Trends in Neurosciences
Volume 13, Issue 12, December 1990, Pages 499-505
Journal home page for Trends in Neurosciences

Presynaptic inhibition of muscle spindle and tendon organ afferents in the mammalian spinal cord

https://doi.org/10.1016/0166-2236(90)90084-NGet rights and content

Abstract

More than 30 years ago, Frank and Fuortes proposed that the synaptic effectiveness of muscle spindle afferents associated with spinal motoneurones could be diminished by the activation of nerves from flexor muscles. Since that time, research has focused on disclosing the mode of operation and the spinal pathways involved in this presynaptic inhibitory control. Initially, it was assumed that the same last-order interneurones mediated presynaptic inhibition of both muscle spindle and tendon organ afferent fibres. More recent evidence indicates that the synaptic effectiveness of these two groups of afferents is controlled by separate sets of GABAergic interneurones synapsing directly with the intraspinal terminals of the afferent fibres. This unique arrangement allows for selective control of the information on muscle length or muscle tension, despite the convergence of muscle spindle and tendon organ afferents on second-order interneurones.

References (75)

  • R.A. Levy

    Progr. Neurobiol.

    (1977)
  • W.C. De Groat et al.

    Brain Res.

    (1972)
  • S. Fox et al.

    Neurosci.

    (1978)
  • R.E.W. Fyffe et al.

    Brain Res.

    (1984)
  • D.J. Maxwell et al.

    Brain Res.

    (1983)
  • E. Carstens et al.

    Brain Res.

    (1981)
  • B.P. Sastry

    Eur. J. Pharmacol.

    (1978)
  • K. Frank et al.
  • K. Frank

    Inst. Radio Eng. Trans. Med. Electron.

    (1959)
  • R.E. Burke et al.
  • J.C. Eccles et al.

    J. Physiol.

    (1962)
  • E. Eide et al.
  • R. Granit
  • R. Granit et al.

    J. Physiol.

    (1964)
  • J.O. Kellerth
  • W.A. Cook et al.

    J. Neurophysiol.

    (1972)
  • P. Rudomin et al.

    J. Neurophysiol.

    (1975)
  • P.L. Carlen et al.

    J. Physiol.

    (1980)
  • M. Kuno

    J. Physiol.

    (1964)
  • J.D. Clements et al.

    J. Physiol.

    (1987)
  • E. Henneman et al.

    J. Physiol.

    (1984)
  • H.R. Luscher
  • S.J. Redman et al.

    J. Physiol.

    (1983)
  • D.H. Barron et al.

    J. Physiol.

    (1938)
  • D.I. Carpenter et al.

    Arch. Ital. Biol.

    (1966)
  • J.C. Eccles et al.

    J. Physiol.

    (1962)
  • T. Hongo et al.

    Exp. Brain Res.

    (1972)
  • S. Lund et al.

    Acta Physiol. Scand.

    (1965)
  • A. Lundberg et al.

    Arch. Ital. Biol.

    (1966)
  • P.D. Wall

    J. Physiol.

    (1958)
  • A. Lev-Tov et al.

    J. Neurophysiol.

    (1983)
  • I. Jiménez et al.

    Exp. Brain Res.

    (1988)
  • H. Gasser et al.

    Am. J. Physiol.

    (1933)
  • N. Kriz et al.

    J. Physiol.

    (1975)
  • G.T. Bruggencate et al.

    Pflügers Arch.

    (1974)
  • E.W. Lothman et al.

    J. Physiol.

    (1975)
  • I. Jiménez et al.

    J. Neurophysiol.

    (1984)
  • Cited by (202)

    • Fundamental contributions of the cat model to the neural control of locomotion

      2020, The Neural Control of Movement: Model Systems and Tools to Study Locomotor Function
    • The lesion of dorsolateral funiculus changes the antiallodynic effect of the intrathecal muscimol and baclofen in distinct phases of neuropathic pain induced by spinal nerve ligation in rats

      2016, Brain Research Bulletin
      Citation Excerpt :

      In fact, the excitability of spinal neurons is physiologically modulated by peripheral afferents and neurons from supraspinal nuclei, which project their axons along the spinal cord (Castro et al., 2006). Vestibular and rubrospinal terminals that descend through the DLF are not modulated by presynaptic GABAA receptors (Curtis and Malik, 1984, 1985; Curtis et al., 1984; Delgado-Lezama et al., 2004; Rudomin, 1990). However, GABAB receptors inhibit the release of neurotransmitters by axons of neurons that descend in the DLF to control spinal motoneurons in cats (Curtis and Malik, 1985; Jiménez et al., 1991) and turtles (Delgado-Lezama et al., 2004).

    • State-dependent modulation of locomotion by GABAergic spinal sensory neurons

      2015, Current Biology
      Citation Excerpt :

      During active locomotion, sensory afferent neurons provide excitatory feedback to motor neurons and spinal interneurons in response to muscle contraction. Local GABAergic interneurons can modulate this pathway by inhibiting sensory afferents at the presynaptic level [1, 2]. Genetic targeting and manipulation of these GABAergic interneurons recently demonstrated the importance of presynaptic modulation of sensory afferents to control fine motor behaviors in mice [3, 4].

    • Error signals as powerful stimuli for the operant conditioning-like process of the fictive respiratory output in a brainstem-spinal cord preparation from rats

      2014, Behavioural Brain Research
      Citation Excerpt :

      1) The Golgi tendon afferents from one muscle contribute to the functional control of muscle groups as a whole and, vice versa, the afferent information forwarded to individual motorneurons is affected by the length and tension of many muscles. This is in contrast with the view that the function of Golgi tendon organs is to contribute to a feed-back system controlling the homonymous muscle, since muscles are not normally activated in isolation and the afferents from several muscles are fused together before reaching specific motorneurons [40,41]. ( 2) Although these organs do not have a specific centrifugal system that control their ability to respond, they are frequently anatomically associated with muscle spindles to form dyads, in parallel [42,43] or in series with Golgi receptors attached to intrafusal fibers [43,44].

    View all citing articles on Scopus
    View full text