Vestibular modulation of muscle sympathetic nerve activity by the utricle during sub-perceptual sinusoidal linear acceleration in humans

Abstract

We assessed the capacity for the vestibular utricle to modulate muscle sympathetic nerve activity (MSNA) during sinusoidal linear acceleration at amplitudes extending from imperceptible to clearly perceptible. Subjects (n = 16) were seated in a sealed room, eliminating visual cues, mounted on a linear motor that could deliver peak sinusoidal accelerations of 30 mG in the antero-posterior direction. Subjects sat on a padded chair with their neck and head supported vertically, thereby minimizing somatosensory cues, facing the direction of motion in the anterior direction. Each block of sinusoidal motion was applied at a time unknown to subjects and in a random order of amplitudes (1.25, 2.5, 5, 10, 20 and 30 mG), at a constant frequency of 0.2 Hz. MSNA was recorded via tungsten microelectrodes inserted into muscle fascicles of the common peroneal nerve. Subjects used a linear potentiometer aligned to the axis of motion to indicate any perceived movement, which was compared with the accelerometer signal of actual room movement. On average, 67% correct detection of movement did not occur until 6.5 mG, with correct knowledge of the direction of movement at ~10 mG. Cross-correlation analysis revealed potent sinusoidal modulation of MSNA even at accelerations subjects could not perceive (1.25-5 mG). The modulation index showed a positive linear increase with acceleration amplitude, such that the modulation was significantly higher (25.3 ± 3.7%) at 30 mG than at 1.25 mG (15.5 ± 1.2%). We conclude that selective activation of the vestibular utricle causes a pronounced modulation of MSNA, even at levels well below perceptual threshold, and provides further evidence in support of the importance of vestibulosympathetic reflexes in human cardiovascular control.

Vestibular modulation of muscle sympathetic nerve activity during sinusoidal linear acceleration in supine humans

“…However, GVS modulates afferent activity from the entire vestibular apparatus, and whilst there is considerable evidence supporting the otoliths being the source of the vestibulosympathetic responses (Yates et al, 1993 ), even during sinusoidal GVS (Cohen et al, 2012 ; Holstein et al, 2012 ), we do not know whether the modulation is of utricular and/or saccular origin. To further investigate the afferent source of the vestibulosympathetic reflexes, we recently employed physiological stimulation to target the utricle selectively: applying slow sinusoidal linear accelerations (0.08 Hz) in the horizontal plane to subjects seated (head vertical) on a motorized platform showed that sympathetic activity to both muscle (Hammam et al, 2013 , 2014 ) and skin (Grewal et al, 2012 ) was sinusoidally modulated in a manner similar to that we had seen with sinusoidal GVS. In the current study we sought to investigate whether physiological activation of the saccule—which normally is sensitive to acceleration in the vertical (gravitational) plane—affects sympathetic outflow to muscle.…”

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

“…To further quantify the capacity for subjects to perceive motion and accurately detect the direction of displacement during sinusoidal linear acceleration, we exposed participants to a range of acceleration amplitudes, extending from 1.25 to 30 mG at 0.2 Hz. As illustrated in Figure 8, the average threshold required to be able to detect the motion is 6.5 mG, while the acceleration required to accurately determine the direction of motion is 10.2 mG (74). Despite the fact that subjects could not perceive motion <6 mG, vestibular modulation of MSNA was apparent even at the lowest acceleration tested—1.25 mG (74).…”

“…As illustrated in Figure 8, the average threshold required to be able to detect the motion is 6.5 mG, while the acceleration required to accurately determine the direction of motion is 10.2 mG (74). Despite the fact that subjects could not perceive motion <6 mG, vestibular modulation of MSNA was apparent even at the lowest acceleration tested—1.25 mG (74). Modulation of MSNA at 1.25 mG and 30 mG is shown for one subject in Figure 9.…”

“…The superimposed sinusoid schematically represents the acceleration profile of the platform: motion in the forward direction is indicated by the positive phase of the sinusoid, which includes the period of acceleration before the peak and deceleration after the peak. Reproduced with permission from Hammam et al (74). …”

Systems physiology of the baroreflex during orthostatic stress: from animals to humans

“…Accordingly, other mechanisms may be responsible for the overshoot of the orthostatic MSNA response in the faster HUT test. One possibility is a vestibulo-sympathetic response (Hammam et al, 2014; Yates et al, 2014). Another possibility is an effect of antigravity muscle contraction on SNA, since head-up suspension that removes antigravity muscle contractions caused smaller MSNA activation than HUT (Shamsuzzaman et al, 1998).…”