Skip to main content
SpringerLink
Log in

Control of the cardiovascular system ofAplysia by identified neurons

  • Multi-Author Reviews
  • Control of Circulation in Invertebrates
  • Published:
Experientia Aims and scope Submit manuscript

Abstract

The neural network that controls the cardiovascular system ofAplysia adapts cardiovascular function to a variety of different physiological and behavioral situations. It (1) coordinates the cardiovascular system with the renal and respiratory systems; (2) modifies both systemic and regional blood flow during food-elicited arousal and feeding; and (3) changes the tension of longitudinal vascular muscle to adapt the arterial tree to changes in body shape. Indirect evidence suggests that the cardiovascular control circuit may also play a role in maintaining homeostasis during egg laying. Several putative neurotransmitters, including acetylcholine, serotonin, R15α1 and R15α2 peptides, have been localized to identified neurons in this circuit.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literatur

  1. Alevizos, A., Bailey, C. H., Chen, M., and Koester, J., Innervation of vascular and cardiac muscle ofAplysia by multimodal motoneuron L7. J. Neurophysiol.61 (1989) 1053–1063.

    Article  CAS  PubMed  Google Scholar 

  2. Alevizos, A., Karagogeos, D., Weiss, K. R., Buck, L., and Koester, J., R15α1 and R15α2 peptides fromAplysia: comparison of bioactivity, distribution, and function of two peptides generated by alternative splicing. J. Neurobiol.22 (1991) 405–417.

    Article  CAS  PubMed  Google Scholar 

  3. Alevizos, A., Weiss, K. R., and Koester, J., Myomodulin: a possible cotransmitter of the cholinergic neuron L10 ofAplysia. Soc. Neurosci. Abstr.13 (1987) 1072.

    Google Scholar 

  4. Alevizos, A., Weiss, K. R., and Koester, J., Synaptic actions of identified peptidergic neuron R15 inAplysia: I. Activation of respiratory pumping. J. Neurosci.11 (1991) 1263–1274.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Alevizos, A., Weiss, K. R., and Koester, J. Synaptic actions of identified peptidergic neuron R15 inAplysia. II. Contraction of pleuroabdominal connectives mediated by motoneuron L7. J. Neurosci.11 (1991) 1275–1281.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Alevizos, A., Weiss, K. R., and Koester, J., Synaptic actions of identified peptidergic neuron R15 inAplysia. III. Activation of the large hermaphroditic duct. J. Neurosci.11 (1991) 1282–1290.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Andrews, E. B., Excretory systems of molluscs, in: The Mollusca, vol. 11, pp. 381–448. Eds A. S. M. Saleuddin and K. M. Wilbur. Academic Press, Inc., New York 1988.

    Google Scholar 

  8. Arshavsky, Y. L., Deliagina, T. G., Gelfand, I. M., Orlovsky, G. N., Panchin, Y. V., Pavlova, G. A., and Popova, L. B., Neural control of heart beat in the pteropod molluscClione limacina: coordination of circulatory and locomotor systems. J. exp. Biol.148 (1990) 461–475.

    Article  Google Scholar 

  9. Blankenship, J. E., Wachtel, H., and Kandel, E. R., Ionic mechanisms of excitatory, inhibitory, and dual synaptic actions mediated by an identified interneuron in abdominal ganglion ofAplysia. J. Neurophysiol.34 (1971) 76–92.

    Article  CAS  PubMed  Google Scholar 

  10. Branton, D. W., Mayeri, E., Brownell, P., and Simon, S. S., Evidence for local hormonal communication between neurons inAplysia. Nature274 (1978) 70–72.

    Article  CAS  PubMed  Google Scholar 

  11. Brown, R. O., and Mayeri, E., Central actions of R15, a putative peptidergic neuron inAplysia. J. Neurobiol.18 (1987) 3–13.

    Article  CAS  PubMed  Google Scholar 

  12. Brownell, P. H., Mechanisms of circulatory homeostasis and response inAplysia. Experientia48 (1992) 818–827.

    Article  CAS  PubMed  Google Scholar 

  13. Buck, L. B., Bigelow, J. M., and Axel, R., Alternative splicing in individualAplysia neurons generates neuropeptide diversity. Cell51 (1987) 127–133.

    Article  CAS  PubMed  Google Scholar 

  14. Bucket, K. J., Peters, M., and Benjamin, P. R., Excitation and inhibition of the heart of the snail,Lymnaea, by non-FMRFamidergic motoneurons. J. Neurophysiol.63 (1990) 1436–1447.

    Article  Google Scholar 

  15. Buckett, K.J., Peters, M., Dockray, D. J., van Minnen, J., and Benjamin, P. R., Regulation of heartbeat inLymnaea, by motoneurons containing FMRFamide-like peptides. J. Neurophysiol.63 (1990) 1413–1425.

    Article  CAS  PubMed  Google Scholar 

  16. Byrne, J., Identification and initial characterization of a cluster of command and pattern-generating neurons underlying respiratory pumping inAplysia californica. J. Neurophysiol.49 (1983) 491–508.

    Article  CAS  PubMed  Google Scholar 

  17. Byrne, J., and Koester, J., Respiratory pumping: neuronal control of a centrally commanded behavior inAplysia. Brain Res.143 (1978) 87–105.

    Article  CAS  PubMed  Google Scholar 

  18. Campanelli, J. T., and Scheller, R. H., Histidine-rich basic peptides: a cardioactive neuropeptide fromAplysia neurons R3-14. J. Neurophysiol.57 (1987) 1201–1209.

    Article  CAS  PubMed  Google Scholar 

  19. Carew, T. J., Pinsker, H., Rubinson, K., and Kandel, E. R., Physiological and biochemical properties of neuromuscular transmission between identified motoneurons and gill muscle inAplysia. J. Neurophysiol.37 (1974) 1020–1040.

    Article  CAS  PubMed  Google Scholar 

  20. Church, P. J., and Lloyd, P. E., Expression of diverse neuropeptide co-transmitters by identified motor neurons inAplysia. J. Neurosci.11 (1991) 618–625.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Croll, R. P., Sensory control of respiratory pumping inAplysia californica. J. exp. Biol.117 (1985) 15–27.

    Article  Google Scholar 

  22. Dieringer, N., Koester, J., and Weiss, K., Adaptive changes in heart rate ofAplysia californica. J. comp. Physiol.123 (1978) 11–21.

    Article  Google Scholar 

  23. Drummond, G. I., Wernham, S., and Lukowiak, K., Stimulation of adenylate-cyclase in the heart ofAplysia californica by biogenic amines. Comp. Biochem. Physiol.80 (1980) 129–133.

    Google Scholar 

  24. Dudek, F. E., Cobbs, J. S., and Pinsker, H. M., Bag cell electrical activity underlying spontaneous egg laying in freely behavingAplysia brasiliana. J. Neurophysiol.42 (1979) 804–817.

    Article  CAS  PubMed  Google Scholar 

  25. Duval A., Heartbeat and blood pressure in terrestrial slugs. Can. J. Zool.61 (1983) 987–992.

    Article  Google Scholar 

  26. Eales, N. B.,Aplysia. Liverpool Marine Biology Committee, Proc. Trans. Liverpool Biol. Soc. (L.M.B.C. Mem. vol. 35),24 (1921) 183–266.

    Google Scholar 

  27. Eberly, L., Kanz, J., Taylor, C., and Pinsker, H., Environmental modulation of a central pattern generator in freely behavingAplysia. Behav. neural Biol.32 (1981) 21–34.

    Article  CAS  PubMed  Google Scholar 

  28. Frazier, W. T., Kandel, E. R., Kupfermann, I., Waziri, R., and Coggeshall, R. E., Morphological and functional properties of identified neurons in the abdominal ganglion ofAplysia californica. J. Neurophysiol.30 (1967) 128–135.

    Article  Google Scholar 

  29. Furgal, S. M., and Brownell, P. H., Ganglionic circulation and its effects on neurons controlling cardiovascular functions inAplysia californica. J. exp. Zool.244 (1987) 347–363.

    Article  CAS  PubMed  Google Scholar 

  30. Furukawa, Y., and Kobayashi, M., Neural control of the heart beat in the African giant snail,Achatina fulica Férussac I. Identification of the heart regulatory neurones. J. exp. Biol.129 (1987) 279–293.

    Article  Google Scholar 

  31. Giller, E., and Schwartz, J. H., Choline acetyltransferase in identified neurons of abdominal ganglion ofAplysia californica. J. Neurophysiol.34 (1971) 93–107.

    Article  CAS  PubMed  Google Scholar 

  32. Grega, D. D., and Prior, D. J., The effects of feeding on heart activity in the terrestrial slug,Limax maximus: central and peripheral control. J. comp. Physiol. A156 (1985) 539–545.

    Article  Google Scholar 

  33. Harris, L. L., and Ono, J. K., The distribution of immunoreactive FMRFamide in neuronal fibers, varicosities, and somata in the heart of the sea hare,Aplysia californica. Soc. Neurosci. Abstr.16 (1990) 549.

    Google Scholar 

  34. Hening, W. A. Central generation and coordination of a complex behavioral sequence inAplysia californica: Locomotion and respiratory pumping. Ph.D. Dissertation, New York University, 1982.

  35. Kandel, E. R., Behavioral Biology ofAplysia. Freeman, 1979.

  36. Kandel, E. R., Frazier, W. T., Waziri, R., and Coggeshall, R. E. Direct and common connections among identified neurons inAplysia. J. Neurophysiol.30 (1967) 1352–1376.

    Article  CAS  PubMed  Google Scholar 

  37. Kehoe, J., The physiological role of three acetylcholine receptors in synaptic transmission inAplysia. J. Physiol.225 (1972) 147–172.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Kobayashi, M., and Muneoka, Y., Structure and action of molluscan neuropeptides. Zool. Sci.7 (1990) 801–814.

    CAS  Google Scholar 

  39. Koch, U. T., and Koester, J., Time sharing of heart power: cardiovascular adaptations to food arousal inAplysia. J. comp. Physiol.149 (1982) 31–42.

    Article  Google Scholar 

  40. Koch, U. T., Koester, J., and Weiss, K. R., Neuronal mediation of cardiovascular effects of food arousal inAplysia. J. Neurophysiol.51 (1984) 126–135.

    Article  CAS  PubMed  Google Scholar 

  41. Koester, J., Chemically and electrically coupled interneurons mediate respiratory pumping inAplysia. J. Neurophysiol.62 (1989) 1113–1126.

    Article  CAS  PubMed  Google Scholar 

  42. Koester, J., and Alevizos, A., Innervation of the kidney ofAplysia by L10, the LUQ cells, and an identified peripheral motoneuron. J. Neurosci.9 (1989) 4078–4088.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Koester, J., and Kandel, E. R., Further identification of neurons in the abdominal ganglion ofAplysia using behavioral criteria. Brain Res.121 (1977) 1–21.

    Article  CAS  PubMed  Google Scholar 

  44. Koester, J. and Koch, U. T., Neural control of the circulatory system ofAplysia. Experientia43 (1987) 972–980.

    Article  CAS  PubMed  Google Scholar 

  45. Koester, J., Dieringer, N., and Mandelbaum, D. E., Cellular neuronal control of molluscan heart. Am. Zool.19 (1979) 103–116.

    Article  CAS  Google Scholar 

  46. Koester, J., Mayeri, E., Liebeswar, G., and Kandel, E. R., Neural control of circulation inAplysia. II. Interneurons. J. Neurophysiol.37 (1974) 476–496.

    Article  CAS  PubMed  Google Scholar 

  47. Krontiris-Litowitz, J. K., Cooper, B. F., and Walters, E. T., Humoral factors released during trauma ofAplysia body wall. I. Body wall contraction, cardiac modulation, and reflex suppression. J. comp. Physiol.159 (1989) 211–223.

    Article  CAS  Google Scholar 

  48. Kupfermann, I., Feeding behavior inAplysia: a simple system for the study of motivation. Behav. Biol.10 (1974) 1–26.

    Article  CAS  PubMed  Google Scholar 

  49. Kupfermann, I., and Carew, T. J., Behavior patterns ofAplysia in its natural environment. Behav. Biol.12 (1974) 317–337.

    Article  CAS  PubMed  Google Scholar 

  50. Kupfermann, I., Carew, T. J., and Kandel, E. R., Local, reflex and central commands controlling gill and siphon movements inAplysia. J. Neurophysiol.37 (1974) 996–1001.

    Article  CAS  PubMed  Google Scholar 

  51. Kurokawa, M., and Kuwasawa, K., Electrophysiological studies on the branchial ganglion in the opisthobranch molluscs (Aplysia andDolabella). J. comp. Physiol.156 (1985) 35–44.

    Article  Google Scholar 

  52. Levy, M., Achituv, Y., and Susswein, A. J., Relationship between respiratory pumping and oxygen consumption inAplysia depilans andAplysia fasciata. J. exp. Biol.141 (1989) 389–405.

    Article  Google Scholar 

  53. Liebeswar, G., Goldman, J.E., Koester, J., and Mayeri, E., Neural control of circulation inAplysia. III. Neurotransmitters. J. Neurophysiol.38 (1975) 767–779.

    Article  CAS  PubMed  Google Scholar 

  54. Ligman, S.H., and Brownell, P.H. Differential hormonal action of the bag cell neurons on the arterial system ofAplysia. J. comp. Physiol.157 (1985), 31–37.

    Article  CAS  Google Scholar 

  55. Lloyd, P. E., The small cardioactive peptides: a class of modulatory neuropeptides inAplysia. Trends Neurosci.9 (1986) 428–431.

    Article  CAS  Google Scholar 

  56. Lloyd, P.E., Kupfermann, I., and Weiss, K. R., Two endogenous neuropeptides (SCPA and SCPB) produce a cAMP-mediated stimulation of cardiac activity inAplysia. J. comp. Physiol.156 (1985) 659–667.

    Article  CAS  Google Scholar 

  57. Mandelbaum, D.E., Koester, J., Schonberg, M., and Weiss, K.R., Cyclic AMP mediation of the excitatory effect of serotonin in the heart ofAplysia. Brain Res.,177 (1979) 388–394.

    Article  CAS  PubMed  Google Scholar 

  58. Mayeri, E., Koester, J., Kupfermann, I., Liebeswar, G., and Kandel, E.R., Neural control of circulation inAplysia. I. Motoneurons. J. Neurophysiol.37 (1974) 458–475.

    Article  CAS  PubMed  Google Scholar 

  59. McMahon, B. R., and Burnett, L. E., The crustacean open circulatory system: a reexamination. Physiol. Zool.63 (1990) 35–71.

    Article  Google Scholar 

  60. Miller, M. W., Alevizos, A., Cropper, E. C., Kupfermann, I., and Weiss, K. R., Localization of buccalin-like immunoreactivity in the central nervous system and peripheral tissues ofAplysia californica. J. comp. Neurol. (1992) in press.

  61. Miller, M. W., Alevizos, A., Cropper, E.C., Vilim, F., Karagogeos, D., Kupfermann, I., and Weiss, K.R., Localization of myomodulin-like immunoreactivity in the central nervous system and peripheral tissues ofAplysia californica. J. comp. Neurol. 313 (1991) 1–8.

    Google Scholar 

  62. Perlman, A.J., Central and peripheral control of siphon-withdrawal reflex inAplysia californica. J. Neurophysiol.42 (1979) 510–529.

    Article  CAS  PubMed  Google Scholar 

  63. Pinsker, H., Kupfermann, I., Castellucci, V., and Kandel, E.R., Habituation and dishabituation of the gill-withdrawal reflex inAplysia. Science167 (1970) 1740–1742.

    Article  CAS  PubMed  Google Scholar 

  64. Pinsker, M.H., and Dudek, F.E., Bag cell control of egg laying in freely behavingAplysia. Science197 (1977) 490–493.

    Article  CAS  PubMed  Google Scholar 

  65. Price, C.H., and McAdoo, D.J., Localization of axonally transported3H-glycine in vesicles of identified neurons. Brain Res.219 (1981) 307–315.

    Article  CAS  PubMed  Google Scholar 

  66. Prince, C.H., Fowle, W., and Rittenhouse, A.R., Anatomy and innervation of the anterior aorta ofAplysia and the ultrastructure of specialized neuromuscular junctions of vascular smooth muscle. J. comp. Neurol.222 (1984) 366–382.

    Article  Google Scholar 

  67. Rittenhouse, A.R., and Price, C.H., Peripheral axons of the parabolic burster neuron R15. Brain Res.333 (1985) 330–335.

    Article  CAS  PubMed  Google Scholar 

  68. Rittenhouse, A.R., and Price, C.H., Anatomical and electrophysiological study of multitransmitter neuron R14. J. comp. Neurol.247 (1986) 447–456.

    Article  CAS  PubMed  Google Scholar 

  69. Rittenhouse, A.R., and Price, C.H., Axons and target tissues ofAplysia neurons R3-14 and their status as multifunctional, multimessenger neurons. J. Neurosci.6 (1986) 2071–2084.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Rózsa, K.S., Organization of the multifunctional neural network regulating visceral organs inHelix pomatia (Mollusca, Gastropoda). Experientia43 (1987) 965–972.

    Article  Google Scholar 

  71. Sawada, M., Blankenship, J.E., and McAdoo, D.J., Neural control of a molluscan blood vessel, anterior aorta ofAplysia. J. neurophysiol.46 (1981) 967–986.

    Article  CAS  PubMed  Google Scholar 

  72. Sawada, M., Ichinose, M., Ito, I., Maeno, T., and McAdoo, D.J., Effects of 5-hydroxytryptamine on membrane potential, contractility, accumulation of cyclic-AMP, and Ca++ movements in anterior aorta and ventricle ofAplysia. J. Neurophysiol.51 (1984) 361–374.

    Article  CAS  PubMed  Google Scholar 

  73. Sawada, M., McAdoo, D.J., Ichinose, M., and Price, C.H., Influences of glycine and neuron R14 on contraction of the anterior aorta ofAplysia. Jap. J. Physiol.34 (1984) 747–767.

    Article  CAS  Google Scholar 

  74. Schaefer, M., Picciolotto, M.R., Kreiner, T., Kaldany, R., Taussig, R., and Scheller, R.H.,Aplysia neurons express a gene encoding multiple FMRFamide neuropeptide. Cell41 (1985) 457–467.

    Article  CAS  PubMed  Google Scholar 

  75. Skelton, M.E., and Koester, J., Innervation of the heart ofAplysia by serotonin- and R15α2 peptide-immunoreactive terminals and by neuron L2. Soc. Neurosoci. Abstr.17 (1991) 1355.

    Google Scholar 

  76. Skelton, M.E., and Koester, J., Morphology, innervation and neural control of the anterior arterial system ofAplysia. J. comp. Physiol. (1992) in press.

  77. Skelton, M.E., Weiss, K.R., and Koester, J., The serotonergic heart exciter neuron RBHE ofAplysia californica synthesizes R15α2 peptide. Soc. Neurosci. Abstr.16 (1990) 549.

    Google Scholar 

  78. Smith, P.J.S., Cardiac output in the Mollusca: scope and regulation. Experientia43 (1987) 956–965.

    Article  Google Scholar 

  79. Taussig, R., Kaldany, R.R., Rothbard, J.B., Schoolnik, G., and Scheller, R.H., Expression of the L11 neuropeptide gene in theAplysia central nervous system. J. comp. Neurol.238 (1985) 53–64.

    Article  CAS  PubMed  Google Scholar 

  80. Teyke, T., Weiss, K.R., and Kupfermann, I., Appetitive feeding behavior ofAplysia: behavioral and neural analysis of directed head turning. J. Neurosci.10 (1990) 3922–3934.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Twarog, B.M., Serotonin: history of a discovery. Comp. Biochem. Physiol.91C (1988) 21–24.

    CAS  Google Scholar 

  82. Umitsu, Y., Masumoto, H., and Koike, H., Active contraction of nerve bundle and identification of a nerve-contractor motoneuron inAplysia. J. Neurophysiol.58 (1987) 1016–1034.

    Article  CAS  PubMed  Google Scholar 

  83. Walters, E.T., and Erickson, M.T., Directional control and the functional organization of defensive responses inAplysia. J. comp. Physiol. A159 (1986) 339–351.

    Article  CAS  PubMed  Google Scholar 

  84. Weiss, K.R., Bayley, H., Lloyd, P.E., Tenenbaum, R., Gawinowicz-Kolks, M.A., Buck, L., Cropper, E.C., Rosen, S.C., and Kupfermann, I., Purification and sequencing of neuropeptides contained in neuron R15 ofAplysia californica. Proc. natl Acad. Sci. USA86 (1989) 2913–2917.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Welsford, I.G., and Prior, D., Modulation of heart activity in the terrestrial slugLimax maximus by the feeding motor program, small cardioactive peptides and stimulation of buccal neuron B1. J. exp. Biol.155 (1991) 1–19.

    Article  CAS  PubMed  Google Scholar 

  86. Wickham, L., and DesGroseillers, L., A bradykinin-like neuropeptide precursor gene is expressed in neuron L5 ofAplysia californica. DNA Cell Biol.10 (1991) 249–258.

    Article  CAS  PubMed  Google Scholar 

  87. Wiens, B.L., and Brownell, P.H., Characterization of cardiac innervation in the nudibranch,Archidoris montereyensis. J. comp. Physiol.167 (1990) 51–60.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Center for Neurobiology and Behavior, Columbia University and New York State Psychiatric Institute, 722 West 168th Street, 10032, New York, New York, USA

    M. Skelton & J. Koester

  2. Propileon 23, Acropolis 11742, Athens, Greece

    A. Alevizos

Authors
  1. M. Skelton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Alevizos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Koester
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Skelton, M., Alevizos, A. & Koester, J. Control of the cardiovascular system ofAplysia by identified neurons. Experientia 48, 809–817 (1992). https://doi.org/10.1007/BF02118413

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02118413

Key words

Search

Navigation