Sensory Feedback in Interlimb Coordination: Contralateral Afferent Contribution to the Short-Latency Crossed Response during Human Walking

PLoS One. 2017 Jan 6;12(1):e0168557. doi: 10.1371/journal.pone.0168557. eCollection 2017.

Abstract

A constant coordination between the left and right leg is required to maintain stability during human locomotion, especially in a variable environment. The neural mechanisms underlying this interlimb coordination are not yet known. In animals, interneurons located within the spinal cord allow direct communication between the two sides without the need for the involvement of higher centers. These may also exist in humans since sensory feedback elicited by tibial nerve stimulation on one side (ipsilateral) can affect the muscles activation in the opposite side (contralateral), provoking short-latency crossed responses (SLCRs). The current study investigated whether contralateral afferent feedback contributes to the mechanism controlling the SLCR in human gastrocnemius muscle. Surface electromyogram, kinematic and kinetic data were recorded from subjects during normal walking and hybrid walking (with the legs moving in opposite directions). An inverse dynamics model was applied to estimate the gastrocnemius muscle proprioceptors' firing rate. During normal walking, a significant correlation was observed between the magnitude of SLCRs and the estimated muscle spindle secondary afferent activity (P = 0.04). Moreover, estimated spindle secondary afferent and Golgi tendon organ activity were significantly different (P ≤ 0.01) when opposite responses have been observed, that is during normal (facilitation) and hybrid walking (inhibition) conditions. Contralateral sensory feedback, specifically spindle secondary afferents, likely plays a significant role in generating the SLCR. This observation has important implications for our understanding of what future research should be focusing on to optimize locomotor recovery in patient populations.

MeSH terms

  • Adult
  • Afferent Pathways
  • Electromyography
  • Feedback, Sensory*
  • Female
  • Humans
  • Leg / physiology
  • Mechanoreceptors / physiology
  • Muscle, Skeletal / innervation*
  • Muscle, Skeletal / physiology
  • Psychomotor Performance*
  • Reaction Time
  • Walking / physiology*
  • Young Adult

Grants and funding

This study was supported by the Obel Family Foundation, the Spar Nord Fonden and by the European Union FP7 program under the project H2R (grant agreement n° 600698). Obelske Familiefonden (grant number n/a) provided funding for purchase of equipment used during data collection. Det Frie Forskningsråd (grant agreement n° 10-082524) provided funding for purchase of equipment used during data collection. The European Union FP7 program under the project H2R (grant agreement n° 600698) provided funding for purchase of equipment used during data collection. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.