Original Research ARTICLE
Voluntary out-of-body experience: an fMRI study
- School of Psychology, University of Ottawa, Ottawa, ON, Canada
The present single-case study examined functional brain imaging patterns in a participant that reported being able, at will, to produce somatosensory sensations that are experienced as her body moving outside the boundaries of her physical body all the while remaining aware of her unmoving physical body. We found that the brain functional changes associated with the reported extra-corporeal experience (ECE) were different than those observed in motor imagery. Activations were mainly left-sided and involved the left supplementary motor area and supramarginal and posterior superior temporal gyri, the last two overlapping with the temporal parietal junction that has been associated with out-of-body experiences. The cerebellum also showed activation that is consistent with the participant’s report of the impression of movement during the ECE. There was also left middle and superior orbital frontal gyri activity, regions often associated with action monitoring. The results suggest that the ECE reported here represents an unusual type of kinesthetic imagery.
The experience of one’s body is a central process to allow us to interact with the outside world. Body experience is based on the integration of visual, vestibular, and somatosensory information (Giummarra et al., 2008; Berlucchi and Aglioti, 2010; de Vignemont, 2011; Blanke, 2012; Moseley et al., 2012). This information allows the tracking of the body in space and in relation with other objects and beings in our environment. Tracking of our body in turn, guides our movements (Goodale et al., 2008). The conscious experience of our body is generally congruent across sensory modalities so that, what we see of our body is also what we feel from somatosensory and vestibular sensations (Tsakiris, 2010). The sensations and percept associated with our body in movement can also be elicited in our imagination albeit most of the time in an attenuated form. Motor imagery corresponds to the cognitive version of motor actions without actual motor movements (Guillot et al., 2012; Moran et al., 2012). This motor “imagery” encompass visual components when we imagine movements as we would see them from our own perspective or from a third-person perspective (imagine someone else moving – or imagine ourselves moving but from a third-person perspective) and proprioceptive and vestibular components often referred to kinesthetic “imagery” (Guillot et al., 2009, p. 698). Motor imagery is intertwined within the brain’s preparatory processes preceding action and, up to a certain point, the brain’s processes subserving actual movement (Guillot and Collet, 2005). The strongest support for this view has come from functional imaging that demonstrated strong but incomplete overlap between imagery, action preparation, and action (Porro et al., 1996; Guillot et al., 2008, 2009; Szameitat et al., 2012a,b). These studies show that motor imagery is dependent both on brain regions associated with the performance of motor action but also on the somatosensory brain regions associated with body perception. Voluntary and involuntary motor imagery is also present in amputated individuals with an associated phantom limb often together with somatosensory perception (Melzack, 1989, p. 657; Ramachandran and Hirstein, 1998, p. 493). Some amputees can also train themselves to experience an anatomically impossible movement with their phantom limb suggesting the plasticity of sensorimotor systems (Moseley and Brugger, 2009, p. 1069).
The multi-component nature of body representation is also revealed in perceptual illusions such as the rubber hand illusion (Botvinick and Cohen, 1998). In the rubber hand illusion, the vision-based belief that the rubber hand is not part of the participant’s body is countered by the simultaneous touching of the rubber hand and the real hand and leads to a shift in the attribution of the localization of sensory stimulation from the real hand to the rubber hand (Hohwy and Paton, 2010). During the process of establishing the illusion, from completely separate to unity with the rubber hand, several intermediate illusory experiences can take place (Valenzuela Moguillansky et al., 2013, p. 1001). In one experiment using a moveable hand model, conditions could be manipulated so that participants reported a dissociation of the sense of ownership (impression that the fake hand is their own) or the sense of agency (impression that participants controlled the movements of the fake hand) (Kalckert and Ehrsson, 2012). Mismatch between the observed position of the hand model and the sensed position of the real hand reduced sense of ownership but did not disrupt the impression of agency. Conversely, passive movement reduced agency but left ownership intact (Kalckert and Ehrsson, 2012). These observations suggest that agency and ownership may depend on different but overlapping brain networks (Jackson et al., 2006, p. 703). Another experiment demonstrated that concurrent limb and full-body orientation illusions elicited by virtual reality visual displacement were undissociated and not dependent on action (Olive and Berthoz, 2012, p. 1050).
During these illusions, the participants do not doubt that the shifted body perception is illusory (Blanke and Metzinger, 2009). In contrast, shifted body perception of neurological origin (Blanke and Mohr, 2005) or pharmacologically induced (Morgan et al., 2011; Wilkins et al., 2011) can lead to ambiguous embodiment whereas people report that the illusory body or body part is more realistic or corresponds to a “double” of their body. In the descriptions below, the “double” refers to the illusory body (or parts thereof). There seems to be a general consensus in adopting the classification proposed by Brugger to describe these illusions (Brugger and Regard, 1997). Autoscopic hallucination is a visual hallucination of the upper part of a double of the body. Heautoscopy is a visual and somesthetic hallucination. The double, which appears as through a veil, can mirror the person’s movements. Heautoscopy hallucination is also accompanied by a vague feeling of detachment and depersonalization. The double is felt vaguely as another self. Feeling of a presence is a mostly somesthetic hallucination that a double is present usually close by or even touching but not seen. Feeling of a presence is also called sensed-presence experience when the presence is identified as another person (Cheyne and Girard, 2007, p. 1065). Out-of-body experience is a visual and somesthetic experience in which the double is seen from a different perspective, often motionless. Because the body in this experience is “seen” from a third-person perspective (i.e., from above), the body seen is illusory even if it is congruent with the body’s position during the illusion (e.g., lying down). The experience is accompanied by a profound feeling of being outside of the body and with feelings of meaningfulness of the experience.
Three studies of self-reported anomalous body experiences in unremarkable normal people (Braithwaite et al., 2011, p. 876; Braithwaite et al., 2011, p. 1063; Braithwaite et al., 2013, p. 1064). In the first one, it was noted that most instances of spontaneous anomalous body experiences occurred during a relaxed or borderline sleeping state and one-third reported (seeing) their body from a different perspective while the rest reported a visual or somatosensory shift in perspective. The participants who reported out-of-body experience also self-reported more perceptual anomalies (Braithwaite et al., 2011, p. 876). In two subsequent experiments, participants self-reporting anomalous body experiences (mostly of visual nature) were more likely to respond strongly to aversive visual patterns suggesting that the visual system of the participants are somehow different, at least functionally (Braithwaite et al., 2013, p. 1064; Braithwaite et al., 2013, p. 1063). The authors also derived the hypothesis that these anomalous body experiences depended on temporal lobe anomalies as measured by perceptual tasks and questionnaires (Braithwaite et al., 2011, p. 876).
There also have been imaging enquiries into the brain areas involved in body representation illusions in neurologically intact participants (Blanke, 2012). Brain imaging studies have suggested that activity in sensory integration areas such as the intraparietal sulcus and the ventral premotor cortex are associated with the establishment of the rubber hand illusion (Ehrsson et al., 2004, 2005, 2007; Tsakiris et al., 2007). One experiment has used repeated transcranial magnetic stimulation to gain information on the brain areas involved in the rubber hand illusion (Tsakiris et al., 2008). They found that, when the activity of the temporal parietal junction (TPJ) was perturbed by repeated transcranial magnetic stimulation, the processing of body representation mental imagery was impaired. However, in another transcranial magnetic stimulation study, mental rotation of letter stimuli was not affected suggesting a specific effect for body representation (Blanke et al., 2005). Another experiment showed that, the temporal parietal junction, which is involved in self processing and multisensory integration of body-related information; and the extrastriate body area (EBA), which responds selectively to human bodies and body parts mental imagery is performed with mentally embodied (EBA) or disembodied (TPJ) self location (Arzy et al., 2006). The more intense hallucinations or illusions are usually associated with brain lesions, abnormal brain function such as epilepsy, major psychiatric syndromes, dissociative drugs such as ketamine, or in micro-gravity conditions (Kornilova, 1997).
The study of the lesioned or abnormal brain areas is often used to gain insight into the brain areas involved in normal body representation phenomena. However, there is also anecdotal evidence that these intense hallucinations can occur in non-neurological cases but they have a low occurrence and, apart from micro-gravity illusions, are unpredictable. In the present report, we used functional MRI to examine an otherwise “normal,” healthy individual that reported the ability to, at will, vividly experience her body moving outside her physical body while lying down at rest. The subjective description of the participant led us to use the term extra-corporeal experience (ECE) throughout this manuscript to underline the difference between the phenomenon studied here and the more common definition of out-of-body experiences. We included a number of guided imagery tasks to specify the ECE-related brain activity. One control task was motor imagery for a different movement (jumping jacks). A second control condition was alternating between actual finger movements and motor imagery of the same movement. Finally, we were interested in determining if there was a difference between imagining herself performing the ECE (but not experiencing the ECE) differed from the imagining of another person performing the same ECE movement.