Evaluating intermuscular Golgi tendon organ feedback with twitch contractions

• Authors: Mark Lyle, Emory University; T. Richard Nichols, Georgia Institute of Technology
• Journal Title: Journal of Physiology London
• Volume: Volume 597, Number 17
• Publisher: Wiley | 2019-07-08, Pages 4627-4642
• Type of Work: Article | Post-print: After Peer Review
• Publisher DOI: http://doi.org/10.1113/JP277363
• Subjects: Biology, Physiology; Biology, Neuroscience; Health Sciences, Rehabilitation and Therapy
• Keywords: Science & Technology; Life Sciences & Biomedicine; Neurosciences; Physiology; Neurosciences & Neurology; Golgi tendon organ; force feedback; spinal reflex; muscle spindle; stretch reflex; Triceps surea muscles; Group I afferents; Heterogenic reflexes; Hindlimb extensors; Mechanical actions; Force feedback; Soleus muscle; Inhibition; Pathways; Ankle

Abstract

Force feedback from Golgi tendon organs (GTOs) has widespread intermuscular projections mediated by interneurons that share inputs from muscle spindles, among others. Because current methods to study GTO circuitry (nerve stimulation or muscle stretch) also activate muscle spindle afferents, the selective role of GTOs remains uncertain. Here, we tested the hypothesis that intramuscular stimulation evoked twitch contractions could be used to naturally bias activation of GTOs and thus evaluate their intermuscular effects in decerebrate cats. This was achieved by comparing the effects of twitch contractions and stretches as donor inputs onto the motor output of recipient muscles. Donor–recipient pairs evaluated included those already known in the cat to receive donor excitatory muscle spindle feedback only, inhibitory GTO feedback only, and both excitatory spindle and inhibitory GTO effects. Muscle stretch, but not twitch contractions, evoked excitation onto recipient muscles with muscle spindle afferent inputs only. Both donor muscle stretch and twitch contractions inhibited a recipient muscle with GTO projections only. In a recipient muscle that receives both muscle spindle and GTO projections, donor muscle stretch evoked both excitatory and inhibitory effects, whereas twitch contractions evoked inhibitory effects only. These data support the hypothesis that muscle stimulation evoked contractions can induce intermuscular effects most consistent with mechanical GTO receptor activation and not direct activation of sensory axons. We propose this approach can be used to evaluate GTO circuitry more selectively than muscle stretch or nerve stimulation and can be adapted to study GTO feedback non-invasively in freely moving cats and humans.