Vestibular Contributions to Primate Neck Postural Muscle Activity during Natural Motion

Abstract

To maintain stable posture of the head and body during our everyday activities, the brain integrates information across multiple sensory systems. Here, we examined how the primate vestibular system, independently and in combination with visual sensory input, contributes to the sensorimotor control of head posture across the range of dynamic motion experienced during daily life. We recorded activity of single motor units in the splenius capitis and sternocleidomastoid muscles in rhesus monkeys during yaw rotations spanning the physiological range of self-motion (up to 20 Hz) in darkness. Splenius capitis motor unit responses continued to increase with frequency up to 16 Hz in normal animals, and were strikingly absent following bilateral peripheral vestibular loss. To determine whether visual information modulated these vestibular-driven neck muscle responses, we experimentally controlled the correspondence between visual and vestibular cues of self-motion. Surprisingly, visual information did not influence motor unit responses in normal animals, nor did it substitute for absent vestibular feedback following bilateral peripheral vestibular loss. A comparison of muscle activity evoked by broadband versus sinusoidal head motion further revealed that low-frequency responses were attenuated when low- and high-frequency self-motion were experienced concurrently. Finally, we found that vestibular-evoked responses were enhanced by increased autonomic arousal, quantified via pupil size. Together, our findings directly establish the vestibular system's contribution to the sensorimotor control of head posture across the dynamic motion range experienced during everyday activities, as well as how vestibular, visual, and autonomic inputs are integrated for postural control.SIGNIFICANCE STATEMENT Our sensory systems enable us to maintain control of our posture and balance as we move through the world. Notably, the vestibular system senses motion of the head and sends motor commands, via vestibulospinal pathways, to axial and limb muscles to stabilize posture. By recording the activity of single motor units, here we show, for the first time, that the vestibular system contributes to the sensorimotor control of head posture across the dynamic motion range experienced during everyday activities. Our results further establish how vestibular, autonomic, and visual inputs are integrated for postural control. This information is essential for understanding both the mechanisms underlying the control of posture and balance, and the impact of the loss of sensory function.

Keywords: motor unit; natural motion; neck muscle; postural control; vestibular; vestibulocollic.

Figure 1.

Experimental paradigm to study descending postural control pathways. A, Illustration of the different descending postural control pathways that can contribute to neck motor unit activity. B, Schematic of our vestibular stimulation protocol where we applied sinusoidal and broadband yaw angular motion containing frequencies up to 20 Hz to head-fixed monkeys. C, The conditions used to manipulate visual feedback to assess visual-vestibular integration for postural control during sinusoidal motion.

Figure 2.

Neck motor units show vestibular-evoked responses across the dynamic range of natural motion. A, SPL motor unit responses to sinusoidal vestibular stimulation in normal monkeys (N = 26 motor units) in the dark. Dashed lines indicate 99% CIs for coherence between rotation velocity and motor unit spike times. Gain (spikes/m/s) and phase lag (deg) of motor unit responses relative to velocity are demonstrated at frequencies with significant coherence. Error bars indicate 95% CIs. Red arrow (at 8 Hz) indicates where the transition occurs between two different phase slopes. The modulation in motor unit firing rate in response to 3 sine wave frequencies (2, 5, and 10 Hz) is shown for one example neuron. B, SPL (N = 6 motor units) responses to the same sinusoidal stimulation after BVL.

Figure 3.

Visual cues do not affect vestibular-evoked postural responses. SPL motor unit responses to sinusoidal vestibular stimulation in healthy monkeys under three different visual conditions: A, complete darkness (N = 26 motor units); B, world-referenced visual surround (N = 18 motor units); C, head-referenced visual surround (N = 26 motor units). Dashed lines indicate 99% CIs for coherence. Gain (spikes/m/s) and phase (deg) data are demonstrated at frequencies with significant coherence. Error bars indicate 95% CIs.

Figure 4.

Motor unit response gains and phases are similar across visual conditions. A, Comparison of motor unit response gain (spikes/m/s) and phase (deg) between the world-referenced surround (N = 18 motor units) and dark (N = 26 motor units) conditions. B, Comparison between the world-referenced and head-referenced (N = 26 motor units) visual conditions. Shaded areas represent 95% CIs.

Figure 5.

Out of plane visual stimulation does not influence vestibular postural reflexes. SPL motor unit responses to sinusoidal vestibular stimulation with a stationary visual scene of dots compared with roll and pitch downward visual motion stimulation. Insets, Comparisons between pitch upward (N = 18 motor units) versus downward (N = 17 motor units), and roll CCW (N = 16 motor units) versus CW (N = 14 motor units).

Figure 6.

Visual cues do not substitute for absent vestibular feedback following bilateral peripheral vestibular loss. SPL motor unit responses (N = 6 motor units) to sinusoidal vestibular stimulation with a world-referenced visual surround (i.e., with accurate visual cues of self-motion) after BVL. Dashed lines indicate 99% CIs for coherence between rotation velocity and motor unit spike times. Error bars indicate 95% CIs.

Figure 7.

Neck motor units show nonlinear responses during complex motion, and responses at high frequencies differ markedly from previous model predictions. A, SPL motor unit responses to broadband (0-20 Hz white noise) vestibular stimulation in normal monkeys (N = 12 motor units). Dashed lines indicate 99% CIs for coherence between rotation velocity and motor unit spike times. Gain (normalized to maximum) and phase (deg) data are demonstrated at frequencies that exhibit significant coherence. Error bars indicate 95% CIs. For comparison, the superimposed dots represent gain for motor units in response to sinusoidal stimulation from Figure 2A. Black lines indicate the predicted VCR gain and phase from the neuromechanical model developed by Peng et al. (1996). B, SPL motor unit responses (N = 5 motor units) to the same broadband vestibular stimulation after BVL.

Figure 8.

Multiunit muscle activity demonstrates similar responses to single motor units. SPL rectified EMG responses to broadband noise (0-20 Hz) vestibular stimulation in healthy (A, N = 15 trials) and BVL (B, N = 6 trials) monkeys. Dashed lines indicate 99% CIs for coherence. Gain (spikes/m/s) and phase (deg) data are demonstrated at frequencies with significant coherence. Error bars indicate 95% CIs.

Figure 9.

SCM motor units demonstrate increasing response gain across the range of natural self-motion. SCM single motor unit (N = 2 motor units) responses to broadband noise (0-20 Hz) vestibular stimulation in a normal monkey. Dashed lines indicate 99% CIs for coherence. Gain (spikes/m/s) and phase (deg) data are demonstrated at frequencies with significant coherence. Error bars indicate 95% CIs.

Figure 10.

Autonomic arousal enhances neck motor unit responses during natural self-motion. A, SPL motor unit responses to broadband noise (0-20 Hz) vestibular stimulation under normal conditions (left, N = 6 motor units) and increased autonomic arousal (right, N = 6 motor units). Dashed lines indicate 99% CIs for coherence between rotation velocity and motor unit spike times. Gain and phase data are demonstrated at frequencies that exhibit significant coherence. B, Comparisons of coherence, gain, and phase between arousal states. Dashed line indicates the significance level for the χ² test. Shaded areas represent 95% CIs.