Vestibular contribution to motor output is also suppressed by voluntary action of the arm

Abstract

The vestibular sensory system is among the oldest and most fundamental contributors to motor behaviour as it is critical to maintaining posture and balance. However such low-level motor responses could interfere with cortically mediated voluntary behaviour that naturally involves posture and balance. Consequently, it has been proposed that – much like the inhibition of reflex responses – vestibular contributions to motor output are ‘gated’ (dubbed vestibular suppression) to avoid undesirable self-perturbations during voluntary head movements. Here we demonstrate that such suppression also occurs for unperturbed voluntary arm function. Our evidence comes from comparing coherence at baseline (No Stimulation) and after Sham and Galvanic Vestibular Stimulation (GVS). Specifically neck muscles showed shared neural drive (intermuscular coherence [IMC]), which increased with GVS – but not Sham – at Rest. This GVS-mediated increased coherence in neck muscles, however, was suppressed during voluntary isometric contractions and reaching movements of the arm on the same side as the GVS was applied. No changes were found in pairwise IMC during Sham (compared with No stimulation) or in arm muscles either at rest or during voluntary movement during GVS in neurotypical adults. In addition to extending vestibular suppression to unperturbed voluntary arm function, these results provide support for the common (yet unproven to our knowledge) notion that arm muscles do not receive vestibular neural drive during unperturbed voluntary movement. Moreover, these results shed light on the mechanisms that mediate competing descending outputs for voluntary function and serve as a baseline against which to compare potential task-dependent dysregulation of vestibular-mediated output to the neck and arms in stroke and neurological conditions.

Key points

• The vestibular system is critical for correcting perturbations during voluntary movement.
• During voluntary head movements, vestibular suppression occurs to avoid undesirable self-perturbations.
• However, the contribution of the vestibular system to unperturbed voluntary arm movement remains unclear.
• We used intermuscular coherence (IMC) to measure vestibulospinal drive to neck and arm muscles while applying Galvanic Vestibular Stimulation (GVS), Sham and No Stimulation. We compared IMC at Rest and unperturbed voluntary movement of the arm in neurotypical adults.
• Neck muscles showed increased shared neural drive at rest, only when GVS was applied. However, vestibular drive was suppressed during unperturbed voluntary isometric contractions and reaching movements of the arm.
• Vestibular drive to arm muscles did not increase when GVS was applied.
• We provide evidence that arm muscles do not receive vestibulospinal drive, excluding its contribution to unperturbed voluntary movement.
• These results could provide valuable insights into the vestibular contribution to motor impairments following neurological conditions such as stroke.