The concerted activity in parallel proprioceptive pathways controls the initiation of co-activation in the locust kick motor programme

Eur J Neurosci. 1997 Jan;9(1):55-64. doi: 10.1111/j.1460-9568.1997.tb01353.x.

Abstract

To jump and kick the locust uses a catapult mechanism implemented by a three-stage motor programme: initial flexion of the hind tibiae, co-activation of the antagonist flexor and extensor tibiae motor neurons and trigger inhibition of the flexor motorneurons. The transition from stage 1 to stage 2 thus involves a switch from the normal alternate activation to co-activation of the antagonist tibrae motorneurons. However, co-activation has never been observed when the central nervous system has been isolated from the leg. This led us to investigate the possibility that the transition from stage 1 to stage 2 is controlled by a proprioceptive signal. In the first set of experiments intracellular recordings were made in the flexor and extensor motorneurons while the position of the tendon of the femoral chordotonal organ (FCO), which signals tibial position and movement, was experimentally controlled. In these heavily dissected preparations, stretch of the FCO tendon (signalling tibial flexion) was a necessary condition for co-activation. However, in minimally dissected preparations (in which merely EMG recordings were made), we found that co-activation occurred even when the FCO was signalling tibial extension, suggesting the involvement of other proprioceptors. A series of experiments were then conducted on minimally dissected preparations to determine the relative contributions of each of the three main hind leg proprioceptors which might signal tibial flexion: the FCO, the lump receptor and Brünners organ. When all three proprioceptors were intact the chance of evoking co-activation was largest, when all three were eliminated co-activation could no longer be evoked, irrespective of the level of arousal. Various combinations of partial de-afferentation showed that the FCO plays the major role, with the lump receptor and Bünners organ playing significant, but progressively less important, roles. We conclude that the three receptors act together as a permissive proprioceptive gate for the kick and jump motor programme, but with a hierarchy of the strengths of their effectiveness.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Electromyography
  • Extremities / innervation
  • Extremities / physiology
  • Female
  • Grasshoppers / physiology*
  • In Vitro Techniques
  • Instinct
  • Male
  • Mechanoreceptors / physiology
  • Movement / physiology*
  • Muscles / innervation
  • Muscles / physiology
  • Neural Pathways / physiology
  • Proprioception / physiology*
  • Reflex, Stretch / physiology