Summary
The distribution of GABA receptors on various categories of primary afferents was studied by means of intracellular recordings from rat dorsal root ganglion neurones. Cells were identified on the basis of their conduction velocity and classified as Aδ and C neurones. Transient applications of GABA led to a decrease of membrane resistance and a concomitant depolarization. Maximal GABA-induced responses were weaker in C than in Aδ and Aβ cells. Smaller conductance changes in C cells suggest a lower density of GABAA receptors, and the heterogeneity of the “membrane potential/response amplitude” relationship indicate that the ionic mechanisms underlying GABA-induced responses may not be uniform on all primary afferents; this is supported by the wide range of reversal potential values recorded under voltage-clamp conditions in Aδ cells.
Similar content being viewed by others
References
Allan RD, Evans RH, Johnston GAR (1980) γ-aminobutyric acid agonists: an in vitro comparison between depression of spinal synaptic activity and depolarisation of spinal root fibers in the rat. Brit J Pharmacol 70: 609–615
Barber RP, Vaughn JE, Saito K, MacLaughlin BJ, Roberts E (1978) GABA-ergic terminals are presynaptic to primary afferent terminals in the substantia gelatinosa of the rat spinal cord. Brain Res 141: 35–55
Barber RP, Vaughn JE, Roberts E (1982) The cytoarchitecture of GABA-ergic neurons in rat spinal cord. Brain Res 238: 305–328
Barker JL, Nicoll RA (1973) The pharmacology and ionic dependancy of aminoacid responses in the frog spinal cord. J Physiol (Lond) 228: 259–277
Birren JE, Wall PD (1956) Age changes in conduction velocity, refractory period, number of fibers, connective tissue space and blood vessels in sciatic nerve of rats. J Comp Neurol 104: 1–16
Bixby JL, Spitzer NC (1982) The appearance and development of chemosensitivity in Rohon-Beard neurones in the Xenopus spinal cord. J Physiol (Lond) 330: 513–536
Bowery NG, Hill DR, Hudson AL, Doble A, Middlemiss DN, Show J, Turnbull M (1980) Baclofen decreases neurotransmitter release in the mammalian CNS by an action at a novel GABA receptor. Nature 283: 92–94
Bowery NG, Doble A, Hill DR, Hudson AL, Shaw JS, Turnbull MJ, Warrington R (1981) Bicuculline-insensitive GABA receptors on peripheral autonomic nerve terminals. Eur J Pharmacol 71: 53–70
Brown DA, Higgins AJ (1979) Presynaptic effect of GABA in isolated rat superior cervical ganglia. Br J Pharmacol 66:108P
Brown DA, Marsh S (1978) Axonal GABA receptors in mammalian peripheral nerve trunks. Brain Res 156: 187–191
Brown DA, Higgins AJ, Marsh S, Smart TG (1981) Actions of GABA on mammalian neurones, axons and nerve terminals. In: Roberts E, Chase T, Towers DB (eds) GABA in nervous system functions. Raven Press, New York, pp 321–326
Calvillo O, Madrid J, Rudomin P (1982) Presynaptic depolarization of unmyelinated primary afferent fibers in the spinal cord of the cat. Neuroscience 7: 1389–1400
Choi DW, Fischbach GD (1981) GABA conductance on chick spinal cord and dorsal root ganglion neurons in cell culture. J Neurophysiol 45: 605–620
Curtis DR, Duggan AW, Felix D, Johnston GAR (1971) Bicuculline: an antagonist of GABA and synaptic inhibition in the spinal cord of the cat. Brain Res 32: 69–96
Curtis DR, Lodge D, Bornstein JC, Peet MJ, Leah JD (1982) The dual effect of GABA and related amine acids on the electrical threshold of ventral horn group IA afferent terminations in the cat. Exp Brain Res 48: 387–400
Curtis DR, Lodge D (1982) The depolarization of feline ventral horn group IA spinal afferent terminations by GABA. Exp Brain Res 46: 215–233
Desarmenien M, Feltz P, Headley PM (1980) Does glial uptake affect GABA responses? An intracellular study on rat dorsal root ganglion neurones in vitro. J Physiol (Lond) 307: 163–182
Desarmenien M, Feltz P, Headley PM, Santangelo F (1981) SL 75102 as a γ-aminobutyric acid agonist: experiments on dorsal root ganglion neurones in vitro. Brit J Pharmacol 72: 355–364
Desarmenien M, Feltz P, Loeffler J Ph, Occhipinti G, Santangelo F (1982) Multiple GABA receptors on Aδ and C primary afferent neurones in the adult rat. Br J Pharmacol 76: 289 P
Desarmenien M, Feltz P, Occhipinti G, Santangelo F, Schlichter R (1983) Coexistance of GABAA and GABAB receptors on Aδ and C primary afferents. Br J Pharmacol (in press)
Deschenes M, Feltz P (1976) GABA-induced rize of extracellular potassium in rat dorsal root ganglia: an electrophysiological study in vivo. Brain Res 118: 494–499
Dudel J, Finger W, Stettmeier H (1980) Inhibitory synaptic channels activated by γ-aminobutyric acid (GABA) in crayfish muscle. Pfluegers Arch 387: 143–151
Dunlap K (1981) Two types of γ aminobutyric acid receptors on embryonic sensory neurons. Br J Pharmacol 74: 579–585
Feltz P, Rasminsky M (1974) A model for the mode of action of GABA on primary afferent terminals: depolarizing effects of GABA applied iontophoretically to neurones of mammalian dorsal root neurons. Neuropharmacology 13: 553–563
Fitzegerald M, Woolf CI (1981) Effects of cutaneous nerve and intraspinal conditioning on C fiber afferent terminal excitability in decerebrate spinal rats. J Physiol (Lond) 318: 25–40
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
Headley PM, Desarmenien M, Santangelo F, Feltz P (1981) Direct action of pentobarbitone in potentiating the responses to GABA of rat dorsal root ganglion neurones in vitro. Neurosci Lett 24: 273–278
Hopkins AP, Lambert EH (1973) Age changes in conduction velocity of unmyelinated fibers. J Comp Neurol 147: 547–552
Jankowska E, MacCrea D, Rudomin P, Sykova E (1982) Observations of neuronal pathways subserving primary afferent depolarization. J Neurophysiol 46: 506–516
Johnston GAR, Allan RD, Kennedy SME, Twitchin B (1979) Systematic study of GABA analogues of restricted conformation. In: Krogsgaard-Larsen P, Scheel-Krager J, Kofod H (eds) GABA neurotransmitters. 12th Alfred Benzon Symposium. Murksgaard, Copenhagen, pp 149–164
Kato E, Kuba K, Koketsu K (1978) Presynaptic inhibition by γ-aminobutyric acid in bullfrog sympathetic ganglion cells. Brain Res 153: 398–402
Levy RA (1977) The role of GABA in primary afferent depolarization. Progress in Neurobiology 9: 211–267
Nagy JI, Iversen LL, Goedert M, Chapman D, Hunt SP (1983) Dose-dependent effect of capsaicin in primary sensory neurons in the neonatal rat. J Neurosci 3: 399–406
Nishi S, Minota S, Karczmar AG (1974) Primary afferent neurones: the ionic mechanism of GABA-mediated depolarization. Neuropharmacol 13: 215–219
Otsuka M, Konishi S (1976) GABA in the spinal cord. In: Roberts E, Chase T, Tower DB (eds) GABA in nervous system function Raven Press, New York, pp 197–202
Rudomin P, Jankowska E (1982) Presynaptic depolarization of terminals of rubrospinal tract fibers in intermediate nucleus of cat spinal cord. J Neurophysiol 46: 517–531
Sakmann B, Hamill OP, Bormann J (1982) Activation of chloride channels by putative inhibitory transmitters in spinal cord neurons. Pfluegers Arch Suppl 392 Abst 74
Sastry BR (1979) γ aminobutyric acid and primary afferent depolarization in feline spinal cord. Can J Physiol Pharmacol 57: 1157–1167
Singer E, Placheta P (1980) Reduction of (3H) muscimol binding sites in rat dorsal spinal cord after neonatal capsaicin treatment. Brain Res 202: 484–487
Vyklicky L, Sykova E, Mellerova B (1976) Depolarization of primary afferents in the frog spinal cord under high Mg++ concentration. Brain Res 117: 153–156
Wall PD (1982) The effect of peripheral nerve lesion and of neonatal capsaicin in the rat on primary afferent depolarization. J Physiol (Lond) 329: 21–35
Wilson WA, Goldner MM (1975) Voltage clamping with a single microelectrode. J Neurobiol 6: 411–422
Yoshida S, Matsuda M (1979) Studies on sensory neurones of the mouse with intracellular recording and horseradish peroxidase — injection techniques. J Neurophysiol 42: 1134–1145
Author information
Authors and Affiliations
Additional information
With the support of INSERM and CNRS (PRC 121009/ATP 2581)
Rights and permissions
About this article
Cite this article
Desarmenien, M., Santangelo, F., Loeffler, J.P. et al. Comparative study of GABA-mediated depolarizations of lumbar Aδ and C primary afferent neurones of the rat. Exp Brain Res 54, 521–528 (1984). https://doi.org/10.1007/BF00235477
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00235477