Skip to main content
SpringerLink
Log in

Primary sensory neurons containing command neuron peptide constitute a morphologically distinct class of sensory neurons in the terrestrial snail

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

Abstract

In the central nervous system of the terrestrial snail Helix, the gene HCS2, which encodes several neuropeptides of the CNP (command neuron peptide) family, is mostly expressed in cells related to withdrawal behavior. In the present work, we demonstrate that a small percentage (0.1%) of the sensory cells, located in the sensory pad and in the surrounding epithelial region (“collar”) of the anterior and posterior tentacles, is immunoreactive to antisera raised against the neuropeptides CNP2 and CNP4, encoded by the HCS2 gene. No CNP-like-immunoreactive neurons have been detected among the tentacular ganglionic interneurons. The CNP-like-immunoreactive fiber bundles enter the cerebral ganglia within the nerves of the tentacles (tentacular nerve and medial lip nerve) and innervate the metacerebral lobe, viz., the integrative brain region well-known as the target area for many cerebral ganglia nerves. The procerebral lobe, which is involved in the processing of olfactory information, is not CNP-immunoreactive. Our data suggest that the sensory cells, which contain the CNP neuropeptides, belong to a class of sensory neurons with a specific function, presumably involved in the withdrawal behavior of the snail.

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

Similar content being viewed by others

References

  • Balaban PM (2002) Cellular mechanisms of behavioral plasticity in terrestrial snail. Neurosci Biobehav Rev 26:597–630

    Article  PubMed  CAS  Google Scholar 

  • Balaban PM, Poteryaev DA, Zakharov IS, Uvarov P, Malyshev AY, Belyavsky AV (2001) Up- and down-regulation of Helix command-specific 2 (HCS2) gene expression in the nervous system of terrestrial snail Helix lucorum. Neuroscience 103:551–559

    Article  PubMed  CAS  Google Scholar 

  • Bogdanov YuD, Balaban PM, Poteryaev DA, Zakharov IS, Belyavsky AV (1998) Putative neuropeptides and an EF-hand motif region are encoded by a novel gene expressed in the four giant interneurons of the terrestrial snail. Neuroscience 85:637–647

    Article  PubMed  CAS  Google Scholar 

  • Bullock TH, Horridge GA (1965) Structure and function in the nervous systems of invertebrates, vol 2. Freeman, San Francisco

    Google Scholar 

  • Cardot J, Fellmann D (1988) Apparent immunoreactivity of CRF in the tentacles of the mollusk Helix pomatia. Gen Comp Endocrinol 77:43–51

    Article  Google Scholar 

  • Chase R (1981) Electrical responses of snail tentacle ganglion to stimulation of the epithelium with wind and odors. Comp Biochem Physiol [A] 70:149–155

    Article  Google Scholar 

  • Chase R (1985) Responses to odors mapped in snail tentacle and brain by [14C]-2-deoxyglucose autoradiography. J Neurosci 5:2930–2939

    PubMed  CAS  Google Scholar 

  • Chase R (1986) Lessons from snail tentacles. Chem Senses 11:411–426

    Article  Google Scholar 

  • Chase R, Croll RP (1981) Tentacular function in snail olfactory orientation. J Comp Physiol 143:357–362

    Article  Google Scholar 

  • Chase R, Kamil R (1983) Neuronal elements in snail tentacles as revealed by horseradish peroxidase backfilling. J Neurobiol 14:29–42

    Article  PubMed  CAS  Google Scholar 

  • Chase R, Rieling J (1986) Autoradiographic evidence for receptor cell renewal in the olfactory epithelium of a snail. Brain Res 384:232–239

    Article  PubMed  CAS  Google Scholar 

  • Chase R, Tolloczko B (1986) Synaptic glomeruli in the olfactory system of a snail, Achatina fulica. Cell Tissue Res 246:567–571

    Article  Google Scholar 

  • Chase R, Tolloczko B (1989) Interganglionic dendrites constitute an output pathway from the procerebrum of the snail Achatina fulica. J Comp Neurol 283:143–152

    Article  PubMed  CAS  Google Scholar 

  • Chase R, Tolloczko B (1993) Tracing neural pathways in snail olfaction: from the tip of the tentacles to the brain and beyond. Microsc Res Tech 24:214–230

    Article  PubMed  CAS  Google Scholar 

  • Elekes K, Nässel DR (1990) Distribution of FMRFamide-like immunoreactive neurons in the central nervous system of the snail Helix pomatia. Cell Tissue Res 262:177–190

    Article  CAS  Google Scholar 

  • Gelperin A (1999) Oscillatory dynamics and information processing in olfactory systems. J Exp Biol 202:1855–1864

    PubMed  Google Scholar 

  • Gelperin A, Tank DW, Tesauro G (1989) Olfactory processing and associative memory: cellular and modelling studies. In: Bryne JW, Berry WO (eds) Neural models of plasticity: theoretical and empirical approaches. Elsevier, New York, pp 133–159

    Google Scholar 

  • Gervais R, Kleinfeld D, Delaney KR, Gelperin A (1996) Central and reflex neuronal responses elicited by odor in a terrestrial mollusk. J Neurophysiol 76:1327–1339

    PubMed  CAS  Google Scholar 

  • Hernadi L, Benedeczky I (1994) Ultrastructural differentiation and the renewal of the receptor cells in the sensory epithelia of the lips and the anterior tentacles of the snail Helix pomatia. Neurobiology 2:283–300

    PubMed  CAS  Google Scholar 

  • Hernadi 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  CAS  Google Scholar 

  • Ierusalimsky VN, Balaban PM (2003) Novel family of neuropeptides: immunoreactive neurons in several invertebrate species. VI IBRO Congress, Prague, Abstracts, p 2380

  • Ierusalimsky VN, Balaban PM (2006) Immunoreactivity to molluskan neuropeptides in the central and stomatogastric nervous systems of the earthworm, Lumbricus terrestris L. Cell Tissue Res 325:555–565

    Article  PubMed  CAS  Google Scholar 

  • Ierusalimsky VN, Boguslavsky DV, Belyavsky AV, Balaban PM (2003) Helix peptide immunoreactivity pattern in the nervous system of juvenile Aplysia. Mol Brain Res 120:84–89

    Article  PubMed  CAS  Google Scholar 

  • Ito I, Nakamura H, Kimura T, Suzuki H, Sekiguchi T, Kawabata K, Ito E (2000) Neuronal components of the superior and inferior tentacles in the terrestrial slug, Limax marginatus. Neurosci Res 37:191–200

    Article  PubMed  CAS  Google Scholar 

  • Kaufmann W, Kerschbaum HH, Hauser-Kronberger C, Hacker GW, Hermann A (1995) Distribution and seasonal variation of vasoactive intestinal (VIP)-like peptides in the nervous system of Helix pomatia. Brain Res 695:125–136

    Article  PubMed  CAS  Google Scholar 

  • Kimura T, Suzuki H, Kono E, Sekiguchi T (1998) Mapping of interneurons that contribute to food aversive conditioning in the slug brain. Learn Mem 4:376–388

    Article  PubMed  CAS  Google Scholar 

  • Lane NJ (1962) Neurosecretory cells in the optic tentacles of certain pulmonates. Q J Microsc Sci 103:211–226

    Google Scholar 

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

    PubMed  Google Scholar 

  • Marchand CR, Dubois MP (1986) Immunocytochemical detection of substances related to methionine enkephalin in the tentacles and foot of the snail (Helix aspersa). C R Seances Soc Biol Fil 180:184–189

    PubMed  CAS  Google Scholar 

  • Nikitin ES, Balaban PM (2001) Optical recording of responses to odor in olfactory structures of the nervous system in the terrestrial mollusk Helix. Neurosci Behav Physiol 31:21–30

    Article  PubMed  CAS  Google Scholar 

  • Nikitin ES, Zakharov IS, Samarova EI, Kemenes G, Balaban PM (2005) Fine tuning of olfactory orientation behaviour by the interaction of oscillatory and single neuronal activity. Eur J Neurosci 22:2833–2844

    Article  PubMed  Google Scholar 

  • Prescott SA, Chase R (1999) Sites of plasticity in the neural circuit mediating tentacle withdrawal in the snail Helix aspersa: implications for behavioral change and learning kinetics. Learn Mem 6:363–380

    PubMed  CAS  Google Scholar 

  • Prescott SA, Gill N, Chase R (1997) Neural circuit mediating tentacle withdrawal in Helix aspersa, with specific reference to the competence of the motor neuron C3. J Neurophysiol 78:2951–2965

    PubMed  CAS  Google Scholar 

  • Ratte S, Chase R (1997) Morphology of interneurons in the procerebrum of the snail Helix aspersa. J Comp Neurol 384:359–372

    Article  PubMed  CAS  Google Scholar 

  • Rogers DC (1969) The fine structure of the collar cells in the optic tentacles of Helix aspersa. Z Zellforsch Mikrosk Anat 102:113–128

    Article  PubMed  CAS  Google Scholar 

  • Rogers DC (1971) The fine structure of sensory neurons and their processes in the optic tentacles of Helix aspersa. Z Mikrosk Anat Forsch 84:52–64

    PubMed  CAS  Google Scholar 

  • Suzuki H, Kimura T, Sekiguchi T, Mizukami A (1997) FMRF amide-like-immunoreactive primary sensory neurons in the olfactory system of the terrestrial mollusc, Limax marginatus. Cell Tissue Res 289:339–345

    Article  PubMed  CAS  Google Scholar 

  • Wright BR (1974) Sensory structure of the tentacles of the slug, Arion ater (Pulmonata, Mollusca). 1. Ultrastructure of the distal epithelium, receptor cells and tentacular ganglion. Cell Tissue Res 151:229–244

    Article  PubMed  CAS  Google Scholar 

  • Zakharov IS (1994) Avoidance behavior of the snail. Neurosci Behav Physiol 24:63–69

    Article  PubMed  CAS  Google Scholar 

  • Zs-Nagy I, Sakharov DA (1970) The fine structure of the procerebrum of pulmonate molluscs, Helix and Limax. Tissue Cell 2:399–411

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, 5A Butlerova Street, Moscow, 117485, Russia

    Victor N. Ierusalimsky & Pavel M. Balaban

Authors
  1. Victor N. Ierusalimsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pavel M. Balaban
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Victor N. Ierusalimsky.

Additional information

This work was supported by INTAS (grant 01-2117) and the Russian Foundation for Basic Research (grants 05-04-48724 and 06-04-48294).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ierusalimsky, V.N., Balaban, P.M. Primary sensory neurons containing command neuron peptide constitute a morphologically distinct class of sensory neurons in the terrestrial snail. Cell Tissue Res 330, 169–177 (2007). https://doi.org/10.1007/s00441-007-0447-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-007-0447-x

Keywords

Search

Navigation