Balancing Interoception and Exteroception: Vestibular and Spatial Contributions to the Bodily Self
Experiencing the body as a coherent, stable, entity involves the dynamic integration of information from several internal (i.e. interoceptive) and external (i.e. exteroceptive) sensory sources, to produce a feeling that the body is mine (sense of body ownership), that I am in control (sense of agency) and I am aware of its movements (motor awareness). However, the exact contribution of these different sensory sources to self-consciousness, as well as the context in which we experience them, is still a matter of debate. This thesis aimed to investigate the neurocognitive mechanisms of body ownership, agency and motor awareness, including interoceptive (via affective touch), proprioceptive, exteroceptive (visuo-spatial) and vestibular contributions to body representation, in both healthy subjects and brain damaged patients. To examine the role of the vestibular and interoceptive systems in body ownership, a series of studies in healthy subjects was devised, using multisensory illusions (i.e. the rubber hand illusion; RHI), that involve the integration of interoceptive and exteroceptive sensory sources, and using electrical stimulation of the vestibular system (i.e. Galvanic Vestibular Stimulation; GVS). To investigate ownership, agency and motor awareness in neuropsychological patients with disorders of ownership and/or unawareness of motor deficits, behavioural manipulation of body ownership (via a rubber hand) and visual perspective (via a mirror) were tested. Finally, to explore underlying mechanisms of awareness of one’s own performance (i.e. meta-cognition), two studies were carried out in healthy subjects using behavioural manipulations of spatial reference frames (either centred on the subject, i.e. egocentric, or world-centred, i.e. allocentric). The results of these studies indicate that the vestibular system balances vision and proprioception according to contextual relevance: when there is no tactile stimulation, visual cues are stronger than proprioceptive ones (i.e. proprioceptive drifts are greater); when touch is delivered synchronously, this effect is enhanced (even more when touch is affective rather than neutral). However, when touch is only felt but not seen, the vestibular system downregulates vision in favour of proprioception (i.e. proprioceptive drifts are smaller), whilst the opposite happens when touch is only vicariously perceived via vision. Nevertheless, when the rubber hand is positioned in a non-biomechanically possible fashion, there appears to be no difference in proprioceptive drifts in comparison with anatomically plausible positions, suggesting that such rebalancing may be more related to basic multisensory integration processes underlying body representation. In patients with disorders of the self, visual cues seem to dominate over proprioceptive ones, leading to strong feelings of ownership of a rubber hand following mere exposure to it; however, the same is not true for agency, which seems to be more susceptible to changes in the environment (i.e. presence or absence of a visual feedback following attempted movement). Moreover, manipulating visual perspective using a mirror (from 1st to 3rd) seem to lead to a temporary remission of dis-ownership but not motor unawareness, suggesting that awareness may not be influenced by online changes in visual perspectives. Finally, when judging their own performance in a visuo-proprioceptive task from an egocentric rather than an allocentric perspective, healthy subjects appear less objective prospectively rather than during the task (i.e. their belief updating is biased when judging their ability to complete a task egocentrically). In sum, the work described above adds to the evidence that the sense of self derives from a complex integration of several sensory modalities, flexibly adjusting to the environment. Following brain damage, such flexibility may be impaired, even though it can be influenced by spatial perspective. Similarly, the point of reference from which we perceive stimuli affects the way we judge our own perceptual choices. Hence, the way we represent our bodily self is a dynamic process, constantly updated by exteroceptive and interoceptive incoming stimuli, regulated by the vestibular system. These findings could provide new avenues in rehabilitating disorders of the self (such as unawareness and dis-ownership).
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