RESUMEN
Previous studies investigated bodily self-consciousness (BSC) by experimentally exposing subjects to multisensory conflicts (i.e., visuo-tactile, audio-tactile, visuo-cardiac) in virtual reality (VR) that involve the participant's torso in a paradigm known as the full-body illusion (FBI). Using a modified FBI paradigm, we found that synchrony of visuo-respiratory stimulation (i.e., a flashing outline surrounding an avatar in VR; the flash intensity depending on breathing), is also able to modulate BSC by increasing self-location and breathing agency toward the virtual body. Our aim was to investigate such visuo-respiratory effects and determine whether respiratory motor commands contributes to BSC, using non-invasive mechanical ventilation (i.e., machine-delivered breathing). Seventeen healthy participants took part in a visuo-respiratory FBI paradigm and performed the FBI during two breathing conditions: (a) "active breathing" (i.e., participants actively initiate machine-delivered breaths) and (b) "passive breathing" (i.e., breaths' timing was determined by the machine). Respiration rate, tidal volume, and their variability were recorded. In line with previous results, participants experienced subjective changes in self-location, breathing agency, and self-identification toward the avatar's body, when presented with synchronous visuo-respiratory stimulation. Moreover, drift in self-location was reduced and tidal volume variability were increased by asynchronous visuo-respiratory stimulations. Such effects were not modulated by breathing control manipulations. Our results extend previous FBI findings showing that visuo-respiratory stimulation affects BSC, independently from breathing motor command initiation. Also, variability of respiratory parameters was influenced by visuo-respiratory feedback and might reduce breathing discomfort. Further exploration of such findings might inform the development of respiratory therapeutic tools using VR in patients.
Asunto(s)
Ilusiones/fisiología , Interocepción/fisiología , Propiocepción/fisiología , Respiración , Percepción Visual/fisiología , Adolescente , Adulto , Femenino , Humanos , Masculino , Estimulación Física , Respiración Artificial , Realidad Virtual , Adulto JovenRESUMEN
OBJECTIVES: To develop and test a new immersive digital technology for complex regional pain syndrome (CRPS) that combines principles from mirror therapy and immersive virtual reality and the latest research from multisensory body processing. METHODS: In this crossover double-blind study, 24 patients with CRPS and 24 age- and sex-matched healthy controls were immersed in a virtual environment and shown a virtual depiction of their affected limb that was flashing in synchrony (or in asynchrony in the control condition) with their own online detected heartbeat (heartbeat-enhanced virtual reality [HEVR]). The primary outcome measures for pain reduction were subjective pain ratings, force strength, and heart rate variability (HRV). RESULTS: HEVR reduced pain ratings, improved motor limb function, and modulated a physiologic pain marker (HRV). These significant improvements were reliable and highly selective, absent in control HEVR conditions, not observed in healthy controls, and obtained without the application of tactile stimulation (or movement) of the painful limb, using a readily available biological signal (the heartbeat) that is most often not consciously perceived (thus preventing placebo effects). CONCLUSIONS: Next to these specific and well-controlled analgesic effects, immersive HEVR allows the application of prolonged and repeated doses of digital therapy, enables the automatized integration with existing pain treatments, and avoids application of painful bodily cues while minimizing the active involvement of the patient and therapist. CLASSIFICATION OF EVIDENCE: This study provides Class III evidence that HEVR reduces pain and increases force strength in patients with CRPS.
Asunto(s)
Síndromes de Dolor Regional Complejo/diagnóstico , Síndromes de Dolor Regional Complejo/terapia , Frecuencia Cardíaca/fisiología , Dimensión del Dolor/métodos , Terapia de Exposición Mediante Realidad Virtual/métodos , Adulto , Anciano , Anciano de 80 o más Años , Síndromes de Dolor Regional Complejo/fisiopatología , Estudios Cruzados , Método Doble Ciego , Electrocardiografía/métodos , Femenino , Humanos , Masculino , Persona de Mediana EdadRESUMEN
Interoceptive signals, such as the heartbeat, are processed in a network of brain regions including the insular cortex. Recent studies have shown that such signals modulate perceptual and cognitive processing, and that they impact visual awareness. For example, visual stimuli presented synchronously to the heartbeat take longer to enter visual awareness than the same stimuli presented asynchronously to the heartbeat, and this is reflected in anterior insular activation. This finding demonstrated a link between the processing of interoceptive and exteroceptive signals as well as visual awareness in the insular cortex. The advantage for visual stimuli which are asynchronous to the heartbeat to enter visual consciousness may indicate a role for the anterior insula in the suppression of the sensory consequences of cardiac signals. Here, we present data from the detailed investigation of two patients with insular lesions (as well as four patients with non-insular lesions and healthy age matched controls) indicating that a lesion of the anterior insular cortex, but not of other regions, abolished this cardio-visual suppression effect. The present data provide causal evidence for the role of the anterior insula in the integration of internal interoceptive and external sensory signals for visual awareness.
Asunto(s)
Corteza Cerebral/fisiología , Estado de Conciencia/fisiología , Frecuencia Cardíaca/fisiología , Interocepción/fisiología , Percepción Visual/fisiología , Adulto , Teorema de Bayes , Mapeo Encefálico , Corteza Cerebral/diagnóstico por imagen , Cognición , Electrocardiografía , Electroencefalografía , Emociones , Femenino , Lateralidad Funcional , Humanos , Imagen por Resonancia Magnética , Masculino , Persona de Mediana Edad , Estimulación Luminosa/métodos , Adulto JovenRESUMEN
Dyspnoea, a subjective experience of breathing discomfort, is a most distressing symptom. It implicates complex cortical networks that partially overlap with those underlying bodily self-consciousness, the experience that the body is one's own within a given location (self-identification and self-location, respectively). Breathing as an interoceptive signal contributes to bodily self-consciousness: we predicted that inducing experimental dyspnoea would modify or disrupt this contribution. We also predicted that manipulating bodily self-consciousness with respiratory-visual stimulation would possibly attenuate dyspnoea. Twenty-five healthy volunteers were exposed to synchronous and asynchronous respiratory-visual illumination of an avatar during normal breathing and mechanically loaded breathing that elicited dyspnoea. During normal breathing, synchronous respiratory-visual stimulation induced illusory self-identification with the avatar and an illusory location of the subjects' breathing towards the avatar. This did not occur when respiratory-visual stimulation was performed during dyspnoea-inducing loaded breathing. In this condition, the affective impact of dyspnoea was attenuated by respiratory-visual stimulation, particularly when asynchronous. This study replicates and reinforces previous studies about the integration of interoceptive and exteroceptive signals in the construction of bodily self-consciousness. It confirms the existence of interferences between experimental dyspnoea and cognitive functions. It suggests that respiratory-visual stimulation should be tested as a non-pharmacological approach of dyspnoea treatment.
Asunto(s)
Imagen Corporal , Estado de Conciencia , Disnea , Respiración , Autoimagen , Adulto , Femenino , Voluntarios Sanos , Humanos , Masculino , Estimulación Luminosa , Adulto JovenRESUMEN
Multisensory perception research has largely focused on exteroceptive signals, but recent evidence has revealed the integration of interoceptive signals with exteroceptive information. Such research revealed that heartbeat signals affect sensory (e.g., visual) processing: however, it is unknown how they impact the perception of body images. Here we linked our participants' heartbeat to visual stimuli and investigated the spatio-temporal brain dynamics of cardio-visual stimulation on the processing of human body images. We recorded visual evoked potentials with 64-channel electroencephalography while showing a body or a scrambled-body (control) that appeared at the frequency of the on-line recorded participants' heartbeat or not (not-synchronous, control). Extending earlier studies, we found a body-independent effect, with cardiac signals enhancing visual processing during two time periods (77-130 ms and 145-246 ms). Within the second (later) time-window we detected a second effect characterised by enhanced activity in parietal, temporo-occipital, inferior frontal, and right basal ganglia-insula regions, but only when non-scrambled body images were flashed synchronously with the heartbeat (208-224 ms). In conclusion, our results highlight the role of interoceptive information for the visual processing of human body pictures within a network integrating cardio-visual signals of relevance for perceptual and cognitive aspects of visual body processing.
Asunto(s)
Interocepción/fisiología , Percepción Visual/fisiología , Adulto , Electroencefalografía , Potenciales Evocados Visuales/fisiología , Femenino , Corazón , Humanos , Masculino , Estimulación Luminosa/métodos , Procesamiento de Señales Asistido por Computador , Adulto JovenRESUMEN
Exteroceptive bodily signals (including tactile, proprioceptive and visual signals) are important information contributing to self-consciousness. Moreover, prominent theories proposed that visceral signals about internal bodily states are equally or even more important for self-consciousness. Neuroimaging studies have described several brain regions which process signals related to bodily self-consciousness (BSC) based on the integration of exteroceptive signals (e.g. premotor cortex, angular gyrus, supramarginal gyrus and extrastriate body area), and that another brain region, the insula/operculum which is involved in interoception and interoceptive awareness, processes signals critical for self-awareness. Providing evidence for the integration of exteroceptive and interoceptive bodily signals, recent behavioral experiments have demonstrated that the manipulation of interoceptive (e.g. cardiac) signals, coupled with exteroceptive (e.g. visual) signals, also modulates BSC. Does this integration occur within or outside the structures described above? To this end, we adapted a recently designed protocol that uses cardio-visual stimulation to induce altered states of BSC to fMRI. Additionally, we measured neural activity in a classical interoceptive task. We found six brain regions (bilateral Rolandic operculum, bilateral supramarginal gyrus, right frontal inferior operculum and left temporal superior gyrus) that were activated differently during the interoception task as opposed to a control task. The brain regions which showed the highest selectivity for BSC based on our cardio-visual manipulation were found in the bilateral Rolandic operculum. Given our findings, we propose that the Rolandic operculum processes integrated exteroceptive-interoceptive signals that are necessary for interoceptive awareness as well as BSC.
Asunto(s)
Concienciación , Encéfalo/fisiología , Frecuencia Cardíaca , Interocepción , Adulto , Imagen Corporal , Femenino , Humanos , Imagen por Resonancia Magnética , MasculinoRESUMEN
Vision is known to be shaped by context, defined by environmental and bodily signals. In the Taylor illusion, the size of an afterimage projected on one's hand changes according to proprioceptive signals conveying hand position. Here, we assessed whether the Taylor illusion does not just depend on the physical hand position, but also on bodily self-consciousness as quantified through illusory hand ownership. Relying on the somatic rubber hand illusion, we manipulated hand ownership, such that participants embodied a rubber hand placed next to their own hand. We found that an afterimage projected on the participant's hand drifted depending on illusory ownership between the participants' two hands, showing an implication of self-representation during the Taylor illusion. Oscillatory power analysis of electroencephalographic signals showed that illusory hand ownership was stronger in participants with stronger α suppression over left sensorimotor cortex, whereas the Taylor illusion correlated with higher ß/γ power over frontotemporal regions. Higher γ connectivity between left sensorimotor and inferior parietal cortex was also found during illusory hand ownership. These data show that afterimage drifts in the Taylor illusion do not only depend on the physical hand position but also on subjective ownership, which itself is based on the synchrony of somatosensory signals from the two hands. The effect of ownership on afterimage drifts is associated with ß/γ power and γ connectivity between frontoparietal regions and the visual cortex. Together, our results suggest that visual percepts are not only influenced by bodily context but are self-grounded, mapped on a self-referential frame. SIGNIFICANCE STATEMENT: Vision is influenced by the body: in the Taylor illusion, the size of an afterimage projected on one's hand changes according to tactile and proprioceptive signals conveying hand position. Here, we report a new phenomenon revealing that the perception of afterimages depends not only on bodily signals, but also on the sense of self. Relying on the rubber hand illusion, we manipulated hand ownership, so that participants embodied a rubber hand placed next to their own hand. We found that visual afterimages projected on the participant's hand drifted laterally, only when the rubber hand was embodied. Electroencephalography revealed spectral dissociations between somatic and visual effects, and higher γ connectivity along the dorsal visual pathways when the rubber hand was embodied.
Asunto(s)
Ritmo beta/fisiología , Ritmo Gamma/fisiología , Mano , Autoimagen , Percepción Visual , Postimagen , Ritmo alfa/fisiología , Imagen Corporal , Ego , Electroencefalografía , Femenino , Lóbulo Frontal/fisiología , Humanos , Ilusiones , Masculino , Lóbulo Parietal/fisiología , Corteza Sensoriomotora/fisiología , Corteza Visual/fisiología , Adulto JovenRESUMEN
UNLABELLED: Recent research has investigated self-consciousness associated with the multisensory processing of bodily signals (e.g., somatosensory, visual, vestibular signals), a notion referred to as bodily self-consciousness, and these studies have shown that the manipulation of bodily inputs induces changes in bodily self-consciousness such as self-identification. Another line of research has highlighted the importance of signals from the inside of the body (e.g., visceral signals) and proposed that neural representations of internal bodily signals underlie self-consciousness, which to date has been based on philosophical inquiry, clinical case studies, and behavioral studies. Here, we investigated the relationship of bodily self-consciousness with the neural processing of internal bodily signals. By combining electrical neuroimaging, analysis of peripheral physiological signals, and virtual reality technology in humans, we show that transient modulations of neural responses to heartbeats in the posterior cingulate cortex covary with changes in bodily self-consciousness induced by the full-body illusion. Additional analyses excluded that measured basic cardiorespiratory parameters or interoceptive sensitivity traits could account for this finding. These neurophysiological data link experimentally the cortical mapping of the internal body to self-consciousness. SIGNIFICANCE STATEMENT: What are the brain mechanisms of self-consciousness? Prominent views propose that the neural processing associated with signals from the internal organs (such as the heart and the lung) plays a critical role in self-consciousness. Although this hypothesis dates back to influential views in philosophy and psychology (e.g., William James), definitive experimental evidence supporting this idea is lacking despite its recent impact in neuroscience. In the present study, we show that posterior cingulate activities responding to heartbeat signals covary with changes in participants' conscious self-identification with a body that were manipulated experimentally using virtual reality technology. Our finding provides important neural evidence about the long-standing proposal that self-consciousness is linked to the cortical processing of internal bodily signals.
Asunto(s)
Imagen Corporal , Mapeo Encefálico , Encéfalo/fisiología , Estado de Conciencia/fisiología , Frecuencia Cardíaca/fisiología , Autoimagen , Adulto , Electrocardiografía , Electroencefalografía , Femenino , Análisis de Fourier , Humanos , Ilusiones/fisiología , Masculino , Encuestas y Cuestionarios , Adulto JovenRESUMEN
UNLABELLED: The processing of interoceptive signals in the insular cortex is thought to underlie self-awareness. However, the influence of interoception on visual awareness and the role of the insular cortex in this process remain unclear. Here, we show in a series of experiments that the relative timing of visual stimuli with respect to the heartbeat modulates visual awareness. We used two masking techniques and show that conscious access for visual stimuli synchronous to participants' heartbeat is suppressed compared with the same stimuli presented asynchronously to their heartbeat. Two independent brain imaging experiments using high-resolution fMRI revealed that the insular cortex was sensitive to both visible and invisible cardio-visual stimulation, showing reduced activation for visual stimuli presented synchronously to the heartbeat. Our results show that interoceptive insular processing affects visual awareness, demonstrating the role of the insula in integrating interoceptive and exteroceptive signals and in the processing of conscious signals beyond self-awareness. SIGNIFICANCE STATEMENT: There is growing evidence that interoceptive signals conveying information regarding the internal state of the body influence perception and self-awareness. The insular cortex, which receives sensory inputs from both interoceptive and exteroceptive sources, is thought to integrate these multimodal signals. This study shows that cardiac interoceptive signals modulate awareness for visual stimuli such that visual stimuli occurring at the cardiac frequency take longer to access visual awareness and are more difficult to discriminate. Two fMRI experiments show that the insular region is sensitive to this cardio-visual synchrony even when the visual stimuli are rendered invisible through interocular masking. The results indicate a perceptual and neural suppression for visual events coinciding with cardiac interoceptive signals.
Asunto(s)
Corteza Cerebral/fisiología , Corazón/fisiología , Estimulación Luminosa , Adolescente , Adulto , Concienciación , Mapeo Encefálico , Femenino , Humanos , Procesamiento de Imagen Asistido por Computador , Interocepción , Imagen por Resonancia Magnética , Masculino , Enmascaramiento Perceptual , Percepción Visual/fisiología , Adulto JovenRESUMEN
Recent evidence suggests that multisensory integration of bodily signals involving exteroceptive and interoceptive information modulates bodily aspects of self-consciousness such as self-identification and self-location. In the so-called Full Body Illusion subjects watch a virtual body being stroked while they perceive tactile stimulation on their own body inducing illusory self-identification with the virtual body and a change in self-location towards the virtual body. In a related illusion, it has recently been shown that similar changes in self-identification and self-location can be observed when an interoceptive signal is used in association with visual stimulation of the virtual body (i.e., participants observe a virtual body illuminated in synchrony with their heartbeat). Although brain imaging and neuropsychological evidence suggest that the insular cortex is a core region for interoceptive processing (such as cardiac perception and awareness) as well as for self-consciousness, it is currently not known whether the insula mediates cardio-visual modulation of self-consciousness. Here we tested the involvement of insular cortex in heartbeat awareness and cardio-visual manipulation of bodily self-consciousness in a patient before and after resection of a selective right neoplastic insular lesion. Cardio-visual stimulation induced an abnormally enhanced state of bodily self-consciousness; in addition, cardio-visual manipulation was associated with an experienced loss of the spatial unity of the self (illusory bi-location and duplication of his body), not observed in healthy subjects. Heartbeat awareness was found to decrease after insular resection. Based on these data we propose that the insula mediates interoceptive awareness as well as cardio-visual effects on bodily self-consciousness and that insular processing of interoceptive signals is an important mechanism for the experienced unity of the self.