Survival of Egg-Laying Controlling Neuroendocrine Cells During Reproductive Senescence of a Mollusc


During brain aging neuronal degradation occurs. In some neurons this may result in degeneration and cell death, still other neurons may survive and maintain their basic properties. The present study deals with survival of the egg-laying controlling neuroendocrine caudodorsal cells (CDCs) during reproductive senescence of the pond snail Lymnaea stagnalis. In senescent animals CDCs exhibited reduced branching patterns but still maintained their electrophysiological characteristics. In the isolated CNS the cells could still respond with an afterdischarge upon electrical stimulation. After an extended period of no egg laying of Lymnaea CDCs failed to exhibit an afterdischarge. In senescent CDCs that failed an afterdischarge, discharge activity could be restored by exposure to peptides released by CDCs from reproductive animals. Moreover, raising the intracellular cAMP level could induce discharge activity in CDCs with afterdischarge failure. Discharge activity also occurred during depolarization of senescent CDCs by exposure of the cells to saline with a high potassium concentration. These results indicate that in senescent CDCs the pacemaking mechanism of the afterdischarge is still intact but that the initial activation fails. Chemical (auto)transmission of CDCs in such animals was indeed reduced as indicated by the small amplitude of the depolarizing afterpotential (DAP) induced by electrical stimulation. Interestingly, CDCs of senescent animals contained a relative large amount of a particular small peptide. The artificially synthesized peptide appeared to suppress DAP induction in CDCs. Possibly, release of the peptide contributes to the prevention of afterdischarge induction in senescent CDCs. The results so far indicate that in senescent Lymnaea neurons electrophysiological functions persist even after long periods of inactivity and severe morphological reduction.


  1. 1.

    Brussaard, A. B., Kits, K. S., TerMaat, A., Van Minnen, J., Moed, P. J. (1988) Dual inhibitory action of FMRFamide on neurosecretory cells controlling egg-laying behavior in the pond snail. Brain Res. 447, 35–51.

    CAS  Article  Google Scholar 

  2. 2.

    Brussaard, A. B., Schluter, N. C. M., Ebberink, R. H. M., Kits, K. S., TerMaat, A. (1990) Discharge induction in molluscan peptidergic cells requires a specific set of four autoexcitatory neuropeptides. Neuroscience 39, 479–491.

    CAS  Article  Google Scholar 

  3. 3.

    DeVlieger, T. A., Kits, K. S., TerMaat, A., Lodder, J. C. (1980) Morphology and electrophysiology of the ovulation hormone producing neuroendocrine cells of the freshwater snail Lymnaea stagnalis (L.). J. Exp. Biol. 84, 259–271.

    CAS  Google Scholar 

  4. 4.

    Geraerts, W. P. M., TerMaat, A., Vreugdenhil, E. (1988) The peptidergic neuroendocrine control of egg laying behavior in Aplysia and Lymnaea. In: H. Laufer and G. H. Downer (eds) Endocrinology of selected invertebrate types. Vol. II. Alan R. Liss, New York, pp. 141–231.

    Google Scholar 

  5. 5.

    Hermann, P. M., Ter Maat, A., Jansen, R. F. (1994) The neuronal control of egg-laying behaviour in the pond snail Lymnaea stagnalis: motor control of shell turning. J. Exp. Biol. 197, 79–99.

    CAS  PubMed  Google Scholar 

  6. 6.

    Hermann, P. M., De Lange, R. P. J., Pieneman, A. W., TerMaat, A., Jansen, R. F. (1997) The role of neuropeptides encoded on the CDCH-1 gene in the organisation of egg laying behavior in the pond snail, Lymnaea stagnalis. J. Neurophysiol. 78, 2859–2869.

    CAS  Article  Google Scholar 

  7. 7.

    Janse, C., Joosse, J. (1989) Aging in molluscan nervous and neuroendocrine systems. In: Schreibman, M. P., Scanes, C. G. (eds) Development, maturation, and senescence of neuroendocrine systems. A comparative approach. Academic Press New York, pp. 43–61.

    Google Scholar 

  8. 8.

    Janse, C., Slob, W., Popelier, C. M., Vogelaar, J. W. (1988) Survival characteristics of the mollusc Lymnaea stagnalis under constant culture conditions: effects of aging and disease. Mech. Ageing Dev. 42, 263–274.

    CAS  Article  Google Scholar 

  9. 9.

    Janse, C., Wildering, W. C., Popelier, C. M. (1989) Age-related changes in female reproductive activity and growth in the mollusc Lymnaea stagnalis. J. Gerontol. 44, B 148–155.

    Article  Google Scholar 

  10. 10.

    Janse, C., TerMaat, A., Pieneman, A. W. (1990) Molluscan ovulation hormone containing neurons and age-related reproductive decline. Neurobiol. Aging 11, 457–463.

    CAS  Article  Google Scholar 

  11. 11.

    Janse, C., van der Roest, M., Jansen, R. F., Montagne-Wajer, C., Boer, H. H. (1996) Atrophy and degeneration of peptidergic neurons and cessation of egg-laying in the aging pond snail Lymnaea stagnalis. J. Neurobiol. 29, 202–212.

    CAS  Article  Google Scholar 

  12. 12.

    Janse, C., Peretz, B., van der Roest, M., Dubelaar, E. J. G. (1999) Excitability and branching of neuroendocrine cells during reproductive senescence. Neurobiol. Aging 20, 675–683.

    CAS  Article  Google Scholar 

  13. 13.

    Janse, C., van der Roest, M. (2001) cAMP and excitability in neuroendocrine cells during reproductive senescence. Neurobiol. Aging 22, 503–514.

    CAS  Article  Google Scholar 

  14. 14.

    Jiménez, C. R. (1997) Generation of complex peptide diversity in neuroendocrine cells of Lymnaea stagnalis and the rat. Thesis Vrije Universiteit, Amsterdam, The Netherlands.

    Google Scholar 

  15. 15.

    Kits, K. S. (1980) States of excitability in ovulation hormone producing neuroendocrine cells of Lymnaea stagnalis (Gastropoda) and their relation to the egg-laying cycle. J. Neurobiol. 11, 397–410.

    CAS  Article  Google Scholar 

  16. 16.

    Kits, K. S., Bos, N. P. A. (1981) Pacemaking mechanisms of the afterdischarge of the caudodorsal cells. J. Neurobiol. 12, 424–441.

    Article  Google Scholar 

  17. 17.

    Kits, K. S., Dreijer, A. M. C., Lodder, J. C., Borgdorff, A., Wadman, W. J. (1997) High intracellular calcium levels during and after electrical discharges in molluscan peptidergic neurons. Neuroscience 79, 275–284.

    CAS  Article  Google Scholar 

  18. 18.

    Klaassen, L., Janse, C., van der Roest, M. (2002) Recovery of neuroendocrine cells after injury in the aging brain of a mollusc. Neurobiol. Aging 23, 295–307.

    CAS  Article  Google Scholar 

  19. 19.

    Leventhal, A. G., Wang, Y., Pu, M., Zhou, Y., Ma, Y. (2003) GABA and its agonists improved visual cortical function in senescent monkeys. Science 300, 812–815.

    CAS  Article  Google Scholar 

  20. 20.

    Moed, P. J., Pieneman, A. W., Bos, N. P. A., TerMaat, A. (1989) The role of cAMP in regulation of electrical activity of the neuroendocrine caudodorsal cells of Lymnaea stagnalis. Brain Res. 476, 298–306.

    CAS  Article  Google Scholar 

  21. 21.

    Morrison, J. H., Hof, P. R. (1997) Life and death of neurons in the aging brain. Science 278, 412–419.

    CAS  Article  Google Scholar 

  22. 22.

    Slob, W., Janse, C. (1988) A quantitative method to evaluate the quality of interrupted animal cultures in aging studies. Mech. Ageing and Dev. 42, 275–290.

    CAS  Article  Google Scholar 

  23. 23.

    Swaab, D. F., Dubelaar, E. J. G., Hofman, M. A., Scherder, E. J. A., van Someren, E. J. W., Verwer, R. W. H. (2002) Brain aging and Alzheimer’s disease; use it or lose it. Progr. Brain Res. 138, 345–373.

    Google Scholar 

  24. 24.

    TerMaat, A., Dijks, F. A., Bos, N. P. A. (1986) In vivo recordings of neuroendocrine cells (caudodorsal cells) in the pond snail. J. Comp. Physiol. 158A, 853–859.

    Article  Google Scholar 

  25. 25.

    TerMaat, A., Geraerts, W. P. M., Jansen, R. F., Bos, N. P. (1988) Chemically mediated positive feed back generates long-lasting afterdischarge in a molluscan neuroendocrine system. Brain Res. 438, 77–82.

    CAS  Article  Google Scholar 

  26. 26.

    TerMaat, A. (1992) Egg laying in the hermaphrodite pond snail Lymnaea stagnalis. Progr. Brain Res. 92, 345–359.

    CAS  Article  Google Scholar 

  27. 27.

    Zolman, J. F., Peretz, B. (1987) Motor neuronal function in old Aplysia is improved by long-term stimulation of the siphon/gill reflex. Behav. Neurosci. 101, 1–10.

    Article  Google Scholar 

Download references

Author information



Corresponding author

Correspondence to C. Janse.

Additional information

Presented at the 10th ISIN Symposium on Invertebrate Neurobiology, July 5–9, 2003, Tihany, Hungary.

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (, which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Reprints and Permissions

About this article

Cite this article

Janse, C. Survival of Egg-Laying Controlling Neuroendocrine Cells During Reproductive Senescence of a Mollusc. BIOLOGIA FUTURA 55, 251–259 (2004).

Download citation


  • Senescence
  • reproduction
  • neuroendocrine cells
  • neuropeptides
  • neurophysiology