Summary
Several environmental factors influence the growth of the basommatophoran freshwater snail Lymnaea stagnalis. Growth is hormonally controlled by 4 cerebral clusters of ca 50–75 peptidergic, neuroendocrine Light Green Cells (LGC). The present light, transmission, and scanning electron microscopic study shows that the LGC are synaptically contacted by a tentacle sensory system (TSS). The TSS consists of 2 types of primary sensory neurone, viz. ca 150 S1-cells and ca 50–100 S2-cells. A S1-cell has a non-ciliated dendrite and an axon branch that synaptically contacts the soma of a S2-cell. A S2-cell has a branching, ciliated dendrite. Probably, S1- and S2-cells have different sensory modalities and can integrate sensory information by intersensory interaction. The S2-axons run through the tentacular nerves, the cerebral ganglia, and the intercerebral commissure. In each ganglion S2-axons branch and form synaptic contacts on the axons and somata of the LGC and on glial cells that surround the LGC. In an LGC-cluster, 1–3 LGC-somata are particularly strongly innervated. Probably, the TSS is involved in the environmental control of growth in L. stagnalis.
Similar content being viewed by others
References
Alkon DL, Akaike T, Harrigan J (1978) Interaction of chemosensory, visual and statocyst pathways in Hermissenda crassicornis. J Gen Physiol 71:177–194
Bannister LH (1965) The fine structure of the olfactory surface of teleostean fishes. Quart J Micr Sci 106:333–342
Benjamin PR, Swindale NV, Slade CT (1976) Electrophysiology of identified neurosecretory neurones in the pond snail, Lymnaea stagnalis (L.). In: Salánki (ed) Neurobiology of invertebrates — Gastropoda brain. Akadémiai Kiadó, Budapest, pp 85–100
Boer HH, Douma E, Koksma JMA (1968) Electron microscope study of neurosecretory cells and neurohaemal organs in the pond snail Lymnaea stagnalis. Symp Zool Soc Lond 22:237–256
Boer HH, Schot LPC, Roubos EW, Maat A ter, Lodder JC, Reichelt D, Swaab DF (1979) ACTH-like immunoreactivity in two electrotonically coupled giant neurones in the pond snail Lymnaea stagnalis. Cell Tissue Res 202:231–240
Bohlken S, Joosse J (1982) The effect of photoperiod on female reproductive activity and growth of the freshwater pulmonate snail Lymnaea stagnalis kept under laboratory breeding conditions. Int J Inv Reprod 4:213–222
Brousse-Gaury P (1971a) Influences de stimuli externes sur le comportement neuro-endocrinien de blattes. I. Les organes sensoriels céphaliques, point de départ des réflexes neuro-endocriniens. Ann Sci Nat Zool 13:181–332
Brousse-Gaury P (1971b) Influence de stimuli externes sur le comportement neuro-endocrinien de blattes. II. Histophysiologie des voies réflexes neuro-endocriniennes. Ann Sci Nat Zool 13:333–450
Dellman HD, Rodríguez EM (1970) Herring bodies; an electron microscope study of local degeneration and regeneration of neurosecretory axons. Z Zellforsch 111:293–315
Geraerts WPM (1976) Control of growth by the neurosecretory hormone of the Light Green Cells in the freshwater snail Lymnaea stagnalis. Gen Comp Endocrinol 29:61–71
Hanström B (1925) Über die sogenannten Intelligenzsphären des Molluskengehirns und Innervation des Tentakels von Helix. Acta Zool 6:183–215
Hökfelt T, Johansson O, Ljungsdahl Å, Lundberg JM, Schultzberg M (1980) Peptidergic neurones. Nature 284:515–521
Hughes HPI (1970) A light and electron microscope study of some opisthobranch eyes. Z Zellforsch 106:79–98
Iversen LL, Lee CM, Gilbert RF, Hunt S, Emson PC (1980) Regulation of neuropeptide release. Proc R Soc Lond 210:91–111
Janse C, Swigchem H van (1975) Neurophysiological properties of primary touch sensitive neurones in the gastropod mollusc Lymnaea stagnalis (L.). J Comp Physiol 103:343–351
Joosse J (1964) Dorsal bodies and dorsal neurosecretory cells of the cerebral ganglia of Lymnaea stagnalis L. Arch Néerl Zool 15:1–103
Joosse J, Vlieger TA de, Roubos EW (in press) Nervous systems of lower animals as models, with particular reference to peptidergic neurones in gastropods. In: Buijs RM, Pévet P, Swaab DF (eds) Progr Brain Res Vol 55, Chemical Transmission in the Brain. Elsevier Biomedical Press, Amsterdam
Lincoln DW (1974) Dynamics of oxytocin secretion. In: Knowles F, Vollrath L (eds) Neurosecretion — The final common pathway. Springer-Verlag, Berlin Heidelberg New York, pp 129–133
Maat A ter (1979) Neuronal input on the ovulation hormone producing neuroendocrine Caudo-Dorsal Cells of the freshwater snail Lymnaea stagnalis. Proc Kon Ned Akad Wet C 82:333–342
Maat A ter, Roubos EW, Lodder JC, Buma P (in press) Integration of synaptic input modulating pacemaker activity of electrotonically coupled neuroendocrine Caudo-Dorsal Cells in the pond snail. J Neurophysiol
Maddrell SHP (1963) Excretion in the blood-sucking bug, Rhodnius prolixus Stal. 1. The control of diuresis. J Exp Biol 40:247–256
McDonald SLC (1969) The biology of Lymnaea stagnalis L. (Gastropoda Pulmonata). Sterkiana 36:1–17
Minnen J van, Reichelt D (1980) Effects of photoperiod on the activity of neurosecretory cells in the Lateral Lobes of the cerebral ganglia of the pond snail Lymnaea stagnalis, with particular reference to the Canopy Cell. Proc Kon Ned Akad Wet C 83:1–13
Minnen J van, Reichelt D, Lodder JC (1979) An ultrastructural study of the neurosecretory Canopy Cell of the pond snail Lymnaea stagnalis (L.), with the use of the horseradish peroxidase tracer technique. Cell Tissue Res 204:453–462
Murray PG (1973) The ultrastructure of taste buds. In: Friedmann I (ed) The ultrastructure of sensory organs. North Holland, American Elsevier Publ Comp, Amsterdam London New York, pp 1–84
Nordmann JJ, Louis F, Morris SJ (1979) Purification of two structurally and morphologically distinct populations of rat neurohypophyseal secretory granules. Neuroscience 4:1367–1379
Phillips DW (1979) Ultrastructure of sensory cells of the mantle tentacles of the gastropod Notoacmea scutum. Tissue Cell 11:623–632
Roubos EW (1975) Regulation of neurosecretory activity in the freshwater pulmonate Lymnaea stagnalis (L.) with particular reference to the role of the eyes. Cell Tissue Res 160:291–314
Roubos EW (in press) Intracellular and extracellular control of neuroendocrine activity in the freshwater snail Lymnaea stagnalis. In: Lofts B (ed) Advances in Comparative Endocrinology. Hong Kong University Press, Hong Kong
Roubos EW, Moorer-van Delft CM (1979) Synaptology of the central nervous system of the freshwater snail Lymnaea stagnalis (L.), with particular reference to neurosecretion. Cell Tissue Res 198:217–235
Roubos EW, Wal-Divendal RM van der (1980) Ultrastructural analysis of peptide-hormone release by exocytosis. Cell Tissue Res 207:267–275
Roubos EW, Buma P (in press) Cellular mechanisms of neurohormone release in the snail Lymnaea stagnalis. In: Buijs RM, Pévet P, Swaab DF (eds) Progr Brain Res Vol 55, Chemical Transmission in the Brain. Elsevier Biomedical Press, Amsterdam
Roubos EW, Boer HH, Schot LPC (1981) Peptidergic neurones and the control of neuroendocrine activity in the freshwater snail Lymnaea stagnalis (L.). In: Farner DS, Lederis K (eds) Neurosecretion — Molecules, Cells, Systems. Plenum Press, New York London, pp 119–127
Roubos EW, Geraerts WPM, Boerrigter GH, Kampen GPJ van (1980) Control of the activities of the neurosecretory Light Green and Caudo-Dorsal Cells and of the endocrine Dorsal Bodies by the Lateral Lobes in the freshwater snail Lymnaea stagnalis. Gen Comp Endocrinol 40:446–454
Scharrer B (1978) Peptidergic neurones: facts and trends. Gen Comp Endocrinol 34:50–62
Scheerboom JEM (1978) The influence of food quantity and food quality on assimilation, body growth and egg production in the pond snail Lymnaea stagnalis (L.) with particular reference to the haemolymph glucose concentration. Proc Kon Ned Akad Wet C 81:184–197
Schot LPC, Boer HH (1982) Immunocytochemical demonstration of peptidergic cells in the pond snail Lymnaea stagnalis with an antiserum to the molluscan cardioactive tetrapeptide FMRF-amide. Cell Tissue Res 225:347–354
Schulz F (1938) Bau und Funktion der Sinneszellen in der Körperoberfläche von Helix pomatia. Morphol Ökol Tiere 33:555–581
Steen WJ van der, Jager JC, Tiemersma D (1973) The influence of food quantity on feeding, reproduction and growth in the pond snail Lymnaea stagnalis (L.), with some methodological comments. Proc Kon Ned Akad Wet C 76:47–60
Vlieger TA de, Roubos EW (1978) Morphological and electrophysiological aspects of the regulation of neurosecretory cell activity in the pond snail Lymnaea stagnalis. In: Gaillard PJ, Boer HH (eds) Comparative Endocrinology. Elsevier/North Holland Biomedical Press, Amsterdam New York Oxford, pp 317–322
Vlieger TA de, Kits KS, Maat A ter, Lodder JC (1980) Morphology and electrophysiology of the ovulation hormone producing neuroendocrine cells of the freshwater snail Lymnaea stagnalis (L.). J Exp Biol 84:259–271
Wendelaar Bonga SE (1970) Ultrastructure and histochemistry of neurosecretory cells and neurohaemal areas in the pond snail Lymnaea stagnalis (L.). Z Zellforsch 108:190–224
Zaitseva OV, Bocharova LS (1981) Sensory cells in the head skin of pond snails. Cell Tissue Res 220:797–807
Zylstra U (1972) Distribution and ultrastructure of epidermal sensory cells in the freshwater snails Lymnaea stagnalis and Biomphalaria pfeifferi. Neth J Zool 22:283–298
Author information
Authors and Affiliations
Additional information
The authors are greatly indebted to Prof. Dr. H.H. Boer for stimulating interest during the study and helpful comments during the preparation of the manuscript, and to Prof. Dr. J. Lever for critically reading the manuscript
Rights and permissions
About this article
Cite this article
Roubos, E.W., van der Wal-Divendal, R.M. Sensory input to growth stimulating neuroendocrine cells of Lymnaea stagnalis . Cell Tissue Res. 227, 371–386 (1982). https://doi.org/10.1007/BF00210892
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00210892