Vestibular Modulation of Sympathetic Nerve Activity to Muscle and Skin in Humans

Abstract

We review the existence of vestibulosympathetic reflexes in humans. While several methods to activate the human vestibular apparatus have been used, galvanic vestibular stimulation (GVS) is a means of selectively modulating vestibular afferent activity via electrodes over the mastoid processes, causing robust vestibular illusions of side-to-side movement. Sinusoidal GVS (sGVS) causes partial entrainment of sympathetic outflow to muscle and skin. Modulation of muscle sympathetic nerve activity (MSNA) from vestibular inputs competes with baroreceptor inputs, with stronger temporal coupling to the vestibular stimulus being observed at frequencies remote from the cardiac frequency; “super entrainment” was observed in some individuals. Low-frequency (<0.2 Hz) sGVS revealed two peaks of modulation per cycle, with bilateral recordings of MSNA or skin sympathetic nerve activity, providing evidence of lateralization of sympathetic outflow during vestibular stimulation. However, it should be noted that GVS influences the firing of afferents from the entire vestibular apparatus, including the semicircular canals. To identify the specific source of vestibular input responsible for the generation of vestibulosympathetic reflexes, we used low-frequency (<0.2 Hz) sinusoidal linear acceleration of seated or supine subjects to, respectively, target the utricular or saccular components of the otoliths. While others had discounted the semicircular canals, we showed that the contributions of the utricle and saccule to the vestibular modulation of MSNA are very similar. Moreover, that modulation of MSNA occurs at accelerations well below levels at which subjects are able to perceive any motion indicates that, like vestibulospinal control of posture, the vestibular system contributes to the control of blood pressure through potent reflexes in humans.

The influence of vestibular stimulation on metabolism and body composition

“…Consistent with these findings, clinical studies have highlighted modulation of muscle sympathetic nerve activity as a direct target of electrical stimulation of the vestibular nerves . One such study reported increased muscle sympathetic nerve activity, recorded by electrodes placed at the common peroneal nerve, in response to a range of frequencies of vestibular nerve stimulation, induced by electrical stimulation bilaterally, up to 156% baseline . With specific regard to metabolism, muscle sympathetic nerve activity, which is known to regulate energy expenditure and adipose storage, is reported to positively correlate with weight loss in response to a hypocaloric diet .…”

“…For example, animal studies have reported that vestibular modulation specifically alters expression of both FK506 binding protein 5 and follistatin, key regulators of muscle protein synthesis [27]. Consistent with these findings, clinical studies have highlighted modulation of muscle sympathetic nerve activity as a direct target of electrical stimulation of the vestibular nerves [28]. One such study reported increased muscle sympathetic nerve activity, recorded by electrodes placed at the common peroneal nerve, in response to a range of frequencies of vestibular nerve stimulation, induced by electrical stimulation bilaterally, up to 156% baseline [28].…”

Distinct activation of the sympathetic adreno-medullar system and hypothalamus pituitary adrenal axis following the caloric vestibular test in healthy subjects

“…The interactions between stress and vestibular functions have been investigated in animal models and in clinical studies [ 1 , 50 ] and the possible functional consequences of the consistent SBP, MAP and HR changes evoked by vestibular stimulation have been reported in a healthy population [ 51 ]. We cannot exclude that activating component of vestibular apparatus different from those activated in the present study by CVT might elicit different somatic (muscle, skin, cardiovascular output, etc) and neuro-endocrine responses [ 52 ]. Further research is needed before we can establish the potential importance of vestibular input to cardiovascular regulation and orthostatic tolerance in humans.…”

Understanding vestibular-related physiological functions could provide clues on adapting to a new gravitational environment

“…Gravitational change is a stressor that is detected by the peripheral vestibular apparatus, including otolith organs. Short-term gravity changes, including microgravity and hypergravity, or GVS activate the sympathetic nervous system in rodents and humans [24,26,66,67]. Therefore, it is possible that stress detected by the peripheral vestibular organs induces hyperthermia with a similar response to that of other stressors, including air jet, restraint, social defeat, novel cage, cage switch, and handling [68].…”