Summary
The relative contribution of specific and unspecific (potassium) components involved in the generation of primary afferent depolarization (PAD) of cutaneous fibres was analyzed in the spinal cord of the anaesthetized cat. To this end we examined the correlation between the intraspinal threshold changes of single afferent fibres in the sural nerve produced by segmental and descending inputs and the negative DC potential shifts produced by these same stimuli at the site of excitability testing, the latter taken as indicators of the changes in extracellular concentration of potassium ions. Stimulation of the ipsilateral brain-stem reticular formation and of the contralateral red nucleus with 100–200 Hz trains reduced very effectively the intraspinal threshold of sural nerve fibres ending in the dorsal horn practically without producing any negative DC potential shifts at the site of excitability testing. However, negative DC potential shifts were produced more ventrally, in the intermediate nucleus and/or motor nucleus. Stimulation of the sural and superficial peroneus nerves with pulses at 2 Hz and strengths below 2×T, also reduced the intraspinal threshold of single SU fibres without producing significant DC potential changes at the site of excitability testing. On the other hand, 100 Hz trains with strengths above 2×T produced negative DC potential shifts and a proportional reduction of the intraspinal threshold of the SU fibres. The PAD of sural fibres produced by stimulation of rubro-spinal and reticulospinal fibres as well as by stimulation of sensory nerves with low frequency trains was unaffected or slightly increased, by i.v. injection of strychnine (0.2 mg/kg), but was readily abolished 5–10 min after the i.v. injection of picrotoxin (2 mg/kg). The results suggest that activation of reticulo-spinal and rubrospinal fibres, as well as stimulation of cutaneous nerves with low frequencies and low strengths, produce PAD of cutaneous fibres involving activation of specific interneuronal pathways with interposed last-order GABAergic interneurons. The potassium component of the PAD produced by cutaneous fibres becames dominant with high stimulus frequencies and strengths.
Similar content being viewed by others
References
Benoist JM, Besson JM, Boissier JR (1974) Modifications of presynaptic inhibition of various origins by local application of convulsant drugs on cat's spinal cord. Brain Res 71: 172–177
Benoist JM, Besson JM, Conseiller C, Le Bars D (1972) Action of bicuculline on presynaptic inhibition of various origins in the cat's spinal cord. Brain Res 43: 672–676
Besson JM, Rivot JP, Aleonard P (1971) Action of picrotoxin on presynaptic inhibition of various origins in the cat's spinal cord. Brain Res 26: 212–216
Brink E, Jankowska E, Skoog B (1984) Convergence onto interneurons subserving primary afferent depolarization of group I afferents. J Neurophysiol 51: 432–449
Brown AG, Rose PK, Snow PJ (1976) The morphology of identified cutaneous afferent fibre collaterals in the spinal cord. J Physiol 263: 132–134p
Bruggencate ten G, Lux HD, Liebl L (1974) Possible relationship between extracellular potassium activity and presynaptic inhibition in the spinal cord of the cat. Pflügers Arch Ges Physiol 349: 301–307
Burke RE, Rudomin P (1977) Spinal Neurons and Synapses. In: Kandel ER (ed) Handbook of physiology, Sect I. The nervous system. Am Physiol Soc, Bethesda MD, pp 877–944
Carpenter D, Engberg I, Lundberg A (1963) Primary afferent depolarization evoked from the brain stem and the cerebellum. Arch Ital Biol 104: 73–83
Carstens E, Klumpp D, Randic M, Zimmermann M (1981) Effect of iontophoretically applied 5-hydroxytryptamine on the excitability of single primary afferent C- and A-fibers in the cat spinal cord. Brain Res 220: 151–158
Coombs JS, Eccles JC, Landgren S (1956) Spinal cord potentials generated by impulses in muscle and cutaneous afferent fibers. J Neurophysiol 19: 452–467
Curtis DR, Lodge DR (1982) The depolarization of feline ventral horn group Ia spinal afferent terminations by GABA. Brain Res 46: 215–233
Czeh G, Kriz N, Sykova E (1981) Extracellular potassium accumulation in the frog spinal cord induced by stimulation of the skin and ventrolateral columns. J Physiol (Lond) 320: 57–72
Desarmenien M, Santangelo F, Loeffer JP, Feltz P (1984) Comparative study of GABA-mediated depolarizations of lumbar A and C primary afferent neurones of the rat. Exp Brain Res 54: 521–528
Eccles JC, Kostyuk PG, Schmidt RF (1962a) Central pathways responsible for depolarization of primary afferent fibres. J Physiol (Lond) 161: 237–257
Eccles JC, Magni F, Willis WD (1962b) Depolarization of central terminals of group I afferent fibres from muscle. J Physiol (Lond) 160: 62–93
Eccles JC, Schmidt RF, Willis WD (1963a) Pharmacological studies on presynaptic inhibition. J Physiol (Lond) 168: 500–530
Eccles JC, Schmidt RF, Willis WD (1963b) The location and the mode of action of the presynaptic inhibitory pathways on group I afferent fibers from muscle. J Neurophysiol 26: 506–522
Eccles JC, Schmidt RF, Willis WD (1963c) Depolarization of the central terminals of cutaneous afferent fibers. J Neurophysiol 26: 646–661
Gmelin GW, Zimmermann M (1984) Effects of γ-aminobutyrate and bicuculline on primary afferent depolarization of cutaneous fibres in the cat spinal cord. Neuroscience 10: 869–874
Hajek I, Sykova E (1981) Potassium-induced decrease of enkephalin binding in the frog spinal cord. Physiol Bohemoslov 30: 428–429
Kongo T, Jankowska E, Lundberg A (1972) The rubrospinal tract III. Effects on primary afferent terminals. Exp Brain Res 15: 39–53
Janig W, Schmidt RF, Zimmermann M (1968a) Single unit responses and the total afferent outflow from the cat's foot pad upon mechanical stimulation. Exp Brain Res 6: 100–115
Janig W, Schmidt RF, Zimmermann M (1968b) Two specific feedback pathways to the central afferent terminals of phasic and tonic mechanoreceptors. Exp Brain Res 6: 116–129
Jankowska E, McCrea D, Rudomin P, Sykova E (1981) Observation on neuronal pathways subserving primary afferent depolarization. J Neurophysiol 46: 506–516
Jessel TM, Iversen LL (1977) Opiate analgesics inhibit substance P release from rat trigeminal nucleus. Nature 268: 549–551
Jiménez I, Rudomin P (1980) Effects of sensory inputs, intraspinal microstimulation and iontophoretic application of GABA and glutamate on the intraspinal excitability of the terminal arborizations of low threshold cutaneous afferents in the cat spinal cord. Proc Mex Soc Physiol Sci 23: 95
Jiménez I, Rudomin M, Solodkin L, Vyklicky L (1984) Specific and nonspecific mechanisms involved in generation of PAD of group Ia afferents in cat spinal cord. J Neurophysiol 52: 921–940
Jiménez I, Solodkin M, Rudomin P (1985) Specific and unspecific mechanisms involved in the generation of PAD of cutaneous fibers. Soc Neurosci 11: 401
Krnjević K, Morris ME (1974) Extracellular accumulation of K+ evoked by activity of primary afferent fibers in the cuneate nucleus and dorsal horn of cats. Can J Physiol Pharmacol 52: 852–871
Krnjević K, Morris ME (1975) Correlation between focal potentials and K+ potentials evoked by primary afferent activity. Can J Physiol Pharmacol 53: 912–922
Lundberg A, Vyklicky L (1966) Inhibition of transmission to primary afferents by electrical stimulation of the brain stem. Arch Ital Biol 104: 86–97
Madrid J, Alvarado J, Dutton H, Rudomin P (1979) A method for the dynamic continuous estimation of excitability changes of single fiber terminals in the central nervous system. Neurosci Lett 11: 253–258
Martin RF, Haber LH, Willis WD (1979) Primary afferent depolarization of identified cutaneous fibers following stimulation in medial brain stem. J Neurophysiol 42: 779–790
Nicoll RA (1979) Dorsal root potentials and changes in extracellular potassium in the spinal cord of the frog. J Physiol (Lond) 290: 113–127
Proudfit HK, Larson AA, Anderson EG (1980) The role of GABA and serotonin in the mediation of raphe-evoked spinal cord dorsal root potentials. Brain Res 195: 149–165
Rudomin P, Engberg I, Jiménez I (1981) Mechanisms involved in presynaptic depolarization of group I and rubrospinal fibers in cat spinal cord. J Neurophysiol 46: 532–548
Rudomin P, Jankowska E (1981) Presynaptic depolarization of terminals of rubrospinal tract fibers in intermediate nucleus of cat spinal cord. J Neurophysiol 46: 517–531
Rudomin P, Jiménez I, Solodkin M, Duenas S (1983) Sites of action of segmental and descending control of transmission on pathways mediating PAD of Ia- and Ib-afferent fibers in cat spinal cord. J Neurophysiol 50: 743–769
Rudomin P, Nuñez R, Madrid J, Burke RE (1974) Primary afferent hyperpolarization and presynaptic facilitation of Ia afferent terminals induced by large cutaneous afferents. J Neurophysiol 37: 413–429
Rudomin P, Solodkin M, Jiménez I (1986) PAD and PAH response patterns of group Ia- and Ib-fibers to cutaneous and descending inputs in the cat spinal cord. J Neurophysiol 56: 987–1006
Sastry BP (1978) Morphine and met-enkephalin effects on sural A afferent terminal excitability. Eur J Pharmacol 50: 269–273
Schmidt RF (1971) Presynaptic inhibition in the vertebrate central nervous system. Ergebn Physiol 63: 20–101
Solodkin M, Jiménez I, Rudomin P (1984) Identification of common interneurons mediating pre- and post-synaptic inhibition in the cat spinal cord. Science 224: 1453–1456
Somjen GG (1979) Extracellular potassium in the mammalian central nervous system. Am Rev Physiol 41: 159–177
Somjen GG (1983) Spinal fluids and ions. In: Davidoff RA (ed) Handbook of the spinal cord: pharmacology. Dekker, New York, pp 329–380
Somjen GG, Lothman EW (1974) Potassium, sustained focal potentials shifts and dorsal root potentials of the mammalian spinal cord. Brain Res 69: 153–157
Sykova E, Vyklicky L (1977) Changes of extracellular potassium activity in isolated spinal cord of frog under high Mg++ concentration. Neurosci Lett 4: 161–165
Vyklicky L (1981) Developing concept of the gating mechanism in pain perception. Acta Neurobiol Exp 41: 583–591
Vyklicky L, Sykova E, Kriz N (1975) Slow potentials induced by changes of extracellular potassium in the spinal cord of the cat. Brain Res 87: 77–80
Vyklicky L, Sykova E, Kriz N, Ujec E (1972) Post-stimulation changes of extracellular potassium concentration in the spinal cord of the rat. Brain Res 45: 608–611
Wall PD (1958) Excitability changes in afferent fibre terminations and their relation to slow potentials. J Physiol (Lond) 142: 1–21
Woolf GJ, Mitchell D, Barrett GD (1980) Antinoceptive effect of peripheral segmental electrical stimulation in the rat. Pain 8: 237–252
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Jiménez, I., Rudomin, P. & Solodkin, M. Mechanisms involved in the depolarization of cutaneous afferents produced by segmental and descending inputs in the cat spinal cord. Exp Brain Res 69, 195–207 (1987). https://doi.org/10.1007/BF00247042
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00247042