Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Post-tetanic influences on primary afferent depolarization in the cat spinal cord

Summary

In the spinal cord of pentobarbitone anaesthetised cats, increases in the electrical threshold of the terminations of extensor muscle group Ia afferent fibres, produced by tetanic stimulation of either the appropriate peripheral nerve or the central termination, were associated with parallel changes in the bicuculline-sensitive reduction in electrical threshold of the termination produced synaptically by impulses in flexor muscle low threshold afferent fibres (primary afferent depolarization, PAD) or by microelectrophoretic piperidine-4-sulphonic acid (P4S), an analogue of GABA. Since this post-tetanic hyperpolarization (PTH) could be produced by tetanic stimulation of a single termination centrally, and not by peripheral stimulation of heteronymous nerves, it presumably resulted from changes intrinsic to the tetanized termination. Increases in PAD and the effectiveness of P4S were probably associated with post-tetanic activation of an electrogenic Na+/K+ pump as the predominant cause of PTH, whereas decreases may have been largely the consequence of post-tetanic increases in intracellular Ca2+ levels. These results provide further evidence that GABA is the depolarizing transmitter at axo-axonic synapses upon primary afferent terminals, and that the underlying membrane conductance increase has a reversal potential at a more depolarized level than the resting potential.

This is a preview of subscription content, log in to check access.

References

  1. Baker M, Bostock H, Grafe P, Martius P (1987) Function and distribution of three types of rectifying channel in rat spinal root myelinated axons. J Physiol (Lond) 383: 45–67

  2. Barrett EF, Barrett JN (1982) Intracellular recording from vertebrate myelinated axons: mechanism of the depolarizing after-potential. J Physiol (Lond) 323: 117–144

  3. Bostock H, Grafe P (1985) Activity-dependent excitability changes in normal and demyelinated rat spinal root axons. J Physiol (Lond) 365: 239–257

  4. Connelly CM (1959) Recovery processes and metabolism of nerve. Rev Mod Phys 31: 475–484

  5. Curtis DR (1979) A method for continuously monitoring the electrical threshold of single intraspinal nerve fibres. Electroencephalogr Clin Neurophysiol 47: 503–506

  6. Curtis DR, Lodge D (1982) The depolarization of feline ventral horn group Ia spinal afferent terminations by GABA. Exp Brain Res 46: 215–233

  7. Curtis DR, Lodge D, Bornstein JC, Peet MJ, Leah JD (1982) The dual effects of GABA and related amino acids on the electrical threshold of ventral horn group Ia afferent terminations in the cat. Exp Brain Res 48: 387–400

  8. Curtis DR, Gynther BD, Malik R (1986) A pharmacological study of group I muscle afferent terminals and synaptic excitation in the intermediate nucleus and Clarke's column of the cat spinal cord. Exp Brain Res 64: 105–113

  9. Eccles JC, Krnjević K (1959) Potential changes recorded inside primary afferent fibres within the spinal cord. J Physiol (Lond) 149: 250–273

  10. Eccles JC, Eccles RM, Lundberg A (1957) The convergence of monosynaptic excitatory afferents on to many different species of alpha motoneurones. J Physiol (Lond) 137: 22–50

  11. Eccles JC, Magni F, Willis WD (1962) Depolarization of central terminals of group I afferent fibres from muscle. J Physiol (Lond) 160: 62–93

  12. Eccles JC, Schmidt RF, Willis WD (1963) The mode of operation of the synaptic mechanism producing presynaptic inhibition. J Neurophysiol 26: 523–538

  13. Gage PW, Hubbard JI (1966a) The origin of the post-tetanic hyperpolarization of mammalian motor nerve terminals. J Physiol (Lond) 184: 335–352

  14. Gage PW, Hubbard JI (1966b) An investigation of the post-tetanic potentiation of end-plate potentials at a mammalian neuromuscular junction. J Physiol (Lond) 184: 353–375

  15. Gallagher JP, Higashi H, Nishi S (1978) Characterization and ionic basis of GABA-induced depolarizations recorded in vitro from cat primary afferent neurones. J Physiol (Lond) 275: 263–282

  16. Gasser HS, Grundfest H (1936) Action and excitability in mammalian A fibers. Am J Physiol 117: 113–133

  17. Inoue M, Tokutomi N, Akaike N (1987) Modulation of the γ-aminobutyric acid-gated chloride current by intracellular calcium in frog sensory neurones. Jpn J Physiol 37: 379–391

  18. Kretz R, Shapiro E, Kandel ER (1982) Post-tetanic potentiation at an identified synapse in Aplysia is correlated with a Ca2+-activated K+ current in the presynaptic neuron: evidence for Ca2+ accumulation. Proc Natl Acad Sci USA 79: 5430–5434

  19. Krnjević K, Leblond J (1987) Anoxia reversibly suppresses neuronal calcium currents in rat hippocampal slices. Can J Physiol Pharmacol 65: 2157–2161

  20. Lev-Tov A, Fleshman JW, Burke RE (1983) Primary afferent depolarization and presynaptic inhibition of monosynaptic group Ia EPSPs during posttetanic potentiation. J Neurophysiol 50: 413–427

  21. Lev-Tov A, Meyers DER, Burke RE (1988) Modification of primary afferent depolarization in cat group Ia afferents following high frequency intra-axonal tetanization of individual afferents. Brain Res 438: 328–330

  22. Mallart A (1985) A calcium-activated potassium current in motor nerve terminals of the mouse. J Physiol (Lond) 368: 577–591

  23. Meech RW (1974) Calcium influx induces a post-tetanic hyperpolarization in Aplysia neurones. Comp Biochem Physiol [A] 48: 387–395

  24. Nussinovitch I, Rahamimoff R (1988) Ionic basis of tetanic and post-tetanic potentiation at a mammalian neuromuscular junction. J Physiol (Lond) 396: 435–455

  25. Penner R, Dreyer F (1986) Two different presynaptic calcium currents in mouse motor nerve terminals. Pflügers Arch 406: 190–197

  26. Rang HP, Ritchie JM (1968) On the electrogenic sodium pump in mammalian non-myelinated nerve fibres and its activation by various external cations. J Physiol (Lond) 196: 183–221

  27. Rudomin P, Engberg I, Jimenez I (1981) Mechanisms involved in presynaptic depolarization of group I and rubrospinal fibers in cat spinal cord. J Neurophysiol 46: 532–548

  28. Taleb O, Trouslard J, Demeneix BA, Feltz P, Bossu J-L, Dupont J-L, Feltz A (1987) Spontaneous and GABA-evoked chloride channels on pituitary intermediate lobe cells and their internal Ca requirements. Pflügers Arch 409: 620–631

  29. Thomas RC (1972) Electrogenic sodium pump in nerve and muscle cells. Physiol Rev 52: 563–594

  30. Thompson SM, Prince DA (1986) Activation of electrogenic sodium pump in hippocampal CA1 neurons following glutamate-induced depolarization. J Neurophysiol 56: 507–522

  31. Wall PD (1958) Excitability changes in afferent fibre terminations and their relation to slow potentials. J Physiol (Lond) 142: 1–21

  32. Wall PD, Johnson AR (1958) Changes associated with post-tetanic potentiation of a monosynaptic reflex. J Neurophysiol 21: 148–158

Download references

Author information

Correspondence to D. R. Curtis.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Gynther, B.D., Curtis, D.R. Post-tetanic influences on primary afferent depolarization in the cat spinal cord. Exp Brain Res 74, 365–374 (1989). https://doi.org/10.1007/BF00248870

Download citation

Key words

  • Cat spinal cord
  • Primary afferent terminations
  • Post-tetanic hyperpolarization
  • GABA-mediated depolarization