Role of the Vestibular System in the Construction of Self

How do we construct a unified self-identity as a thinking and feeling person inhabiting a body, separate and unique from other entities? A “self” with the capacity for autobiographical memory and complex thought? Traditionally, the field of cognitive science has been concerned with explaining the mind in isolation from the body.

The growing field of embodied cognition, on the other hand, seeks to rejoin them. One major strand has focused on grounding higher-order semantics and language understanding in perceptual and sensory-motor representations. This view is distinct from theories of knowledge based on abstract, amodal representations divorced from sensory-motor experience. Another wing of the embodied approach is concerned with how interoception — the inner sense of your physical state — grounds your feelings and emotions in the body. Interoceptive awareness of visceral functions such as heartbeat has been related to core consciousness and awareness of self, including body image.

A relatively neglected yet critical aspect of any grand theory of the embodied self is the vestibular system. The vestibular system is the set of sensory organs responsible for maintaining our balance and keeping our visual field in a stable position while our head moves around. These organs are located in the inner ear and include...

...two otolith organs (the saccule and utricle), which sense linear acceleration (i.e., gravity and translational movements), and the three semicircular canals, which sense angular acceleration in three planes. The receptor cells of the otoliths and semicircular canals send signals through the vestibular nerve fibers to the neural structures that control eye movements, posture, and balance.

The quote above is from Kathleen Cullen and Soroush Sadeghi (2008), who have an excellent review on the vestibular system in Scholarpedia.

We take the vestibular system for granted until something goes wrong, like motion sickness (a mismatch of movement perceived by the vestibular and visual systems) or a rare disorder of the inner ear such as Menière’s disease. But how can a dysfunction of the inner ear influence our sense of self?

Song, Jáuregui-Renaud, and colleagues (2008) looked at symptoms of depersonalization (a feeling of detachment from oneself) in 50 patients with peripheral vestibular disease and 121 healthy controls. The participants were given the Depersonalization/Derealization Inventory of Cox and Swinson (2002) to assess symptoms of these conditions:

1. Depersonalization: Experiences of unreality, detachment, or being an outside observer with respect to one's thoughts, feelings, sensations, body, or actions (e.g.,perceptual alterations, distorted sense of time, unreal or absent self, emotional and/or physical numbing.)" 
2. Derealization: "Experiences of unreality or detachment with respect to surroundings (e.g., individuals or objects are experienced as unreal, dreamlike, foggy, lifeless, or visually distorted."

Beyond the expected high frequency of dizziness, the patients were much more likely to experience feelings of Shifting Ground, Spaced Out, Body Feels Strange, and Not Being in Control of Self than were controls (see bottom half of the figure below).

The authors suggest that abnormal vestibular signals disrupt the relationship of the self to the environment, leading to strange feelings of detachment:

Vestibular disease causes primary symptoms of vertigo and feelings that the ground is unstable ... which are more marked in distinct, acute episodes. These immediate symptoms are, by definition, unreal experiences since the body is not spinning and the ground is not heaving, but they are readily understandable as perceptions derived directly from abnormal sensory signals. Vestibular dysfunction could also compromise more general precepts of stable relationships between the self and the environment...

Symptoms of depersonalization/derealization can be induced experimentally in healthy people via caloric stimulation. This procedure is used medically to check the vestibulo-ocular reflex, which stabilizes the visual image while the head is moving. The test involves delivering warm or cold water into the ear canal and observing the resultant eye movements (or lack thereof).

Song et al. (2008) administered caloric stimulation to 20 of their vestibular patients and 20 controls. After stimulation, many healthy participants reported feelings of detachment/separation from their surroundings (40%), and that their body feels strange/different (50%). These were novel experiences for most. Conversely, the patients reported no such changes after stimulation because they already experience these symptoms.

An even more extreme way to stimulate the vestibular system is through unilateral centrifugation (i.e., spinning around in a specialized chair). NOTE: this has nothing to do with the fictional Centrifuge Brain Project. See more about that here.

Neuro Kinetics I-Portal®-NOTC

(I don't think I'd be smiling)

A recent study subjected 100 healthy participants to unilateral centrifugation to stimulate the utricles (Aranda-Moreno & Jáuregui-Renaud, 2016). The target of this test differs from the caloric procedure, which stimulates the semicircular canals. The utricles and the semicircular canals detect different types of motion (linear acceleration and angular acceleration, respectively), and the authors wanted to see if unilateral centrifugation would produce the same effects as caloric stimulation. And indeed, after centrifugation, symptoms of depersonalization and derealization were reported with increased frequency — e.g., Surroundings seem strange and unreal; Time seems to pass very slowly; Body feels strange or different in some way (see Table below for details).

- click on image for a larger view -

modified from Table 2 (Aranda-Moreno & Jáuregui-Renaud, 2016). Frequency (Freq) and severity (score range) for each of the symptoms of the Cox and Swinson (2002) depersonalization/derealization inventory reported by 100 subjects.


These results provide further evidence that the vestibular system contributes to the construction of the self. The sense of inhabiting one's body is assembled from many different inputs, of course. These can go awry in epilepsy, migraine, focal brain injury, psychiatric disturbances, and under extreme stress. Although rare, out-of-body experiences are more frequent in persons who suffer from dizziness due to vestibular disorders (Lopez & Elzière, 2017). In these instances, the vestibular system is unable to ground the self within the body.


References

Aranda-Moreno C, Jáuregui-Renaud K. (2016). Derealization during utricular stimulation. Journal of Vestibular Research 26(5-6):425-431.

Cullen K, Sadeghi S (2008). Vestibular system. Scholarpedia, 3(1):3013.

Lopez C, Elzière M. (2017). Out-of-body experience in vestibular disorders - A prospective study of 210 patients with dizziness. Cortex Jun 8.

Sang FY, Jauregui-Renaud K, Green DA, Bronstein AM, Gresty MA. (2006). Depersonalisation/derealisation symptoms in vestibular disease. Journal of Neurology, Neurosurgery & Psychiatry 77(6):760-6.

Further Reading

Research Topic: The Vestibular System in Cognitive and Memory Processes in Mammalians (collection edited by Besnard et al., 2015)

Personality changes in patients with vestibular dysfunction (review by Smith & Darlington, 2013)

Feeling Mighty Unreal: Derealization in Kleine-Levin Syndrome (blog post by The Neurocritic)

A Detached Sense of Self Associated with Altered Neural Responses to Mirror Touch (blog post by The Neurocritic)

Theme issue ‘Interoception beyond homeostasis: affect, cognition and mental health’ (edited by Manos Tsakiris and Hugo D. Critchley).

The poverty of embodied cognition (Goldinger et al., 2016).

Arguments about the nature of concepts: Symbols, embodiment, and beyond (Mahon & Hickok, 2016).