Evaluating intermuscular Golgi tendon organ feedback with twitch contractions

• Type of Material: Article
• Authors: Mark Lyle, Emory University; T. Richard Nichols, Georgia Institute of Technology
• Language: English
• Date: 2019-07-08
• Publisher: Wiley
• Publication Version: Author Accepted Manuscript (After Peer Review)
• Copyright Statement: © 2019 The Authors. The Journal of Physiology © 2019 The Physiological Society.
• Final Published Version (URL): http://dx.doi.org/10.1113/JP277363
• Title of Journal or Parent Work: Journal of Physiology London
• Volume: 597
• Issue: 17
• Start Page: 4627
• End Page: 4642
• Grant/Funding Information: The study was supported by a NRSA Postdoctoral Fellowship (F32NS080393) to M. Lyle and HD32571 to TR Nichols.
• Keywords: Neurosciences & Neurology; Mechanical actions; Hindlimb extensors; muscle spindle; Force feedback; Golgi tendon organ; Neurosciences; Inhibition; Science & Technology; Triceps surea muscles; Group I afferents; Ankle; Soleus muscle; spinal reflex; stretch reflex; Heterogenic reflexes; force feedback; Physiology; Life Sciences & Biomedicine; Pathways
• Research Categories: Biology, Neuroscience; Biology, Physiology; Health Sciences, Rehabilitation and Therapy

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.