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Mechanisms of heterosynaptic facilitation in molluscan neurons

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Abstract

This review is focused on the analysis of research data obtained in one of the models of conditioned reflex, heterosynaptic facilitation (HSF), in the molluscan nervous system. Our experiments were performed on identified giant command neurons LS1 and PS1 of the freshwater snail Planorbarius corneus. HSF was elicited during the electrical stimulation of two nerves: pallial (the analog of unconditioned stimulation — US) and one of the cerebral nerves (the analog of the conditioned stimulation — CS). The degree of HSF manifestation depended not on the intensity of the synaptic response of the giant neuron to US, but the efficacy of the connection between the pallial nerve and neurosecretory neurons surrounding the command neuron of the mesocerebrum. It is demonstrated that HSF develops due to the diffuse neurohumoral action of serotonin (5-hydroxytryptamine — 5-HT) on the postsynaptic structures, but not as a result of local synaptic action on the presynaptic mechanism. Approximately 70% of US cases of 5-HT application induced a four- to six-fold increase in amplitude of the excitatory postsynaptic potential (EPSP) and acetylcholine (ACh) response. Both responses are N-cholinergic and depend on the membrane permeability to Na+ and K+. In 30% of the cases, ACh response diminished simultaneously with EPSP increase. The 5-HT effect on EPSP and ACh responses were mimicked by the action of phosphodiersterase blockers and adenylate cyclase activators. Thus, the activation of the adenylate cyclase system following 5-HT action facilitates the postsynaptic mechanism underlying HSF formation in command neurons of Planorbarius corneus. Dopamine (DA) and noradrenaline (NA) blocked EPSP and simultaneously increased the amplitude of ACh response. These monoamines were also blocked HSF. The wash-out of catecholamines following HSF blockade enhanced the restoration and subsequent prolongation of synaptic facilitation. It is thus concluded that DA or NA may control the HSF intensity and duration under natural conditions of the nervous system in the molluscs.

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References

  1. E. R. Kandel and L. Tauc, “Heterosynaptic facilitation in neurons of the abdominal ganglion ofAplysia depilans,”J. Physiol.,181, No. 1, 1–27 (1965).

    Google Scholar 

  2. E. R. Kandel and L. Tauc, “Mechanism of heterosynaptic facilitation in the giant cell ofAplysia depilans,”J. Physiol.,181, No. 1, 28–47 (1965).

    Google Scholar 

  3. E. Kandel,Cellular Basis of Behavior [Russian translation], Mir, Moscow (1980).

    Google Scholar 

  4. G. A. Vartanyan, M. I. Lokhov, and I. I. Stepanov, “Features of investigations into the mechanism of conditioned reflex in higher invertebrates,”Usp. Fiziol. Nauk,19, No. 2, 3–26 (1988).

    Google Scholar 

  5. T. L. D'yakonova, “Why and how do we study the neuron?”Zh. Obshch. Biol.,48, No. 3, 311–324 (1987).

    Google Scholar 

  6. E. N. Sokolov, “Types of postsynaptic plasticity All-Union Congress of the I. P. Pavlov Physiological Society (Alma-Ata, 1979) [in Russian]; Summaries of Reports, Leningrad (1979), p. 214.

  7. M. B. Kennedy, “Molecules underlying memory,”Nature,329, No. 6134, 15–16 (1987).

    Google Scholar 

  8. O. N. Oispenko, “Modulatory action of oxytocin on electrical responses of the neurons in the snailHelix pomatia,” in:Simpler Nervous Systems, D. A. Sakharov and W. Winlow (eds.), Manchester Univ. Press, Manchester, New York (1991).

    Google Scholar 

  9. V. M. Storozhuk,Neuronal Mechanisms of Learning [in Russian], Naukova Dumka, Kiev (1986).

    Google Scholar 

  10. B. Bank, T. Nelsen, and D. Alkon, “Molecular mechanisms of associative learning in mammal and mollusc,”J. Physiol.,83, No. 3, 119–125 (1988).

    Google Scholar 

  11. T. J. Carew, R. D. Hawkins, and E. R. Kandel, “Differntial classical conditioning of a defensive withdrawal reflex inAplysia californica,”Science,219, No. 4583, 397–400 (1983).

    Google Scholar 

  12. T. J. Carew, E. T. Walters, and E. R. Randel, “Classical conditioning in a simple withdrawal reflex inAplysia californica,”J. Neurosci.,1, No. 11, 1426–1437 (1981).

    Google Scholar 

  13. B. G. Schreurs, “Classical conditioning of systems: A behavioral review,”Psychobiology,17, No. 2, 145–155 (1989).

    Google Scholar 

  14. A. C. Pivovarov, E. I. Drosdova, and B. I. Kotlyar, “Secondary messengers in the regulation of neuronal plasticity during learning,”Biol. Nauki, No. 3, 75–101 (1989).

    Google Scholar 

  15. E. S. Severin and M. N. Kochetkova,Role of Phosphorylation in the Regulation of Cellular Activity [in Russian], Nauka, Moscow (1985).

    Google Scholar 

  16. D. A. Baxter and J. H. Byrne, “Serotonergic modulation of two potassium currents in the pleural sensory neurons ofaplysia,”J. Neurophysiol.,62, No. 3, 665–672 (1989).

    Google Scholar 

  17. O. Braha, N. Dale, B. Hochner, et al., “Second messengers involved in the two processes of presynaptic facilitation that lead to sensitization and dishabituation inAplysia sensory neurons,”Proc. Natl. Acad. Sci. USA,87, No. 5, 2040–2044 (1990).

    Google Scholar 

  18. J. Farley and R. Wu, “Serotonin modulation of Hermissenda type B photoreceptor light responses and ionic currents: Implications for mechanisms underlying associative learning,”Brain Res. Bull.,22, No. 2, 335–351 (1989).

    Google Scholar 

  19. R. Gillette, M. U. Gillette, D. J. Green, and R. Huang, “The neuromodulatory response: Integrating second messenger pathways,”Am. Zool.,29, No. 4, 1275–1286 (1989).

    Google Scholar 

  20. L. L. Voronin, “Neurophysiological mechanisms underlying after-discharge phenomena,”Usp. Fiziol. Nauk,1, No. 1, 111–136 (1970).

    Google Scholar 

  21. V. I. Gusel'nikov and A. S. Pivovarov, “Neuronal plasticity in learning,”Zh. Biol. Nauk,196, No. 4, 66–81 (1980).

    Google Scholar 

  22. T. L. D'yakonova and T. M. Turpayev, “Plasticity of the electrically excitable membrane of a neuron: Possible role of Ca2+,”Dokl. Akad. Nauk SSSR,271, No. 5, 1261–1265 (1983).

    Google Scholar 

  23. B. I. Kotlyar,Neurological Basis of Learning [in Russian], Nauka, Moscow (1989).

    Google Scholar 

  24. E. I. Sokolov,Neuronal Mechanisms of Memory and Learning [in Russian], Nauka, Moscow (1981).

    Google Scholar 

  25. J. F. Brons and C. D. Woody, “Long-term changes in excitability of cortical neurons after pavlovian conditioning and extinction,”J. Neurophysiol.,44, No. 3, 605–615 (1980).

    Google Scholar 

  26. Yu. Konorski,Integrative Brain Activity [Russian translation], Mir, Moscow (1970).

    Google Scholar 

  27. J. Konorski,Conditioned Reflexes and Neuron Organization, Cambridge University Press, Cambridge (1948).

    Google Scholar 

  28. D. O. Hebb,The Organization of Behavior: A Neuropsychological Theory, Wiley, New York (1949).

    Google Scholar 

  29. W. Fischer, “Dressurversuche mit schnechen,”Z. Vergl. Physiol., No. 15, 50–70 (1931).

    Google Scholar 

  30. E. L. Tompson, “An analysis of the learning process in the snailPhysa gyrina Behav. Mond.,3, No. 14, 89–97 (1917).

    Google Scholar 

  31. D. L. Elcon, “Learning in the sea snail,” in;In the World of Science [Russian translation], Mir, Moscow, Ser. 9 (1983), pp. 34–45.

    Google Scholar 

  32. O. A. Maksimova and P. M. Balaban,Neuronal Mechanisms of Behavioral Plasticity [in Russian], Nauka, Moscow (1983).

    Google Scholar 

  33. E. R. Kandel and L. Tauc, “Mechanism of prolonged heterosynaptic facilitation,”Nature,202, No. 4928, 145–147 (1964).

    Google Scholar 

  34. J. H. Byrne, “Cellular analysis of associative learning,”Physiol. Rev.,67, No. 2, 329–439 (1987).

    Google Scholar 

  35. V. F. Castellucci, W. N. Frost, Ph. Goelet, et al., “Cell and molecular analysis of long-term sensitization inAplysia,”J. Physiol.,81, No. 4, 349–357 (1986).

    Google Scholar 

  36. E. R. Kandel, S. Schacher, V. F. Castellucci, and Ph. Goelet, “The long and short of memory inAplysia: A molecular perspective,” in:Fidia Research Foundation (Neuroscience Award Lectures), Leviana Press, Padova (1986), pp. 7–47.

    Google Scholar 

  37. R. M. Coluill, R. A. Absher, and M. L. Roberts, “Context — US bearning inAplysia californica,”J. Physiol.,8, No. 12, 4434–4439 (1988).

    Google Scholar 

  38. A. J. Hunter, “Serotonergic involvement in learning and memoryBiochem. Soc. Trans.,17, No. 1, 79–81 (1989).

    Google Scholar 

  39. Ya. Pustai, T. A. Safonova, and T. Adam, “Changes in postsynaptic potential in the identified neuron ofHelix pomatia during the process of formation of temporal connection,”Dokl. Akad. Nauk SSSR,230, No. 5, 1246–1249 (1976).

    Google Scholar 

  40. S. G. Rane and K. Dunlap, “Kinase C activator 1,2-oleoylacetylglycerol attenuates voltage-dependent calcium current in sensory neurons,”Comp. Biochem. Physiol.,83, No. 1, 184–188 (1966).

    Google Scholar 

  41. R. J. Baumgarten and B. Jahar-Parvar, “Time-course of repetitive heterosynaptic facilitation inAplysia californica,”Brain Res.,4, No. 1, 295–297 (1967).

    Google Scholar 

  42. V. M. Storozhuk and I. N. Antonov, “Features of heterosynaptic facilitation in giant neurons of the cerebral ganglion of the snailHelix pomatia,”Neirofiziologiya,12, No. 5, 498–507 (1980).

    Google Scholar 

  43. E. T. Walters, “Transformation of siphon responses during conditioning ofAplysia suggests a model of primitive stimulus-response association,”Proc. Natl. Acad. Sci. USA,86, No. 19, 7616–1619 (1989).

    Google Scholar 

  44. B. S. Osipov,Functional Plasticity of Molluscan Neurons [in Russian], Leningrad State University, Leningrad (1980).

    Google Scholar 

  45. D. Zecevic, J. Wu, L. B. Cohen, et al., “Hundreds of neurons inAplysia abdominal ganglion are active during the gill-withdrawal reflex,”J. Neurosci.,3, No. 10, 3681–3689 (1989).

    Google Scholar 

  46. E. R. Kandel and J. H. Schwartz, “Molecular biology of learning: Modulation of transmitter release,”Science,218, No. 4571, 433–443 (1982).

    Google Scholar 

  47. S. L. Mackey, E. R. Kandel, and R. D. Hawkins, “Identified serotonergic neurons LCB1 and RCB1 in the cerebral ganglia ofAplysia produce presynaptic facilitation of siphon sensory neurons,”J. Neurosci.,2, No. 12, 4227–4235 (1989).

    Google Scholar 

  48. R. D. Hawkins, N. Lalevic, and G. A. Clark, “Classical conditioning of theAplysia siphon-withdrawal reflex exhibits response specificity,”Proc. Natl. Acad. Sci. USA,86, No. 19, 7620–7624 (1989).

    Google Scholar 

  49. P. E. Lloyd, “Peripheral actions of the SCPs inAplysia and other gastropod molluscs,”Am. Zool.,29, No. 4, 1265–1274 (1989).

    Google Scholar 

  50. R. D. Hawkins, V. E. Castellucci, and E. R. Kandel, “Interneurons involved on mediation of gill-withdrawal reflex inAplysia,”J. Neurophysiol.,45, No. 2, 304–314 (1981).

    Google Scholar 

  51. M. Brunelli, V. Castellucci, and E. R. Kandel, “Synaptic facilitation and behavioral sensitization inAplysia: Possible role of serotonin and cyclic AMP,”Science,194, No. 4270, 1178–1181 (1976).

    Google Scholar 

  52. T. Shimahara and L. Tauc, “Cyclic AMP-induced by serotonin modulates the activity of an identified synapse inAplysia by facilitating the active permeability to calcium,”Brain Res.,127, No. 1, 168–177 (1977).

    Google Scholar 

  53. T. Shimara and L. Tauc, “The role of cyclic AMP in the modulation of synaptic efficacy,”J. Physiol.,74, No. 5, 515–519 (1978).

    Google Scholar 

  54. C. Bailey and M. Cyen, “Morphological basis of long-term habituation and sensitization inAplysia,”Science,220, No. 4592, 91–93 (1983).

    Google Scholar 

  55. F. Belardetti, C. B. Biondi, L. Colombaioni, et al., “Role of serotonin and cyclic AMP on facilitation of the fast conducting system activity in the leechHirudo medicinalis,”Brain Res.,246, No. 1, 89–103 (1982).

    Google Scholar 

  56. F. Belardetti, C. Biondi, M. Brunelli, et al., “Heterosynaptic facilitation and behavioral sensitization are inhibited by lowering endogenous cAMP inAplysia,”Brain Res.,288, No. 1/2, 95–104 (1983).

    Google Scholar 

  57. L. Bernier, V. F. Castellucci, E. R. Kandel, and J. H. Schwartz, “Facilitatory transmitter causes a selective and prolonged increase in adenosine 3′:5′-monophosphate in sensory neurons mediating the gill and siphon withdrawal reflex inAplysia,”J. Neurosci.,2, No. 12, 1682–1691 (1982).

    Google Scholar 

  58. V. F. Castellucci, A. Nairn, P. Greengard, et al., “Inhibitor of adenosine 3′:5′-monophosphate-dependent protein kinase blocks presynaptic facilitation inAplysia J. Neurosci.,2, No. 12, 1673–1681 (1982).

    Google Scholar 

  59. R. D. Hawkins and S. Schacher, “Identified facilitator neurons L29 and L28 are excited by cutaneous stimuli used in dishabituation, sensitization, and classical conditioning ofAplysia,”J. Neurosci.,9, No. 12, 4236–4245 (1989).

    Google Scholar 

  60. T. W. Abrams and E. R. Kandel, “Is contiguity detection in classical conditioning a system or a cellular property learning inAplysia suggests a possible molecular site,”Trends Neurosci.,11, No. 4, 128–136 (1988).

    Google Scholar 

  61. T. W. Abrams, V. F. Castellucci, J. S. Camardo, et al., “Two endogenous neuropeptides modulate the gian and siphon withdrawal reflex inAplysia by presynaptic facilitation involving cAMP-dependent closure of serotonin-sensitive potassium channel,”Proc. Natl. Acad. Sci. USA, Ser. Biol. Sci.,81, No. 24, 7956–7960 (1984).

    Google Scholar 

  62. S. A. Siegelbaum, J. S. Camardo, and E. R. Kandel, “Serotonin and cyclic AMP close single K+ channels inAplysia sensory neurons,”Nature,299, No. 5882, 413–417 (1982).

    Google Scholar 

  63. V. F. Castellucci, E. R. Kandel, and J. H. Schwartz, “Intracellular injection of the catalytic subunit of cyclic AMF-dependent protein kinase simulates facilitation of transmitter release underlying behavioral sensitization inAplysia,”Proc. Natl. Acad. Sci. USA,77, No. 12, 7492–7497 (1980).

    Google Scholar 

  64. M. Klein, B. Hochner, and E. R. Kandel, “Facilitatory transmitters and cyclic AMP can modulate accommodation as well as transmitter release inaplysia sensory neurons: Evidence for parallel processing in a single cell,”Proc. Natl. Acad. Sci. USA,83, No. 20, 7994–7998 (1986).

    Google Scholar 

  65. M. Klein, E. Shapiro, and E. R. Kandel, “Synaptic plasticity and the modulation of the Ca++ current,”J. Exp. Biol.,89, No. 2, 117–157 (1980).

    Google Scholar 

  66. F. Belardetti, S. Schacher, E. R. Kandel, and S. A. Siegelbaum, “The growth cones ofAplysia sensory neurons: Modulation by means of action potential duration and single potassium currents,”Proc. Natl. Acad. Sci. USA,83, No. 18, 7094–7098 (1986).

    Google Scholar 

  67. T. C. Sackor and J. H. Schwartz, “Sensitizing stimuli cause translocation of kinase C inaplysia sensory neurons,”Proc. Natl. Acad. Sci. USA,87, No. 5, 2036–2039 (1990).

    Google Scholar 

  68. M. Klein, J. Camardo, and E. R. Kandel, “Serotonin modulates a specific potassium current in the sensory neurons that show presynaptic facilitation,”Proc. Natl. Acad. Sci. USA,79, No. 10, 5713–5717 (1982).

    Google Scholar 

  69. L. K. Koczmarek and F. A. Strumwasser, “A voltage-clamp analysis of currents underlying cAMP-induced membrane modulation in isolated peptidergic neurons ofAplysia,”J. Neurophysiol.,52, No. 2, 340–349 (1984).

    Google Scholar 

  70. J. P. Walsch and J. H. Byrne, “Forskolin mimics and blocks a serotonin-sensitive decreased K+ conductance in tail sensory neurons ofAplysia,”Neurosci. Lett.,52, No. 1/2, 77–111 (1984).

    Google Scholar 

  71. E. R. Kandel, “Calcium and the control of synaptic strength by learning,”Nature,293, No. 5835, 697–700 (1981).

    Google Scholar 

  72. D. A. Brown, “G-proteins and potassium currents in neurons,”Annu. Rev. Physiol.,52, 215–242 (1990).

    Google Scholar 

  73. A. C. Dolphin, “G-protein modulation of calcium currents in neurons,”Annu. Rev. Physiol.,52, 243–255 (1990).

    Google Scholar 

  74. M. Klien and E. R. Kandel, “Presynaptic modulation of voltage-dependent Ca++ current: Mechanism for behavioral sensitization inAplysia californica,”Nature,75, No. 7, 3512–3516 (1978).

    Google Scholar 

  75. M. Brunelli and G. Demontis, “Modulation of intercellular communication on the C.N.S.,”Boll. Soc. Ital. Biol. Sper.,60, No. 4, Suppl., 65–69 (1984).

    Google Scholar 

  76. M. Klein and E. R. Kandel, “Mechanism of calcium current modulation underlying synaptic facilitation and behavioral sensitization inAplysia,”Nature,77, No. 11, 6912–6918 (1980).

    Google Scholar 

  77. S. N. Orlov, “Calmodulin,”Itogi Nauki i Tekhniki, Ser. Obssh. Problemy Fiz.-Khim. Biol.,8, 5–209 (1987).

    Google Scholar 

  78. M. Onozuka, H. Furuichi, K. Kishii, and S. Imai, “Calmodulin in the activation process of calcium-dependent potassium channel inEuhadra neurons,”Comp. Biochem. Physiol., Ser. A,86, No. 3, 589–593 (1987).

    Google Scholar 

  79. M. B. Boyle, M. Klein, S. J. Smith, and E. R. Kandel, “Serotonin increases intracellular Ca++ transient in voltage-clamped sensory neurons ofAplysia californica,”Proc. Natl. Acad. Sci. USA.,81, No. 23, 7642–7646 (1984).

    Google Scholar 

  80. E. R. Kandel, “The short and long of memory,”Pflugers Arch.,408, No. 1, Suppl., 111 (1987).

    Google Scholar 

  81. E. R. Kandel, “Molecular biological similarities and differences between long- and short-term memory 31 International Congress Physiology of Science (Helsinki, 9–14 July, 1989), Abstr., Oulu (1989), p. 345.

  82. I. P. Ashmarin,Molecular Mechanisms of Neurological Memory [in Russian], Nauka, Leningrad (1987).

    Google Scholar 

  83. Y. Schiffman, “On the molecular basis of memory,”Biochem. Soc. Trans.,17, No. 6, 1065–1068 (1989).

    Google Scholar 

  84. E. R. Kandel and L. Tauc, “Anomalous rectification in the metacerebral giant cells and its consequences for synaptic transmission,”J. Physiol.,183, No. 2, 287–304 (1966).

    Google Scholar 

  85. J. Eccles,Physiology of Synapses [Russian translation], Mir, Moscow (1966).

    Google Scholar 

  86. V. M. Storozhuk and I. N. Antonov, “Effect of monoamines on heterosynaptic facilitation in snail giant neurons,”Neirofiziologiya,21, No. 2, 224–232 (1989).

    Google Scholar 

  87. A. V. Govorukha, “Functional organization of identified neurons ofPlanorbarius corneus,” Abstr. of Cand. Thesis, Biol. Sci., Kiev (1979).

    Google Scholar 

  88. A. V. Govorukha, V. A. Troshikhin, O. F. Dembnovetsky, and G. A. Taran, “On the synaptic organization of spontaneously active neurons of cerebral ganglia in the molluscanPlanorbarius corneus,”Zh. Évol. Biokhim. Fiziol.,10, No. 1, 29–35 (1974).

    Google Scholar 

  89. V. M. Storozhuk and I. N. Antonov, “Role of humoral factor and postsynaptic sensitization in heterosynaptic facilitation,”Neirofiziologiya,18, No. 2, 250–259 (1986).

    Google Scholar 

  90. I. N. Antonov, “analysis of postsynaptic mechanism of heterosynaptic facilitation in neurons of molluscan cerebral ganglia,” Abstr. of Cand. Thesis, Biol. Sci., Kiev (1992).

    Google Scholar 

  91. T. Shimahara and L. Tauc, “Heterosynaptic facilitation in the giant cell ofAplysia,”J. Physiol.,247, No. 2, 321–341 (1975).

    Google Scholar 

  92. I. N. Antonov, “Dependence of modulatory effect of serotonin (5-HT) on ionic condition of the cholinoceptive membrane,” in:Brain Serotonin, Neuro-Psychic Impairments and Their Pharmacological Correction [in Russian], Summaries of Reports, Donetsk (1990), p. 5.

  93. I. N. Antonov, “Role of secondary messengers in regulation of cholinoceptive membrane conduction,” in:Physiology and Biochemistry of Neurotransmitter Processes, V All-Union Conference [in Russian], Summaries of Reports, Moscow (1990), p. 17.

  94. I. N. Antonov, V. M. Storozhuk, and O. M. Osipenko, “Analysis of heterosynaptic facilitation in identified giant neurons from cerebral ganglion of the ond snailPlanorbarius corneus,”Comp. Biochem. Physiol., Ser. C,98, No. 2/3, 323–327 (1991).

    Google Scholar 

  95. M. U. Gillette and R. Gillette, “Bursting neurons command consummatory feeding behavior and coordinated visceral receptivity in the predatory molluskPleurobranchaea,”J. Neurosci.,3, No. 9, 1791–1806 (1983).

    Google Scholar 

  96. R. A. Nicoll, R. C. Malenka, and J. A. Kauer, “Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system,”Physiol. Rev.,70, No. 2, 513–525 (1990).

    Google Scholar 

  97. L. K. Simmons and J. Koester, “Serotonin enhances the excitatory acetylcholine response in the RB cell cluster ofAplysia californica,”J. Neurosci.,6, No. 3, 774–781 (1986).

    Google Scholar 

  98. A. R. Akopyan, “Cyclic AMP as modulator of chemoceptive membrane excitability in molluscan neurons Abstr. of Cand. Thesis, Biol. Sci., Puschino (1981).

    Google Scholar 

  99. V. A. Dyatlov, “Ionic mechansims of modulatory effect of serotonin on acetylcholine responses inHelix pomatia neurons,”Neirofiziologiya,20, No. 1, 57–64 (1988).

    Google Scholar 

  100. V. A. Dyatlov, “Role of Ca2+ ions in processes of modulation of serotonin responses ofHelix pomatia to acetylcholine application,”Neirofiziologiya,20, No. 5, 666–671 (1988).

    Google Scholar 

  101. N. I. Kononenko and A. D. Scherbatko, “Effect of serotonin on inward calcium current inHelix pomatia neurons,”Dokl. Akad. Nauk SSSR,281, No. 6, 1494–1497 (1985).

    Google Scholar 

  102. T. M. Turpayev, O. P. Yurchenko, and K. Sh. Rozha, “Two types of interaction between serotonin and acetylcholine on identified brain neurons ofHelix pomatia,”Dokl. Akad. Nauk SSSR,270, No. 6, 1505–1508 (1983).

    Google Scholar 

  103. F. Khukho,Neurochemistry. Fundamentals and Principles [Russian translation], Mir, Moscow (1990).

    Google Scholar 

  104. J. Kehoe, “Ionic mechanisms of a two-component cholinergic inhibitions inAplysia neurons,”J. Physiol.,225, No. 1, 85–114 (1972).

    Google Scholar 

  105. J. Kehoe, “Three acetylcholine receptors inAplysia neurons,”J. Physiol.,225, No. 1, 115–146 (1972).

    Google Scholar 

  106. V. A. Dyatlov and A. V. Platoshin, “Effect of Ca2+ ions on acetylcholine-induced current in molluscan neurons,”Neirofiziologiya,22, No. 4, 553–556 (1990).

    Google Scholar 

  107. N. I. Kononenko and P. G. Kosltyuk, “Effect of intracellular cAMP injection on calcium current in identifiedHelix pomatia neurons,”Neirofiziologiya,14, No. 3, 290–297 (1982).

    Google Scholar 

  108. P. G. Kostyuk,Calcium and Cell Excitability, Nauka, Moscow (1986).

    Google Scholar 

  109. N. K. Chemeris, “Interaction and intracellular regulation of the work of electro- and chemosensitive structures of neuronal membrane,” Abstr. of Cand. Thesis, Biol. Sci., Puschino (1988).

    Google Scholar 

  110. P. Greengard, “Possible role for cyclic nucleotides and phosphorylated membrane proteins in postsynaptic actions of neurotransmitters,”Nature,260, No. 5547, 101–108 (1976).

    Google Scholar 

  111. N. I. Kononenko, P. G. Kostyuk, and A. D. Shcherbatko, “Properties of cAMP-induced transmembrane current in mollusc neurons,”Brain Res.,376, No. 2, 239–245 (1986).

    Google Scholar 

  112. V. M. Storozhuk, I. N. Antonov, and O. A. Osipenko, “Involvement of adenylate cyclase systems in postsynaptic mechanisms of heterosynaptic facilitation,”Neirofiziologiya,23, No. 6, 676–683 (1991).

    Google Scholar 

  113. P. G. Kostyuk, A. V. Tepikin, P. V. Belan, and S. L. Mironov, “Mechanisms of alteration in Ca2+ ion concentration in the cytoplasm ofHelix pomatia involving intracellular Ca2+ storage,”Biol. Membrany,4, No. 9, 932–936 (1987).

    Google Scholar 

  114. F. Belardetti, C. Biondi, M. Brunelli, and A. Trevisani, “Role of cAMP on short-term plastic changes such as sensitization in the mediterranean species ofAplysia,”Neurosci. Lett.,13, Suppl., No. 3, 83–91 (1979).

    Google Scholar 

  115. H. M. Gerschenfeld, C. Hammond, and D. Paupardin-Tritsch, “Modulation of the calcium current of molluscan neurons by neurotransmitters,”J. Exp. Biol.,124, No. 1, 73–91 (1986).

    Google Scholar 

  116. M. Metteoli, F. Navon, C. Haimann, et al., “Secretory organelles of neurons and their relationship to organelles of other cells,”Cell Biol. Int. Repts.,13, No. 12, 981–992 (1989).

    Google Scholar 

  117. H. M. Gerschenfeld, D. Paupardin-Tritsch, C. Hammond, and R. Harris-Warrick, “Intracellular mechanism of neurotransmitter-induced modulations of voltage-dependent Ca2+ current in snail neurons,”Cell Biol. Int. Repts.,13, No. 12, 1141–1154 (1989).

    Google Scholar 

  118. A. I. Vislobokov, A. A. Kokarev, and M. I. Sologub, “Depolarization and hyperpolarization of identified pond snail neurons under catecholamine influence,”Vestn. Leningr. Gos. Universit.,3, Ser. 1, 72–79 (1981).

    Google Scholar 

  119. A. J. Bokisch and R. J. Walker, “The ionic mechanism associated with the action of putative transmitters on identified neurons of the snailHelix pomatia,”Comp. Biochem. Physiol., Ser. C,84, No. 2, 231–241 (1986).

    Google Scholar 

  120. O. P. Yurchenko, T. M. Turpayev, D. Konevich, et al., “Effect of dopamine injection on endogenous activity and acetylcholine responses in identified burst neurons ofAplysia,”Dokl. Akad. Nauk SSSR,284, No. 1, 248–252 (1985).

    Google Scholar 

  121. M. V. Chistyakova, “Effect of serotonin and noradrenaline on value of responses by command neurons of defensive behavior inHelix pomatia,”Zh. Vissh. Nerv. Deyat.,37, No. 2, 122–127 (1987).

    Google Scholar 

  122. J. Kupferman and K. R. Weiss, “Functional studies on the metacerebral cells inAplysia,”Abstr. Proc. Neurosci.,3, No. 5, 375 (1974).

    Google Scholar 

  123. K. R. Weiss, J. Chen, and I. Kupferman, “Potentiation of muscle contraction: A possible modulatory function of an identified serotonergic cell inAplysia,”Brain Res.,99, No. 3, 381 (1975).

    Google Scholar 

  124. S. J. Wieland and A. Gelperin, “Dopamine elicits feeding motor program inLimax maximus,”J. Neurosci.,3, No. 9, 1735–1745 (1983).

    Google Scholar 

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Neirofiziologiya/Neurophysiology, Vol. 25, No. 3, pp. 224–232, May–June, 1993.

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Antonov, I.N. Mechanisms of heterosynaptic facilitation in molluscan neurons. Neurophysiology 25, 191–199 (1993). https://doi.org/10.1007/BF01053150

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