body ownership and self-location remains unexplored. To investigate this relationship, we used a multisensory out-of-body illusion to manipulate healthy participants' perceived self-location, head direction, and sense of body ownership during high-resolution fMRI. Activity patterns in the hippocampus and the posterior cingulate, retrosplenial, and intraparietal cortices reflected the sense of self-location, whereas the sense of body ownership was associated with premotor-intraparietal activity. The functional interplay between these two sets of areas was mediated by the posterior cingulate cortex. These results extend our understanding of the role of the posterior parietal and medial temporal cortices in spatial cognition by demonstrating that these areas not only are important for ecological behaviors, such as navigation and perspective taking, but also support the perceptual representation of the bodily self in space. Our results further suggest that the posterior cingulate cortex has a key role in integrating the neural representations of self-location and body ownership.

Illusory ownership of an invisible body reduces autonomic and subjective social anxiety responses.

What is it like to be invisible? This question has long fascinated man and has been the central theme of many classic literary works. Recent advances in materials science suggest that invisibility cloaking of the human body may be possible in the not-so-distant future. However, it remains unknown how invisibility affects body perception and embodied cognition. To address these questions, we developed a perceptual illusion of having an entire invisible body. Through a series of experiments, we characterized the multisensory rules that govern the elicitation of the illusion and show that the experience of having an invisible body reduces the social anxiety response to standing in front of an audience. This study provides an experimental model of what it is like to be invisible and shows that this experience affects bodily self-perception and social cognition.

Disintegration of multisensory signals from the real hand reduces default limb self-attribution: an fMRI study.

The perception of our limbs in space is built upon the integration of visual, tactile, and proprioceptive signals. Accumulating evidence suggests that these signals are combined in areas of premotor, parietal, and cerebellar cortices. However, it remains to be determined whether neuronal populations in these areas integrate hand signals according to basic temporal and spatial congruence principles of multisensory integration. Here, we developed a setup based on advanced 3D video technology that allowed us to manipulate the spatiotemporal relationships of visuotactile (VT) stimuli delivered on a healthy human participant's real hand during fMRI and investigate the ensuing neural and perceptual correlates. Our experiments revealed two novel findings. First, we found responses in premotor, parietal, and cerebellar regions that were dependent upon the spatial and temporal congruence of VT stimuli. This multisensory integration effect required a simultaneous match between the seen and felt postures of the hand, which suggests that congruent visuoproprioceptive signals from the upper limb are essential for successful VT integration. Second, we observed that multisensory conflicts significantly disrupted the default feeling of ownership of the seen real limb, as indexed by complementary subjective, psychophysiological, and BOLD measures. The degree to which self-attribution was impaired could be predicted from the attenuation of neural responses in key multisensory areas. These results elucidate the neural bases of the integration of multisensory hand signals according to basic spatiotemporal principles and demonstrate that the disintegration of these signals leads to "disownership" of the seen real hand.