Rapid limb‐specific modulation of vestibular contributions to ankle muscle activity during locomotion

• Published in: The Journal of physiology Vol. 595; no. 6; pp. 2175 - 2195
• Main Authors: Forbes, Patrick A., Vlutters, Mark, Dakin, Christopher J., der Kooij, Herman, Blouin, Jean‐Sébastien, Schouten, Alfred C.
• Format: Journal Article
• Language: English
• Published: England Wiley Subscription Services, Inc 15.03.2017; John Wiley and Sons Inc
• Subjects: Adult; Biomechanical Phenomena; Cognitive and Behavioural Neuroscience; Electromyography; Female; Humans; limb‐specific vestibular contributions; Lower Extremity - physiology; Male; Muscle, Skeletal - physiology; Neuroscience; Neuroscience ‐ Behavioural/Systems/Cognitive; Research Paper; Sensory Neuroscience; split‐belt locomotion; Vestibular Nuclei - physiology; vestibulo‐muscular coupling; Walking - physiology; Young Adult; limb-specific vestibular contributions; split-belt locomotion; vestibulo-muscular coupling
• ISSN: 0022-3751; 1469-7793; 1469-7793
• DOI: 10.1113/JP272614

Key points The vestibular influence on human walking is phase‐dependent and modulated across both limbs with changes in locomotor velocity and cadence. Using a split‐belt treadmill, we show that vestibular influence on locomotor activity is modulated independently in each limb. The independent vestibular modulation of muscle activity from each limb occurs rapidly at the onset of split‐belt walking, over a shorter time course relative to the characteristic split‐belt error‐correction mechanisms (i.e. muscle activity and kinematics) associated with locomotor adaptation. Together, the present results indicate that the nervous system rapidly modulates the vestibular influence of each limb separately through processes involving ongoing sensory feedback loops. These findings help us understand how vestibular information is used to accommodate the variable and commonplace demands of locomotion, such as turning or navigating irregular terrain. During walking, the vestibular influence on locomotor activity is phase‐dependent and modulated in both limbs with changes in velocity. It is unclear, however, whether this bilateral modulation is due to a coordinated mechanism between both limbs or instead through limb‐specific processes that remain masked by the symmetric nature of locomotion. Here, human subjects walked on a split‐belt treadmill with one belt moving at 0.4 m s−1 and the other moving at 0.8 m s−1 while exposed to an electrical vestibular stimulus. Muscle activity was recorded bilaterally around the ankles of each limb and used to compare vestibulo‐muscular coupling between velocity‐matched and unmatched tied‐belt walking. In general, response magnitudes decreased by ∼20–50% and occurred ∼13–20% earlier in the stride cycle at the higher belt velocity. This velocity‐dependent modulation of vestibular‐evoked muscle activity was retained during split‐belt walking and was similar, within each limb, to velocity‐matched tied‐belt walking. These results demonstrate that the vestibular influence on ankle muscles during locomotion can be adapted independently to each limb. Furthermore, modulation of vestibular‐evoked muscle responses occurred rapidly (∼13–34 strides) after onset of split‐belt walking. This rapid adaptation contrasted with the prolonged adaptation in step length symmetry (∼128 strides) as well as EMG magnitude and timing (∼40–100 and ∼20–70 strides, respectively). These results suggest that vestibular influence on ankle muscle control is adjusted rapidly in sensorimotor control loops as opposed to longer‐term error correction mechanisms commonly associated with split‐belt adaptation. Rapid limb‐specific sensorimotor feedback adaptation may be advantageous for asymmetric overground locomotion, such as navigating irregular terrain or turning. Key points The vestibular influence on human walking is phase‐dependent and modulated across both limbs with changes in locomotor velocity and cadence. Using a split‐belt treadmill, we show that vestibular influence on locomotor activity is modulated independently in each limb. The independent vestibular modulation of muscle activity from each limb occurs rapidly at the onset of split‐belt walking, over a shorter time course relative to the characteristic split‐belt error‐correction mechanisms (i.e. muscle activity and kinematics) associated with locomotor adaptation. Together, the present results indicate that the nervous system rapidly modulates the vestibular influence of each limb separately through processes involving ongoing sensory feedback loops. These findings help us understand how vestibular information is used to accommodate the variable and commonplace demands of locomotion, such as turning or navigating irregular terrain.