Dynamic causal modeling of touch-evoked potentials in the rubber hand illusion

The neural substrate of bodily ownership can be disclosed by the rubber hand illusion (RHI); namely, the illusory self-attribution of an artificial hand that is induced by synchronous tactile stimulation of the subject's hand that is hidden from view. Previous studies have pointed to the premotor cortex (PMC) as a pivotal area in such illusions. To investigate the effective connectivity between – and within – sensory and premotor areas involved in bodily perceptions, we used dynamic causal modeling of touch-evoked responses in 13 healthy subjects. Each subject's right hand was stroked while viewing their own hand (“REAL”), or an artificial hand presented in an anatomically plausible (“CONGRUENT”) or implausible (“INCONGRUENT”) position. Bayesian model comparison revealed strong evidence for a differential involvement of the PMC in the generation of touch-evoked responses under the three conditions, confirming a crucial role of PMC in bodily self-attribution. In brief, the extrinsic (forward) connection from left occipital cortex to left PMC was stronger for CONGRUENT and INCONGRUENT as compared to REAL, reflecting the augmentation of bottom-up visual input when multisensory integration is challenged. Crucially, intrinsic connectivity in the primary somatosensory cortex (S1) was attenuated in the CONGRUENT condition, during the illusory percept. These findings support predictive coding models of the functional architecture of multisensory integration (and attenuation) in bodily perceptual experience

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

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

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

From rubber hands to neuroprosthetics: Neural correlates of embodiment

© 2023 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/)Our interaction with the world rests on the knowledge that we are a body in space and time, which can interact with the environment. This awareness is usually referred to as sense of embodiment. For the good part of the past 30 years, the rubber hand illusion (RHI) has been a prime tool to study embodiment in healthy and people with a variety of clinical conditions. In this paper, we provide a critical overview of this research with a focus on the RHI paradigm as a tool to study prothesis embodiment in individuals with amputation. The RHI relies on well-documented multisensory integration mechanisms based on sensory precision, where parietal areas are involved in resolving the visuo-tactile conflict, and premotor areas in updating the conscious bodily representation. This mechanism may be transferable to prosthesis ownership in amputees. We discuss how these results might transfer to technological development of sensorised prostheses, which in turn might progress the acceptability by users.Peer reviewe

Drifting perceptual patterns suggest prediction errors fusion rather than hypothesis selection: replicating the rubber-hand illusion on a robot

Humans can experience fake body parts as theirs just by simple visuo-tactile synchronous stimulation. This body-illusion is accompanied by a drift in the perception of the real limb towards the fake limb, suggesting an update of body estimation resulting from stimulation. This work compares body limb drifting patterns of human participants, in a rubber hand illusion experiment, with the end-effector estimation displacement of a multisensory robotic arm enabled with predictive processing perception. Results show similar drifting patterns in both human and robot experiments, and they also suggest that the perceptual drift is due to prediction error fusion, rather than hypothesis selection. We present body inference through prediction error minimization as one single process that unites predictive coding and causal inference and that it is responsible for the effects in perception when we are subjected to intermodal sensory perturbations.Comment: Proceedings of the 2018 IEEE International Conference on Development and Learning and Epigenetic Robotic

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 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

The neurophysiological correlates of illusory hand ownership

The rubber hand illusion has been established as one of the most important tools in the quest for understanding body ownership. Such understanding may be vital to neuro-rehabilitative and neurosurgical therapies that aim to modulate this phenomenon. Numerous brain imaging and TMS studies indicate that a wide ranging network of brain areas is associated with illusory hand ownership in the RHI. However, while we have a good idea of where neural activity related to the RHI occurs, the question of how these networks interact on the temporal basis is still rather unexplored as the few EEG studies that have investigated this question have relied on problematic stimulation methods or have failed to induce a strong sense of illusion in participants. Avoiding these limitations the experiments in this thesis provide insights into the temporal dynamics of body ownership in the brain. Experiment One (presented in Chapter Three) focussed on establishing that the purpose-built, automated setup induced the Rubber Hand Illusion reliably as measured by proprioceptive drift measurements and questionnaire ratings. The evoked visual and tactile responses elicited by the setup were identified and timing and intensity of illusory hand ownership were found to be comparable to the existing literature. The results of this experiment provided guidance regarding necessary adjustments to the RHI setup for the following experiments in order to avoid confounds induced by avoidable differences between conditions. Experiment Two (presented in Chapter Four) used a setup adjusted according to the findings of Experiment One and recorded evoked responses and oscillatory responses in participants who felt the rubber hand illusion. A combination of experimental conditions was applied to rule out confounds of attention and body-stimulus position. In addition two control conditions were applied to reveal the neural correlates of illusory hand ownership. The experiment revealed a reduction of alpha and beta power as well as an attenuation of evoked responses around 330 ms over central electrodes associated with illusory hand ownership. Also, the results indicate that body-stimulus processing and illusion processing as measured by evoked potentials might emanate from the same cortical network. Experiment Three (presented in Chapter Four) tested if the findings of the second experiment in regard to illusion effects were robust against changes in stimulus duration. The reduction in alpha and beta power and the attenuation of evoked responses at 330 ms were found to be robust against changes in stimulus duration. Together with the results from Experiment Two, these findings provide the first EEG marker of illusion related activity in the RHI induced by an automated setup with varying stimuli length. Experiment four (presented in Chapter Five) investigated if the neural correlates identified in the Experiment Two and Experiment Three were indeed related to the feeling of illusory hand ownership in the RHI and not to a mere remapping of visual receptive fields. To test this, evoked and oscillatory responses were recorded during the somatic rubber hand illusion, a non-visual variant of the RHI. The somatic rubber hand illusion was found to be associated with an attenuation around 330ms post-stimulus on central electrodes, similar to the classic RHI in Experiment Two and Three. This indicated that this illusion effect in evoked responses was not related to a remapping of visual receptive fields as a result of the RHI but to the neurophysiological processes of the RHI itself. To summarise, the results of the experiments presented in this thesis indicate that an attenuation at 330ms in evoked potentials is associated with illusory hand ownership in both, the classic RHI and the somatic RHI. Further, attenuation in alpha and beta band power is associated with illusory hand ownership in the classic RHI