The sense of self and vestibular dysfunction

In addition to the deficits in eye movement and postural reflexes that occur following vestibular dysfunction, there is convincing evidence that vestibular loss also causes cognitive and emotional disorders, some of which may be due to the reflexive deficits and the role that vestibular pathways play in the spatial orientation.

Patients with vestibular disorders demonstrate also other personality changes suggesting that vestibular sensation is implicated in the sense of self. These are depersonalization and derealization, feeling “spaced out”, “body feeling strange” and “not feeling in control of self”. We propose in this review that these symptoms suggest that the vestibular system may make a unique contribution to the concept of self through information regarding self-motion and self-location that it transmits to the brain.
Recent epidemiological studies suggest that vestibular disorders occur in more than 35% of adults aged 40 or older. Vestibular dysfunction results in a complex neurological syndrome characterized not only by reflex deficits, but also by spatial memory deficits, autonomic and anxiety disorders. Many papers have been published reporting spatial memory and attention deficits in patients with different kinds of vestibular disorders. Although it is possible that cognitive dysfunction is an indirect consequence of symptoms such as vertigo, studies of patients with chronic vestibular loss, but without vertigo, have still demonstrated spatial memory impairment.

In addition, a large body of evidence from animal studies has demonstrated that animals with vestibular lesions suffer from cognitive impairment. It is clear that the loss of vestibular information results in the abnormal function of many brain regions, including the hippocampus, which has been demonstrated to atrophy following complete bilateral vestibular loss in humans. However, exactly why this happens is unclear. The vestibular system encodes angular and linear acceleration of the head in three dimensions and, in addition to generating the VORs and VSRs, provides the brain with information about self-motion that can be used to navigate through the environment and form memories for places in it.

However, the severity of the symptoms of vestibular dysfunction suggests that there may be a critical dependence of the brain and body upon vestibular input. The most primitive part of the vestibular system—the otoliths that transduce linear acceleration, including linear acceleration by gravity—is estimated to be more than 500 million years old and exists in primitive species such as sea squirts.

These sensory organs evolved to provide information about gravitational vertical, before any other sensory system had developed, and it was fully functional before the visual or auditory systems. Therefore, it is highly likely that human physiology has a special dependence upon the otolithic part of the vestibular system.

Vestibular dysfunction in humans is often associated with anxiety disorders, including panic attacks and phobias, as well as depression. While it is possible that anxiety is a direct consequence of vestibular dysfunction, it has also been reported that anxiety disorders can cause dizziness of vestibular origin and antidepressants such as selective serotonin reuptake inhibitors (SSRIs) have been reported to relieve dizziness associated with psychiatric symptoms.

It is possible that emotional disorders arise indirectly from cognitive impairment. However, some researchers have reported that the same neurons that release serotonin, send projections into the amygdala, an area of the brain concerned with fear and panic, as well as the brainstem vestibular nucleus.

This finding suggests that changes in emotional tone may directly influence the vestibular system. This kind of evidence indicates that vestibular impairment may cause a multitude of changes in cognition, emotion and personality, which is consistent with some evidence that vestibular disease is associated with unusually high rates of depersonalization symptoms, which include difficulty to concentrate and be consequent.

The most severe depersonalization and derealization scores were observed in patients with bilateral vestibular loss and the least severe scores were in patients with unilateral canal paresis without balance symptoms.

The presence of depersonalization and derealization symptoms in patients with vestibular dysfunction suggests that vestibular sensation contributes to the definition of the self, in terms of the sense of where the body is in relation to the external world. The vestibular system is one of a number of sensory systems that contributes to the internal representation of the self and can promote feelings of disembodiment when dysfunction occurs.

The data from animal studies support the view that vestibular information is fundamentally important for the generation of hippocampal spatial memories in animals and humans. There is still debate as to how vestibular information reaches the hippocampus. However, the hippocampus is only one part of a highly complex system of limbic-neocortical pathways that are responsible for spatial memory. In humans, functional magnetic resonance imaging has revealed that activation of cortical networks during galvanic vestibular stimulation is not symmetrical; it is stronger in the non-dominant hemisphere, in the hemisphere ipsilateral to stimulated ear, and in the hemisphere ipsilateral to the fast phase of vestibular nystagmus.

While the vestibular system was once recognized mainly for its regulation of eye movement and postural reflexes, increasingly it has become apparent that the cortical representation of vestibular information is important for cognition, emotion and even the sense of self. While it might seem self-evident that knowing where you are using vestibular information, also defines the boundary between the self and the external world, many of the more ethereal effects of vestibular dysfunction, which are difficult to describe, have gone undocumented or at least poorly recognized in the neurological literature.
Source: Frontiers of Human Neuroscience

Galina Toktalieva

Kyrgyzstan-born author residing in Graz, Austria

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