Acquisition of ownership illusion with self-disownership in neurological patients

The multisensory regions in frontoparietal cortices play a crucial role in the sense of body and self. Disrupting this sense may lead to a feeling of disembodiment, or more generally, a sense of disownership. Experimentally, this altered consciousness disappears during illusory own-body perceptions, increasing the intensity of perceived ownership for an external virtual limb. In many clinical conditions, particularly in individuals with a discontinuous or absent sense of bodily awareness, the brain may effortlessly create a convincing feeling of body ownership over a surrogate body or body part. The immediate visual input dominates the current bodily state and induces rapid plastic adaptation that reconfigures the dynamics of bodily representation, allowing the brain to acquire an alternative sense of body and self. Investigating strategies to deconstruct the lack of a normal sense of bodily ownership, especially after a neurological injury, may aid the selection of appropriate clinical treatment

Interoceptive Ingredients of Body Ownership: Affective Touch and Cardiac Awareness in the Rubber Hand Illusion

This document is the Accepted Manuscript version of the following article: Laura Crucianelli, Charlotte Krahe, Paul M. Jenkinson, Aikaterini (Katerina) Fotopoulou, 'Interoceptive Ingredients of Body Ownership: Affective Touch and Cardiac Awareness in the Rubber Hand Illusion', Cortex, first published online 1 May 2017, available at doi: https://doi.org/10.1016/j.cortex.2017.04.018. © 2017 Elsevier Ltd. All rights reserved.The sense of body ownership represents a fundamental aspect of bodily self-consciousness. Using multisensory integration paradigms, recent studies have shown that both exteroceptive and interoceptive information contribute to our sense of body ownership. Interoception refers to the physiological sense of the condition of the body, including afferent signals that originate inside the body and outside the body. However, it remains unclear whether individual sensitivity to interoceptive modalities is unitary or differs between modalities. It is also unclear whether the effect of interoceptive information on body ownership is caused by exteroceptive ‘visual capture’ of these modalities, or by bottom-up processing of interoceptive information. This study aimed to test these questions in two separate samples. In the first experiment (N = 76), we examined the relationship between two different interoceptive modalities, namely cardiac awareness based on a heartbeat counting task, and affective touch perception based on stimulation of a specialized C tactile (CT) afferent system. This is an interoceptive modality of affective and social significance. In a second experiment (N = 63), we explored whether ‘off-line’ trait interoceptive sensitivity based on a heartbeat counting task would modulate the extent to which CT affective touch influences the multisensory process during the rubber hand illusion (RHI). We found that affective touch enhanced the subjective experience of body ownership during the RHI. Nevertheless, interoceptive sensitivity, as measured by a heartbeat counting task, did not modulate this effect, nor did it relate to the perception of ownership or of CT-optimal affective touch more generally. By contrast, this trait measure of interoceptive sensitivity appeared most relevant when the multisensory context of interoception was ambiguous, suggesting that the perception of interoceptive signals and their effects on body ownership may depend on individual abilities to regulate the balance of interoception and exteroception in given contexts.Peer reviewedFinal Accepted Versio

Neurophysiological correlates of the rubber hand illusion in late evoked and alpha/beta band activity

The rubber hand illusion (RHI) allows insights into how the brain resolves conflicting multisensory information regarding body position and ownership. Previous neuroimaging studies have reported a variety of neurophysiological correlates of illusory hand ownership, with conflicting results likely originating from differences in experimental parameters and control conditions. Here, we overcome these limitations by using a fully automated and precisely-timed visuo-tactile stimulation setup to record evoked responses and oscillatory responses in participants who felt the RHI. Importantly, we relied on a combination of experimental conditions to rule out confounds of attention, body-stimulus position and stimulus duration and on the combination of two control conditions to identify neurophysiological correlates of illusory hand ownership. In two separate experiments we observed a consistent illusion-related attenuation of ERPs around 330 ms over frontocentral electrodes, as well as decreases of frontal alpha and beta power during the illusion that could not be attributed to changes in attention, body-stimulus position or stimulus duration. Our results reveal neural correlates of illusory hand ownership in late and likely higher-order rather than early sensory processes, and support a role of premotor and possibly intraparietal areas in mediating illusory body ownership

Intermittent Theta Burst Stimulation Over Ventral Premotor Cortex or Inferior Parietal Lobule Does Not Enhance the Rubber Hand Illusion

An enhanced sense of prosthesis ownership may be the key for higher amputees’ quality of life. In this study in 28 healthy subjects, neuronavigated intermittent Theta Burst Stimulation (iTBS) delivered over the right ventral premotor cortex or inferior parietal lobule has been tested, compared to sham stimulation, to enhance embodiment in the rubber hand illusion paradigm. Neuromodulation of both areas did not result in an enhancement of embodiment, as assessed by the results collected from a self-evaluation questionnaire for the extent of self-attribution of the rubber hand and proprioceptive drift. In all cases, the difference between synchronous and asynchronous stroking confirms the successful induction of the illusion. It may be speculated that the low consistency of iTBS over brain regions other than primary motor cortex may account for the absence of effect, suggesting to test other neuromodulating techniques, acting on cortical networks different from the ones sensitive to iTBS to enhance artificial hand embodiment

Affective Touch Enhances Self-Face Recognition During Multisensory Integration

Multisensory integration is a powerful mechanism for constructing body awareness and key for the sense of selfhood. Recent evidence has shown that the specialised C tactile modality that gives rise to feelings of pleasant, affective touch, can enhance the experience of body ownership during multisensory integration. Nevertheless, no study has examined whether affective touch can also modulate psychological identification with our face, the hallmark of our identity. The current study used the enfacement illusion paradigm to investigate the role of affective touch in the modulation of self-face recognition during multisensory integration. In the first experiment (N = 30), healthy participants were stroked on the cheek while they were looking at another face being stroked on the cheek in synchrony or asynchrony with affective (slow; CT-optimal) vs. neutral (fast; CT-suboptimal) touch. In the second experiment (N = 38) spatial incongruence of touch (cheek vs. forehead) was used as a control condition instead of temporal asynchrony. Overall, our data suggest that CT-optimal, affective touch enhances subjective (but not behavioural) self-face recognition during synchronous and spatially congruent integration of different sensations and possibly reduces deafference during asynchronous multisensory integration. We discuss the role of affective touch in shaping the more social aspects of our self

Embodied Precision : Intranasal Oxytocin Modulates Multisensory Integration

© 2018 Massachusetts Institute of Technology.Multisensory integration processes are fundamental to our sense of self as embodied beings. Bodily illusions, such as the rubber hand illusion (RHI) and the size-weight illusion (SWI), allow us to investigate how the brain resolves conflicting multisensory evidence during perceptual inference in relation to different facets of body representation. In the RHI, synchronous tactile stimulation of a participant's hidden hand and a visible rubber hand creates illusory body ownership; in the SWI, the perceived size of the body can modulate the estimated weight of external objects. According to Bayesian models, such illusions arise as an attempt to explain the causes of multisensory perception and may reflect the attenuation of somatosensory precision, which is required to resolve perceptual hypotheses about conflicting multisensory input. Recent hypotheses propose that the precision of sensorimotor representations is determined by modulators of synaptic gain, like dopamine, acetylcholine, and oxytocin. However, these neuromodulatory hypotheses have not been tested in the context of embodied multisensory integration. The present, double-blind, placebo-controlled, crossover study ( N = 41 healthy volunteers) aimed to investigate the effect of intranasal oxytocin (IN-OT) on multisensory integration processes, tested by means of the RHI and the SWI. Results showed that IN-OT enhanced the subjective feeling of ownership in the RHI, only when synchronous tactile stimulation was involved. Furthermore, IN-OT increased an embodied version of the SWI (quantified as estimation error during a weight estimation task). These findings suggest that oxytocin might modulate processes of visuotactile multisensory integration by increasing the precision of top-down signals against bottom-up sensory input.Peer reviewedFinal Accepted Versio

The effect of intranasal oxytocin on the perception of affective touch and multisensory integration in anorexia nervosa: protocol for a double-blind placebo-controlled crossover study.

INTRODUCTION: Anorexia nervosa (AN) is an eating disorder characterised by restriction of energy intake, fears of gaining weight and related body image disturbances. The oxytocinergic system has been proposed as a pathophysiological candidate for AN. Oxytocin is a neuropeptide involved in bodily processes (eg, breast feeding) and in the onset of social behaviours (eg, bonding). Studies investigating the effect of intranasal oxytocin (IN-OT) in AN showed that it can improve attentional bias for high-calorie food and fat bodies stimuli, and related stress. However, less is known about the effect of IN-OT on bodily awareness and body image distortions, key features of the disorder linked to its development, prognosis and maintenance. Here, we aim to investigate the effect of IN-OT on the perception of affective, C-tactile-optimal touch, known to be impaired in AN and on multisensory integration processes underlying a body ownership illusion (ie, rubber hand illusion). For exploratory purposes, we will also investigate the effect of IN-OT on another interoceptive modality, namely cardiac awareness and its relationship with affective touch. DESIGN, METHODS AND ANALYSIS: Forty women with AN and forty matched healthy controls will be recruited and tested in two separate sessions; self-administering IN-OT (40 IU) or placebo, intranasally, in a pseudo-randomised manner. The data from this double-blind, placebo-controlled, cross-over study will be analysed using linear mixed models that allow the use of both fixed (treatment levels) and random (subjects) effects in the same analysis. To address our main hypotheses, separate analyses will be run for the affective touch task, where the primary outcome dependent variable will be the pleasantness of the touch, and for the rubber hand illusion, where we will investigate multisensory integration quantified as subjective embodiment towards the rubber hand. In the latter, we will manipulate the synchronicity of touch and the size of the hand. ETHICS AND DISSEMINATION: Ethics approval has been obtained by National Research Ethics Service NRES Committee London (Queen's Square Committee, ref number 14/LO/1593). The results will be disseminated through conference presentations and publication in peer-reviewed journals

Neurocognitive and Neuroplastic Mechanisms of Novel Clinical Signs in CRPS.

Complex regional pain syndrome (CRPS) is a chronic, debilitating pain condition that usually arises after trauma to a limb, but its precise etiology remains elusive. Novel clinical signs based on body perceptual disturbances have been reported, but their pathophysiological mechanisms remain poorly understood. Investigators have used functional neuroimaging techniques (including MEG, EEG, fMRI, and PET) to study changes mainly within the somatosensory and motor cortices. Here, we provide a focused review of the neuroimaging research findings that have generated insights into the potential neurocognitive and neuroplastic mechanisms underlying perceptual disturbances in CRPS. Neuroimaging findings, particularly with regard to somatosensory processing, have been promising but limited by a number of technique-specific factors (such as the complexity of neuroimaging investigations, poor spatial resolution of EEG/MEG, and use of modeling procedures that do not draw causal inferences) and more general factors including small samples sizes and poorly characterized patients. These factors have led to an underappreciation of the potential heterogeneity of pathophysiology that may underlie variable clinical presentation in CRPS. Also, until now, neurological deficits have been predominantly investigated separately from perceptual and cognitive disturbances. Here, we highlight the need to identify neurocognitive phenotypes of patients with CRPS that are underpinned by causal explanations for perceptual disturbances. We suggest that a combination of larger cohorts, patient phenotyping, the use of both high temporal, and spatial resolution neuroimaging methods, and the identification of simplified biomarkers is likely to be the most fruitful approach to identifying neurocognitive phenotypes in CRPS. Based on our review, we explain how such phenotypes could be characterized in terms of hierarchical models of perception and corresponding disturbances in recurrent processing involving the somatosensory, salience and executive brain networks. We also draw attention to complementary neurological factors that may explain some CRPS symptoms, including the possibility of central neuroinflammation and neuronal atrophy, and how these phenomena may overlap but be partially separable from neurocognitive deficits.This is the final version of the article. It first appeared from Frontiers via http://dx.doi.org/10.3389/fnhum.2016.0001

The anatomo-clinical picture of the pathological embodiment over someone else's body part after stroke

Recently, a monothematic delusion of body ownership due to brain damage (i.e., the embodiment of someone else's body part within the patient's sensorimotor system) has been extensively investigated. Here we aimed at defining in-depth the clinical features and the neural correlates of the delusion. Ninety-six stroke patients in a sub-acute or chronic phase of the illness were assessed with a full ad-hoc protocol to evaluate the embodiment of an alien arm under different conditions. A sub-group of seventy-five hemiplegic patients was also evaluated for the embodiment of the movements of the alien arm. Fifty-five patients were studied to identify the neural bases of the delusion by means of voxel-based lesion-symptom mapping approach. Our results show that, in forty percent of the whole sample, simply viewing the alien arm triggered the delusion, but only if it was a real human arm and that was seen from a 1st person perspective in an anatomically-correct position. In the hemiplegic sub-group, the presence of the embodiment of the alien arm was always accompanied by the embodiment of its passive and active movements. Furthermore, the delusion was significantly associated to primary proprioceptive deficits and to damages of the corona radiata and the superior longitudinal fasciculus. To conclude, we show that the pathological embodiment of an alien arm is well-characterized by recurrent and specific features and might be explained as a disconnection deficit, mainly involving white matter tracts. The proposed exhaustive protocol can be successfully employed to assess stroke-induced disorders of body awareness, unveiling even their more undetectable or covert clinical forms