Introductory Perspective

  • Kenneth P. Scholz


Two purposes guided the writing of this introductory chapter. My first objective was to provide a concise history and background to the topic covered in this book. In doing so, I have drawn from specific examples of presynaptic inhibition that are not addressed in later chapters. This is an attempt to bind together work performed on a variety of preparations to provide an expanded view of our understanding of the mechanisms of presynaptic inhibition and how this understanding was obtained. It is anticipated that a discussion of these issues will expose important links between mechanisms of presynaptic inhibition in different preparations. A more thorough historical background can be obtained from Eccles (1964) and Nicoli and Alger (1979). My second objective was to present areas of research that I believe will be important in the near future or that perhaps deserve more attention than they have received.


Calcium Current Transmitter Release Presynaptic Terminal Luteinizing Hormone Release Hormone Presynaptic Inhibition 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Anwyl R (1991): Modulation of vertebrate neuronal calcium channels by transmitters. Brain Res Rev 16:265–281PubMedCrossRefGoogle Scholar
  2. Barron DH, Matthews BHC (1938): The interpretation of potential changes in the spinal cord. J Physiol (Lond) 92:276–321PubMedGoogle Scholar
  3. Baskys A, Malenka RC (1991): Agonists at metabotropic glutamate receptors presynaptically inhibit EPSCs in neonatal rat hippocampus. J Physiol (Lond) 444:687–701PubMedGoogle Scholar
  4. Baxter DA, Bittner GD (1991): Synaptic plasticity at crayfish neuromuscular junctions: presynaptic inhibition. Synapse 7:244–251PubMedCrossRefGoogle Scholar
  5. Bean BP (1989): Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence. Nature 340:153–156PubMedCrossRefGoogle Scholar
  6. Bowery N (1989): GABAB receptors and their significance in mammalian pharmacology. Trends Pharm Sci 10:401–407PubMedCrossRefGoogle Scholar
  7. Brock LG, Coombs JS, Eccles JC (1952): The recording of potentials from motoneurones with an intracellular electrode. J Physiol (Lond) 117:431–460PubMedGoogle Scholar
  8. Brown AM, Birnbaumer L (1990): Ionic channels and their regulation by G protein subunits. Annu Rev Physiol 52:197–213PubMedCrossRefGoogle Scholar
  9. Byrne JH (1980): Identification of neurons contributing to presynaptic inhibition in Aplysia californica. Brain Res 199:235–239PubMedCrossRefGoogle Scholar
  10. Charlton MP, Smith SJ, Zucker RS (1982): Role of presynaptic calcium ions and channels in synaptic facilitation and depression at the squid giant synapse. J Physiol (Lond) 323:173–193PubMedGoogle Scholar
  11. Clements JD, Forsythe ID, Redman SJ (1987): Presynaptic inhibition of synaptic potentials evoked in cat spinal motoneurones by impulses in single group la axons. J Physiol (Lond) 383:153–169PubMedGoogle Scholar
  12. Cooper S, Creed RS (1927): More reflex effects of active muscular contraction. J Physiol (Lond) 64:199–214PubMedGoogle Scholar
  13. Dale N, Kandel ER (1990): Facilitatory and inhibitory transmitters modulate spontaneous transmitter release at cultured Aplysia sensorimotor synapses. J Physiol (Lond) 421:203–222PubMedGoogle Scholar
  14. De Camilli P, Jahn R (1990): Pathways to regulated exocytosis in neurons. Annu Rev Physiol 52:625–645PubMedCrossRefGoogle Scholar
  15. Delaney KR, Tank DW, Zucker RS (1991): Presynaptic calcium and serotonin-mediated enhancement of transmitter release at crayfish neuromuscular junction. J Neurosci 11:2631–2643PubMedGoogle Scholar
  16. Dudel J, Kuffler SW (1961): Presynaptic inhibition at the crayfish neuromuscular junction. J Physiol (Lond) 155:543–562PubMedGoogle Scholar
  17. Dunlap K, Fischbach GD (1978): Neurotransmitters decrease the calcium component of sensory neurone action potentials. Nature 276:837–839PubMedCrossRefGoogle Scholar
  18. Eccles JC (1961): The nature of central inhibition. Proc Roy Soc B 153:445–476CrossRefGoogle Scholar
  19. Eccles JC (1964): The Physiology of Synapses. New York: Springer-Verlag, Inc.CrossRefGoogle Scholar
  20. Eccles JC, Kostyuk PG, Schmidt RF (1962): Central pathways responsible for depolarization of primary afferent fibres. J Physiol (Lond) 161:237–257PubMedGoogle Scholar
  21. Eccles JC, Schmidt R, Willis WD (1963): Pharmacological studies on presynaptic inhibition. J Physiol (Lond) 168:500–530PubMedGoogle Scholar
  22. Elmslie KS, Zhou W, Jone SW (1990): LHRH and GTP-gamma-S modify calcium current activation in bullfrog sympathetic neurons. Neuron 5:75–80PubMedCrossRefGoogle Scholar
  23. Forscher P, Oxford GS (1985): Modulation of calcium channels by norepinephrine in internally dialyzed avian sensory neurons. J Gen Physiol 85:743–763PubMedCrossRefGoogle Scholar
  24. Fox S, Krnjevic K, Morris ME, Puil E, Wierman R (1978): Action of baclofen on mammalian synaptic transmission. Neuroscience 3:495–515PubMedCrossRefGoogle Scholar
  25. Frank K (1959): Basic mechanisms of synaptic transmission in the central nervous system. IRE Trans Med Electron ME-6:85–88CrossRefGoogle Scholar
  26. Frank K, Fuortes MGF (1957): Presynaptic and postsynaptic inhibition of monosynaptic reflexes. Fed Proc 16:39–40Google Scholar
  27. Gage PW (1992): Activation and modulation of neuronal K+ channels by GABA. Trends in Neurosci 15:46–51CrossRefGoogle Scholar
  28. Gasser HS, Graham HT (1933): Potentials produced in the spinal cord by stimulation of dorsal roots. Am J Physiol 103:303–320Google Scholar
  29. Gerber U, Greene RW, Haas HL, Stevens DR (1989): Characterization of inhibition mediated by adenosine in the hippocampus of the rat in vitro. J Physiol (Lond) 417:567–578PubMedGoogle Scholar
  30. Gingrich KJ, Baxter DA, Byrne JH (1988): Mathematical model of cellular mechanisms contributing to presynaptic facilitation. Brain Res Bull 21:513–520PubMedCrossRefGoogle Scholar
  31. Grassi F, Lux HD (1989): Voltage-dependent GABA-induced modulation of calcium currents in sensory neurons. Neurosci Lett 105:113–119PubMedCrossRefGoogle Scholar
  32. Hill DR, Bowery NG (1981): 3H-baclofen and 3H-GABA bind to bicuculline-insensitive GABAB sites in rat brain. Nature 290:149–152PubMedCrossRefGoogle Scholar
  33. Hughes J, Gasser HS (1934a): Some properties of the cord potentials evoked by a single afferent volley. Am J Physiol 108:295–306Google Scholar
  34. Hughes J, Gasser HS (1934b): The response of the spinal cord to two afferent volleys. Am J Physiol 108:301–321Google Scholar
  35. Kalman D, O’Lague PH, Erxleben C, Armstrong DL (1988): Calcium-dependent inactivation of the dihydropyridine-sensitive calcium channels in GH3 cells. J Gen Physiol 92:531–548PubMedCrossRefGoogle Scholar
  36. Kalsner S, Westfall TC (1990): Presynaptic receptors and the question of autoregulation of neurotransmitter release. Ann NY Acad Sci 604Google Scholar
  37. Kasai H, Aosaki T (1989): Modulation of Ca-channel current by an adenosine analog mediated by a GTP-binding protein in chick sensory neurons. Pflugers Arch 414:145–149PubMedCrossRefGoogle Scholar
  38. Kramer RH, Kaczmarek LK, Levitan ES (1991): Neuropeptide inhibition of voltage-gated calcium channels mediated by mobilization of intracellular calcium. Neuron 6:557–563PubMedCrossRefGoogle Scholar
  39. Kretz R, Shapiro E, Kandel ER (1986a): Presynaptic inhibition produced by an identified presynaptic inhibitory neuron. I. Physiological mechanisms. J Neurophysiol 55:113–130PubMedGoogle Scholar
  40. Kretz R, Shapiro E, Bailey CH, Chen M, Kandel ER (1986b): Presynaptic inhibition produced by an identified presynaptic inhibitory neuron. II. Presynaptic conductance changes caused by histamine. J Neurophysiol 55:131–146PubMedGoogle Scholar
  41. Kuno M (1964): Mechanism of facilitation and depression of the excitatory synaptic potential in spinal motoneurones. J Physiol (Lond) 175:100–112PubMedGoogle Scholar
  42. Legido A, Reichlin S, Dichter MA, Buchhalter J (1990): Expression of somatostatin and GABA immunoreactivity in cultures of rat hippocampus. Peptides 11:103–109PubMedCrossRefGoogle Scholar
  43. Lester RAJ, Jahr CE (1990): Quisqualate receptor-mediated depression of calcium currents in hippocampal neurons. Neuron 4:741–749PubMedCrossRefGoogle Scholar
  44. Liddell EGT, Sherrington CS (1925): Further observations on myotatic reflexes. Proc Roy Soc B 97:261–283Google Scholar
  45. Lipscombe D, Kongsamut S, Tsien RW (1989): α-adrenergic inhibition of sympathetic neurotransmitter release mediated by modulation of N-type calcium channel gating. Nature 340:637–642CrossRefGoogle Scholar
  46. Llinas R, Gruner JA, Sugimori M, McGuinness TL, Greengard P (1991): Regulation by synapsin I and Ca2+-calmodulin-dependent protein kinase II of transmitter release in squid giant synapse. J Physiol (Lond) 436:257–282PubMedGoogle Scholar
  47. Man-Son-Hing H, Zoran MJ, Lukowiak K, Haydon PG (1989): A neuromodulator of synaptic transmission acts on the secretory apparatus as well as on ion channels. Nature 341:237–239PubMedCrossRefGoogle Scholar
  48. Marchetti C, Carbone E, Lux HD (1986): Effects of dopamine and noradrenaline on Ca channels of cultured sensory and sympathetic neurons of chick. Pflugers Arch 406:104–111PubMedCrossRefGoogle Scholar
  49. Miller RJ (1990): Receptor-mediated regulation of calcium channels and neurotransmitter release. FASEB J 4:3291–3299PubMedGoogle Scholar
  50. Nelson PG, Marshall KC, Pun RYK, Christian CN, Sheriff WH, MacDonald RL, Neale EA (1983): Synaptic interactions between mammalian central neurons in cell culture. II. Quantal analysis of EPSPs. J Neurophysiol 49:1442–1458PubMedGoogle Scholar
  51. Nicoli RA (1988): The coupling of neurotransmitter receptors to ion channels in the brain. Science 241:545–551CrossRefGoogle Scholar
  52. Nicoli RA, Alger BE (1979): Presynaptic inhibition: transmitter and ionic mechanisms. Int Rev Neurobiol 21:217–258CrossRefGoogle Scholar
  53. Nicoli RA, Malenka RC, Kauer JA (1990): Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. Phys Rev 70:513–565Google Scholar
  54. North RA (1989): Drug receptors and the inhibition of nerve cells. Br J Pharmacol 98:13–28PubMedGoogle Scholar
  55. Peng Y-Y, Frank E (1989): Activation of GABAB receptors causes presynaptic inhibition at synapses between muscle spindle afferents and motoneurons in the spinal cord of bullfrogs. J Neurosci 9:1502–1515PubMedGoogle Scholar
  56. Peng Y-Y, Horn JP (1991): Continuous repetitive stimuli are more effective than bursts for evoking LHRH release in bullfrog sympathetic ganglia. J Neurosci 11:85–95PubMedGoogle Scholar
  57. Scholz KP, Geary LJ, Byrne JH (1988): Inositol 1,4,5-trisphosphate alters bursting pacemake activity in Aplysia neurons: voltage-clamp analysis of effects on calcium currents. J Neurophysiol 60:86–104PubMedGoogle Scholar
  58. Scholz KP, Miller RJ (1992): Inhibition of quantal transmitter release in the absence of calcium influx by a G protein-linked adenosine receptor at hippocampal synapses. Neuron 8:1139–1150PubMedCrossRefGoogle Scholar
  59. Segev I (1990): Computer study of presynaptic inhibition controlling the spread of action potentials into axonal terminals. J Neurophysiol 63:987–998PubMedGoogle Scholar
  60. Silinsky EM (1981): On the calcium receptor that mediates depolarization-secretion coupling at cholinergic motor nerve terminals. Br J Pharmacol 73:413–429PubMedGoogle Scholar
  61. Silinsky EM (1984): On the mechanism by which adenosine receptor activation inhibits the release of acetylcholine from motor nerve endings. J Physiol (Lond) 346:243–256PubMedGoogle Scholar
  62. Smith SJ, Augustine GJ (1988): Calcium ions, active zones and synaptic transmitter release. Trends in Neurosci 11:458–464CrossRefGoogle Scholar
  63. Soejima M, Noma A (1984): Mode of regulation of the ACh-sensitive K-channel by the muscarinic receptor in rabbit atrial cells. Pflugers Arch 400:424–431PubMedCrossRefGoogle Scholar
  64. Somogyi P, Hodgson AJ, Smith AD, Nunzi MG, Gorio A, Wu JY (1984): Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholesystokinin-immunoreactive material. J Neurosci 4:2590–2603PubMedGoogle Scholar
  65. Stanley E, Cox C (1991): Calcium channels in the presynaptic nerve terminal of the chick ciliary ganglion giant synapse. Ann NY Acad Sci 635:70–79PubMedCrossRefGoogle Scholar
  66. Starke K, Gothert M, Kilbinger H (1989): Modulation of neurotransmitter release by presynaptic autoreceptors. Physiol Rev 69:864–989PubMedGoogle Scholar
  67. Stjarne L, Msghina M, Stjarne E (1990): “Upstream” regulation of the release probability in sympathetic nerve varicosities. Neuroscience 36:571–587PubMedCrossRefGoogle Scholar
  68. Stuart GJ, Redman SJ (1992): The role of GABAA and GABAB receptors in presynaptic inhibition of Ia EPSPs in cat spinal motoneurones. J Physiol (Lond) 447:675–692PubMedGoogle Scholar
  69. Takeuchi A, Takeuchi N (1966): A study of the inhibitory action of gamma-aminobutyric acid on neuromuscular transmission in the crayfish. J Physiol (Lond) 183:418–432PubMedGoogle Scholar
  70. Ullrich S, Wollheim CB (1988): GTP-dependent inhibition of insulin secretion by epinephrine in permeabilized RINm5F cells. J Biol Chem 263:8615–8620PubMedGoogle Scholar
  71. VanDongen AMJ, Codina J, Olate J, Mattera R, Joho R, Birnbaumer L, Brown A (1988): Newly identified brain potassium channels gated by the guanine nucleotide binding protein Go. Science 242:1433–1437PubMedCrossRefGoogle Scholar
  72. Von Kugelgen I, Starke K (1991): Noradrenaline-ATP co-transmission in the sympathetic nervous system. Trends Pharm Sci 12:319–323CrossRefGoogle Scholar
  73. Waziri R, Kandel ER, Frazier WT (1969): Organization of inhibition in abdominal ganglion of Aplysia. II. Posttetanic potentiation, heterosynaptic depression, and increments in frequency of inhibitory postsynaptic potentials. J Neurophysiol 32:509–519PubMedGoogle Scholar
  74. Whim MD, Lloyd PE (1989): Frequency-dependent release of peptide cotransmitters from identified cholinergic motor neurons in Aplysia. Proc Natl Acad Sci USA 86:9034–9038PubMedCrossRefGoogle Scholar

Copyright information

© Birkhäuser Boston 1993

Authors and Affiliations

  • Kenneth P. Scholz

There are no affiliations available

Personalised recommendations