Skip to main content
SpringerLink
Log in

Neuronal background of activation of estivated snails, with special attention to the monoaminergic system: a biochemical, physiological, and neuroanatomical study

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Osmotic stimulation activates both estivated and inactivated specimens of Helix pomatia and increases their central arousal. High-pressure liquid chromatography has shown that, during activation, the level of both serotonin and dopamine decreases in the central nervous system (CNS) but increases in the foot and heart, organs that are involved in the eversion of the body. In isolated CNS from activated animals, the firing frequency of the heart-modulator serotonergic (RPas) neurons is significantly higher than that in the CNS of estivated or inactivated animals. These neurons innervate both the heart and the anterior aorta. In semi-intact preparations, distilled water (an osmotic stimulus) applied to the mantle collar increases their firing frequency, whereas tactile stimulation evokes their inhibition. Extracellularly applied monoamines mimic the effect of peripheral stimuli: serotonin (0.1–10 μM) increases the activity of the RPas neurons, whereas dopamine (0.1–10 μM) inhibits their activity. Tyrosine-hydroxylase immunocytochemistry and retrograde neurobiotin tracing have revealed similar bipolar receptor cells in the mantle collar and tail, organs that are exposed to environmental stimuli in estivated animals. Serotonin immunocytochemistry carried out on the same tissues does not visualize receptor cells but labels a dense network of fibers that appear to innervate neurobiotin-labeled receptor cells. The combination of neurobiotin-labeling of RPas neurons and immunolabeling suggests that RPas neurons receive direct dopaminergic inputs from receptor cells and serotonergic inputs from central serotonergic neurons, indicating that central serotonergic neurons are interconnected. Thus, the RPas neurons may belong to neuronal elements of the arousal system.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Balaban PM, Zakharov JS, Matz VN (1985) Method of vital selective staining of serotonergic nerve cells by 5,7-dihyroxytryptamine (in Russian). Dk A N SSSR 283:735–738

    Google Scholar 

  • Bullock TH, Horridge GA (1965) Structure and function in the nervous system of invertebrates. Freeman, San Francisco

    Google Scholar 

  • Chase R (2002) Behavior and its neural control in gastropod molluscs. Oxford University Press, Oxford

    Google Scholar 

  • Church PJ, Whim MD, Lloyd PE (1993) Modulation of neuromuscular-transmission by conventional and peptide transmitters released from excitatory and inhibitory motor-neurons in Aplysia. J Neurosci 13:2790–2800

    PubMed  CAS  Google Scholar 

  • Dale B (1974) Extrusion, retraction and respiratory movements in Helix pomatia in relation to distribution and circulation of the blood. J Zool Lond 173:427–439

    Article  Google Scholar 

  • Elliott CJ, Susswein AJ (2002) Comparative neuroethology of feeding control in molluscs. J Exp Biol 205:877–896

    PubMed  CAS  Google Scholar 

  • Fox LE, Lloyd PE (1998) Serotonergic neurons differentially modulate the efficacy of two motor neurons innervating the same muscle fibers in Aplysia. J Neurophysiol 80:647–655

    PubMed  CAS  Google Scholar 

  • Görcs T, Antal M, Olah E, Székely G (1979) An improved cobalt-labeling technique with complex compounds. Acta Biol Hung 30:79–86

    Google Scholar 

  • Hernádi L (1991) A new double labeling technique of the serotonergic neurons in wholemount CNS preparations of the snail Helix pomatia. Acta Biol Hung 42:417–423

    PubMed  Google Scholar 

  • Hernádi L, Elekes K (1999) Topographic organization of serotonergic and dopaminergic neurons in the cerebral ganglia and their peripheral projection patterns in the head areas of the snail Helix pomatia. J Comp Neurol 411:274–287

    Article  PubMed  Google Scholar 

  • Hernádi L, Elekes K, S-Rózsa K (1989) Distribution of serotonin-containing neurons in the central nervous-system of the snail Helix pomatia—comparison of immunocytochemical and 5,6-dihydroxytryptamine labeling. Cell Tissue Res 257:313–323

    Article  Google Scholar 

  • Hernádi L, Juhos S, Elekes K (1993) Distribution of tyrosine-hydroxylase-immunoreactive and dopamine-immunoreactive neurons in the central-nervous-system of the snail Helix pomatia. Cell Tissue Res 27:503–513

    Article  Google Scholar 

  • Hernádi L, Vehovszky A, Hiripi L, Győri J, Walker RJ, Elekes K (2005) Neuroanatomical, immunocytochemical, and physiological studies of the pharyngeal retractor muscle and its putative regulatory neurons playing a role in withdrawal and feeding in the snail, Helix pomatia. Cell Tissue Res 321:257–271

    Article  PubMed  CAS  Google Scholar 

  • Hsu SM, Raine L, Fanger H (1981) The use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques. A comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577–580

    PubMed  CAS  Google Scholar 

  • Kemenes G, Zakharov IS, Vehovszky A, S-Rozsa K (1993) Neurophysiological correlates of tactile stimulus-induced whole-body eversion, a novel type of behavior in the snail Helix pomatia L. Brain Res 612:16–27

    Article  PubMed  CAS  Google Scholar 

  • Kiss T, S-Rózsa K (1972) Effect of biologically active substances on the spontaneous electrical activity of the heart muscle cells of Helix pomatia L. Annal Biol Tihany 39:29–38

    CAS  Google Scholar 

  • Kume K, Kume S, Park SK, Hirsh J, Jackson FR (2005) Dopamine is a regulator of arousal in the fruit fly. Neuroscience 25:7377–7384

    Article  PubMed  CAS  Google Scholar 

  • Kupfermann I, Weiss KR (1981) Tail pinch and handling facilitate feeding behavior in Aplysia. Behav Biol 32:126–132

    Article  Google Scholar 

  • Machin J (1975) Water relationships. In: Fretter V, Peake J (ed) Pulmonates, vol 1. Academic Press, London, pp 105–164

    Google Scholar 

  • Malyshev AY, Balaban PM (2002) Identification of mechanoafferent neurons in terrestrial snails: response properties and synaptic connections. J Neurophysiol 87:2364–2371

    PubMed  Google Scholar 

  • Marder E, Bucher D (2001) Central pattern generators and the control of rhythmic movements. Curr Biol 11:R986–R996

    Article  PubMed  CAS  Google Scholar 

  • Marinesco S, Carew TJ (2002) Serotonin release evoked by tail nerve stimulation in the CNS of Aplysia: characterization and relationship to heterosynaptic plasticity. J Neurosci 22:2299–2312

    PubMed  CAS  Google Scholar 

  • Marinesco S, Kolkman KE, Carew TJ (2004a) Serotonergic modulation in aplysia. I. Distributed serotonergic network persistently activated by sensitizing stimuli.J Neurophysiol 92:2468–2486

    Article  PubMed  CAS  Google Scholar 

  • Marinesco S, Wickremasinghe N, Kolkman KE, Carew TJ (2004b) Serotonergic modulation in aplysia. II. Cellular and behavioral consequences of increased serotonergic tone.J Neurophysiol 92:2487–2496

    Article  PubMed  CAS  Google Scholar 

  • Palovcik RA, Basberg BA, Ram JL (1982) Behavioral state changes induced in Pleurobranchaea and Aplysia by serotonin. Behav Neural Biol 35:383–394

    Article  PubMed  CAS  Google Scholar 

  • Quicke DL, Brace RC (1979) Differential staining of cobalt and nickel-filled neurones using rubeanic acid. J Microsc 115:161–163

    PubMed  CAS  Google Scholar 

  • Ruben P, Lukowiak K (1983) Modulation of the Aplysia gill withdrawal reflex by dopamine. J Neurobiol 14:271–284

    Article  PubMed  CAS  Google Scholar 

  • Schmidt-Nielsen K, Taylor CR, Shkolnik A (1971) Desert snails: problems of heat, water and food. J Exp Biol 55:385–398

    PubMed  CAS  Google Scholar 

  • Siegel JM (2004) The neurotransmitters of sleep. J Clin Psychiatry 65:4–7

    Article  PubMed  CAS  Google Scholar 

  • Sommerville BA (1973a) The circulatory physiology of Helix pomatia. I. Observations on the mechanism by which Helix emerges from its shell and on the effects of body movement on cardiac function. J Exp Biol 59:275–282

    PubMed  CAS  Google Scholar 

  • Sommerville BA (1973b) The circulatory physiology of Helix pomatia. III. The hydrostatic pressure changes in the circulatory system of living Helix. J Exp Biol 59:291–303

    PubMed  CAS  Google Scholar 

  • S-Rózsa K, Kiss T (1976) Role of cyclic nucleotides in effect of transmitters on heart of Helix pomatia L. Comp Biochem Physiol [C] 53:13–16

    Article  Google Scholar 

  • S-Rózsa K, Zhuravlev V (1981) Central regulation and coordination of the activity of cardio-renal system and pneumostoma in the subesophageal ganglia of Helix pomatia L. Comp Biochem Physiol [A] 69:85–98

    Article  Google Scholar 

  • S-Rózsa K, Hernádi L, Kemenes G (1986) Selective in vivo labeling of serotonergic neurones by 5,6-dihydroxytryptamine in the snail Helix pomatia. Comp Biochem Physiol [C] 85:419–425

    Article  Google Scholar 

  • Strecker RE, Jacobs BL (1985) Substantia nigra dopaminergic unit activity in behaving cats: effect of arousal on spontaneous discharge and sensory evoked activity. Brain Res 361:339–350

    Article  PubMed  CAS  Google Scholar 

  • Swann JW, Sinback CN, Pierson MG, Carpenter DO (1982) Dopamine produces muscle contractions and modulates motoneuron-induced contractions in Aplysia gill. Cell Mol Neurobiol 2:291–308

    Article  PubMed  CAS  Google Scholar 

  • Vehovszky A, Kemenes G, S-Rozsa K (1989a) Central and peripheral connections of an identified pedal neuron modifying pneumostome movements in Helix pomatia. Comp Biochem Physiol [A] 94:735–741

    Article  Google Scholar 

  • Vehovszky A, Kemenes G, S-Rozsa K (1989b) Mono-synaptic connections between serotonin-containing neurons labeled by 5,6-dihydroxytryptamine-induced pigmentation in the snail Helix pomatia L. Brain Res 484:404–407

    Article  CAS  Google Scholar 

  • Vehovszky A, Kemenes G, S-Rozsa K (1992) The monosynaptic connections between the serotonin-containing lp3 and rpas neurons in Helix are serotonergic. J Exp Biol 173:109–122

    Google Scholar 

  • Weiss KR, Cohen JL, Kupfermann I (1978) Modulatory control of buccal musculature by a serotonergic neuron (metacerebral cell) in Aplysia. J Neurophysiol 41:181–203

    PubMed  CAS  Google Scholar 

  • Weiss KR, Koch UT, Koester J, Mandelbaum DE, Kupfermann I (1981) Neural and molecular mechanisms of food induced arousel in Aplysia californica. In: Salánki J (ed) Advances in physiological sciences, neurobiology of invertebrates. Pergamon, Oxford, pp 305–344

    Google Scholar 

  • Weiss KR, Koch UT, Koester J, Rosen SC, Kupfermann I (1982) The role of arousal in modulating feeding behavior of Aplysia: neural and behavioral studies. In: Hoebel BG, Novin D (eds) The neural basis of feeding and reward. Haer Institute, Brunswick, pp 25–57

    Google Scholar 

  • Weiss S, Goldberg JI, Lukowiak K, Drummond GI (1985) Effect of dopamine and serotonin on cyclic-AMP and contractility in the gill of Aplysia californica. J Comp Physiol [B] 156:57–65

    CAS  Google Scholar 

Download references

Acknowledgement

The authors thank Professor Robert J. Walker for reading the manuscript.

Author information

Authors and Affiliations

  1. Department of Experimental Zoology, Balaton Limnological Research Institute, Hungarian Academy of Sciences, P.O. Box 35, Tihany, 8237, Hungary

    L. Hernádi, Á. Vehovszky, J. Győri & L. Hiripi

Authors
  1. L. Hernádi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Á. Vehovszky
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Győri
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L. Hiripi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. Hernádi.

Additional information

This work was supported by Hungarian OTKA grants T037389, T046580, T037505, and K63451.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hernádi, L., Vehovszky, Á., Győri, J. et al. Neuronal background of activation of estivated snails, with special attention to the monoaminergic system: a biochemical, physiological, and neuroanatomical study. Cell Tissue Res 331, 539–553 (2008). https://doi.org/10.1007/s00441-007-0522-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-007-0522-3

Keywords

Search

Navigation