Ancestral persistence of vestibulospinal reflexes in axial muscles in humans

J Neurophysiol. 2020 May 1;123(5):2010-2023. doi: 10.1152/jn.00421.2019. Epub 2020 Apr 22.

Abstract

Most studies addressing the role of vestibulospinal reflexes in balance maintenance have mainly focused on responses in the lower limbs, while limited attention has been paid to the output in trunk and back muscles. To address this issue, we tested whether electromyographic (EMG) responses to galvanic vestibular stimulations (GVS) were modulated similarly in back and leg muscles, in situations where the leg muscle responses to GVS are known to be attenuated. Body sway and surface EMG signals were recorded in the paraspinal and limb muscles of humans (n = 19) under three complementary conditions. During treadmill locomotion, EMG responses in the lower limbs were observed only during stance, whereas responses in trunk muscles were observed during all phases of the locomotor cycle. During upright standing, a slight head contact abolished the responses in the lower limbs, while the responses remained present in back muscles. Similarly, during parabolic flight-induced microgravity, EMG responses in lower limb muscles were suppressed but remained in axial muscles despite the abolished gravitational otolithic drive. Our results suggest a differentiated control of axial and appendicular muscles when a perturbation is detected by vestibular inputs. The persistence and low modulation of axial muscle responses suggests that a hard-wired reflex is functionally efficient to maintain posture. By contrast, the ankle responses to GVS occur only in balance tasks when proprioceptive feedback is congruent. This study using GVS in microgravity is the first to present an approach delineating feedforward vestibular control in unconstrained environment.NEW & NOTEWORTHY This study addresses the extent of conservation of trunk muscle control in humans. Results show that galvanic vestibular stimulation-evoked vestibular responses in trunk muscles remain strong in conditions where leg muscle responses are downmodulated (walking, standing, microgravity). This suggests a phylogenetically conserved blueprint of sensorimotor organization, with strongly hardwired vestibulospinal inputs to axial motoneurons and a higher degree of flexibility in the later emerging limb control system.

Keywords: gait; galvanic vestibular stimulation; locomotion; microgravity; posture.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Electric Stimulation
  • Electromyography
  • Humans
  • Leg / physiology*
  • Motor Neurons / physiology*
  • Muscle, Skeletal / physiology*
  • Paraspinal Muscles / physiology
  • Postural Balance / physiology*
  • Reflex / physiology*
  • Spinal Cord / physiology*
  • Vestibule, Labyrinth / physiology*