Task, muscle and frequency dependent vestibular control of posture

Abstract

The vestibular system is crucial for postural control; however there are considerable differences in the task dependence and frequency response of vestibular reflexes in appendicular and axial muscles. For example, vestibular reflexes are only evoked in appendicular muscles when vestibular information is relevant to postural control, while in neck muscles they are maintained regardless of the requirement to maintain head on trunk balance. Recent investigations have also shown that the bandwidth of vestibular input on neck muscles is much broader than appendicular muscles (up to a factor of 3). This result challenges the notion that vestibular reflexes only contribute to postural control across the behavioral and physiological frequency range of the vestibular organ (i.e., 0-20 Hz). In this review, we explore and integrate these task-, muscle- and frequency-related differences in the vestibular system's contribution to posture, and propose that the human nervous system has adapted vestibular signals to match the mechanical properties of the system that each group of muscles controls.

Keywords: appendicular muscles; axial muscles; frequency response; postural control; task dependent; vestibular reflexes.

Figure 1

Signal processing pathways and evoked reflex responses as a result of mechanical perturbations and/or electrical stimulation. Input stimuli span specific bandwidths (see spectra, mechanical: 0–4 Hz; electrical stimulation: 0–75 Hz) and when applied to the head generate vestibular afferent activity. Note: the representative mechanical perturbation is applied via the torso and limited to less than 10 Hz on account of the bandwidth of mechanical device applying the perturbation and the biomechanics of the human body. Consequently, the evoked responses in axial and appendicular muscles are presented only in response to electrical stimuli with identical bandwidths (0–75 Hz). Afferent signals descend through the vestibular nuclei (VN) to axial and appendicular muscle motoneurons. The evoked reflexes in axial muscles have much shorter latencies than those in appendicular muscles (8 ms vs. 50 ms). Different time scales were used to illustrate the evoked responses (250 ms vs. 150 ms). (Data for cumulant density plots and perturbation/stimulation signals are adapted from Forbes et al., 2013a,b, 2014).

Figure 2

Coherence, gain, and phase frequency estimates of vestibular reflexes for r-SOL and r-SCM muscles elicited by a 0–75 Hz stochastic electrical vestibular stimulus. Vestibular reflexes in the r-SCM span a much wider bandwidth (~0–70 Hz) together with high gains and moderate phase lags relative to the r-SOL. The horizontal, segmented line in the coherence plot represents the level above which the coherence is significant. The horizontal, segmented line in the phase plot represents a phase of zero. r-SCM, right sternocleidomastoid; r-SOL, right soleus. (Data are adapted from Forbes et al., 2013a).

Figure 3

Effect of postural task on appendicular and axial muscles. In appendicular muscles (left plots), vestibular reflex frequency- and time-domain estimates (i.e., coherence and cumulant density respectively) are suppressed when a subject is standing with the torso fixed to a rigid support. In axial muscles (right plots), vestibular reflex responses are maintained when the subject’s head is fixed with respect to the torso. Thus, vestibular-evoked responses are present in axial muscles, unlike appendicular muscles, regardless of the postural task. r-SOL, right soleus; r-SCM, right sternocleidomastoid. The horizontal, segmented lines in the coherence plots represent the level above which the coherence is significant. (Data are adapted from Luu et al., ; Forbes et al., 2014).