Skip to main content
SpringerLink
Log in

Acetylcholine receptors in spider peripheral mechanosensilla

  • ORIGINAL PAPER
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Peripherally located parts of spider mechanosensory neurons are modulated by several neurotransmitters released from apposed efferent fibers. Activities of acetylcholine (ACh) synthesizing enzyme choline acetyltransferase (ChAT) and ACh degrading enzyme acetylcholine esterase (AChE) were previously found in some efferent fibers. ChAT activity was also present in all the mechanosensory neurons, while AChE activity was only found in some. We show that spider mechanosensory neurons and probably some efferent neurons are immunoreactive to a monoclonal antibody against muscarinic ACh receptors (mAChRs). However, application of muscarinic agonists did not change the physiological responses or membrane potentials of neurons in the lyriform organ VS-3. Similarly, the sensitivities of the neurons of trichobothria (filiform hairs) remained unchanged after application of these agonists. Therefore, activation of mAChRs may only modulate the function of spider mechanosensory neurons indirectly, for example, by affecting the release of other transmitter(s). However, a subgroup of VS-3 neurons was inhibited by ACh, which also depolarized the membrane similar to these neurons’ responses to GABA, suggesting that ACh activates anion channels in these neurons. Interestingly, all of the neurons responding to ACh were the rapidly adapting Type A neurons that were previously shown to express AChE activity.

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

Similar content being viewed by others

References

  • Adams DJ, Gage PW, Hamill OP (1982) Inhibitory postsynaptic currents at Aplysia cholinergic synapses: effects of permeant anions and depressant drugs. Proc R Soc Lond B Biol Sci 214:335–350

    PubMed  CAS  Google Scholar 

  • Barth FG, Höller A (1999) Dynamics of arthropod filiform hairs. V. The response of spider trichobothria to natural stimuli. Philos Trans R Soc Lond B Biol Sci 354:183–192

    Article  Google Scholar 

  • Barth FG, Libera W (1970) Ein Atlas der Spaltsinnesorgane von Cupiennius salei Keys. Chelicerata (Aranea). Z Morphol Tiere 68:343–369

    Article  Google Scholar 

  • Bendat JS, Piersol AG (1980) Engineering applications of correlation and spectral analysis. Wiley, New York, NY, pp 1–302

    Google Scholar 

  • Bohnenberger J (1981) Matched transfer characteristics of single units in a compound slit sense organ. J Comp Physiol 142:391–402

    Article  Google Scholar 

  • Burrows M (1996) The neurobiology of an insect brain. Oxford University Press, Oxford, pp 1–682

    Google Scholar 

  • Caulfield MP, Birdsall NJ (1988) International union of pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol Rev 50:279–290

    Google Scholar 

  • Chernyavsky AI, Arredondo J, Wess J, Karlsson E, Grando SA (2004) Novel signaling pathways mediating reciprocal control of keratinocyte migration and wound epithelialization through M3 and M4 muscarinic receptors. J Cell Biol 166:261–272

    Article  PubMed  CAS  Google Scholar 

  • Clarac F, Cattaert D, Le Ray D (2000) Central control components of a “simple” stretch reflex. Trends Neurosci 23:199–208

    Article  PubMed  CAS  Google Scholar 

  • Cooley JW, Tukey JW (1965) An algorithm for the machine calculation of complex Fourier series. Math Comput 19:297–301

    Article  Google Scholar 

  • Dani JA (2001) Overview of nicotinic receptors and their roles in the central nervous system. Biol Psychiatry 49:166–174

    Article  PubMed  CAS  Google Scholar 

  • Fabian R, Seyfarth E-A (1997) Acetylcholine and histamine are transmitter candidates in identifiable mechanosensitive neurons of the spider Cupiennius salei: an immunocytochemical study. Cell Tissue Res 287:413–423

    Article  PubMed  CAS  Google Scholar 

  • Fabian-Fine R, Volknandt W, Seyfarth E-A (1999a) Peripheral synapses at identifiable mechanosensory neurons in the spider Cupiennius salei: synapsin-like immunoreactivity. Cell Tissue Res 295:13–19

    Article  PubMed  CAS  Google Scholar 

  • Fabian-Fine R, Höger U, Seyfarth E-A, Meinertzhagen IA (1999b) Peripheral synapses at identified mechanosensory neurons in spiders: three-dimensional reconstruction and GABA-immunoreactivity. J Neurosci 19:298–310

    PubMed  CAS  Google Scholar 

  • Fabian-Fine R, Meinertzhagen IA, Seyfarth E-A (2000) Organization of efferent peripheral synapses at mechanosensory neurons in spiders. J Comp Neurol 420:195–210

    Article  PubMed  CAS  Google Scholar 

  • Fabian-Fine R, Seyfarth E-A, Meinertzhagen IA (2002) Peripheral synaptic contacts at mechanoreceptors in arachnids and crustaceans: morphological and immunocytochemical characteristics. Microsc Res Tech 58:283–298

    Article  PubMed  Google Scholar 

  • French AS (1984) Dynamic properties of the action potential encoder in an insect mechanosensory neuron. Biophys J 46:285–290

    Article  PubMed  CAS  Google Scholar 

  • French AS, Holden AV (1971) Alias-free sampling of neuronal spike trains. Kybernetik 8:165–171

    Article  PubMed  CAS  Google Scholar 

  • French AS, Höger U, Sekizawa SI, Torkkeli PH (2001) Frequency response functions and information capacities of paired spider mechanoreceptor neurons. Biol Cybern 85:293–300

    Article  PubMed  CAS  Google Scholar 

  • Gingl E, French AS, Panek I, Meisner S, Torkkeli PH (2004) Dendritic excitability and localization of GABA-mediated inhibition in spider mechanoreceptor neurons. Eur J Neurosci 20:59–65

    Article  PubMed  Google Scholar 

  • Höger U, Torkkeli PH, Seyfarth E-A, French AS (1997) Ionic selectivity of mechanically activated channels in spider mechanoreceptor neurons. J Neurophysiol 78:2079–2085

    PubMed  Google Scholar 

  • Judge S, Leitch B (1999) Modulation of transmitter release from the locust forewing stretch receptor neuron by GABAergic interneurons activated via muscarinic receptors. J Neurobiol 40:420–431

    Article  PubMed  CAS  Google Scholar 

  • Kehoe J, McIntosh JM (1998) Two distinct nicotinic receptors, one pharmacologically similar to the vertebrate α-7-containing receptor, mediate Cl− currents in Aplysia neurons. J Neurosci 18:8198–8213

    PubMed  CAS  Google Scholar 

  • Kehoe J, Vulfius C (2000) Independence of and interactions between GABA-, glutamate-, and acetylcholine-activated Cl− conductances in Aplysia neurons. J Neurosci 20:8585–8596

    PubMed  CAS  Google Scholar 

  • Murnick JG, Dube G, Krupa B, Liu G (2002) High-resolution iontophoresis for single-synapse stimulation. J Neurosci Methods 116:65–75

    Article  PubMed  CAS  Google Scholar 

  • Onai T, FitzGerald MG, Arakawa S, Gocayne JD, Urquhart DA, Hall LM, Fraser CM, McCombie WR, Venter JC (1989) Cloning, sequence analysis and chromosome localization of a Drosophila muscarinic acetylcholine receptor. FEBS Lett 255:219–225

    Article  PubMed  CAS  Google Scholar 

  • Panek I, Torkkeli PH (2005) Inhibitory glutamate receptors in spider peripheral mechanosensory neurons. Eur J Neurosci 22(3):647–657

    Article  PubMed  Google Scholar 

  • Panek I, French AS, Seyfarth E-A, Sekizawa SI, Torkkeli PH (2002) Peripheral GABAergic inhibition of spider mechanosensory afferents. Eur J Neurosci 16:96–104

    Article  PubMed  Google Scholar 

  • Panek I, Meisner S, Torkkeli PH (2003) The distribution and function of GABAB receptors in spider peripheral mechanosensilla. J Neurophysiol 90:2571–2580

    Article  PubMed  CAS  Google Scholar 

  • Putrenko I, Zakikhani M, Dent JA (2005) A family of acetylcholine-gated chloride channel subunits in Caenorhabditis elegans. J Biol Chem 280:6392–6398

    Article  PubMed  CAS  Google Scholar 

  • Rudomin P, Romo R, Mendell LM (1998) Presynaptic inhibition and neural control. Oxford University press, New York, NY, pp 449

    Google Scholar 

  • Sekizawa SI, French AS, Höger U, Torkkeli PH (1999) Voltage-activated potassium outward currents in two types of spider mechanoreceptor neurons. J Neurophysiol 81:2937–2944

    PubMed  CAS  Google Scholar 

  • Seyfarth E-A, French AS (1994) Intracellular characterization of identified sensory cells in a new spider mechanoreceptor preparation. J Neurophysiol 71:1422–1427

    PubMed  CAS  Google Scholar 

  • Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Urbana, IL, pp 1–117

    Google Scholar 

  • Shapiro RA, Wakimoto BT, Subers EM, Nathanson NM (1989) Characterization and functional expression in mammalian cells of genomic and cDNA clones encoding a Drosophila muscarinic acetylcholine receptor. Proc Natl Acad Sci USA 86:9039–9043

    Article  PubMed  CAS  Google Scholar 

  • Soreq H, Seidman S (2001) Acetylcholinesterase—new roles for an old actor. Nat Rev Neurosci 2:294–302

    Article  PubMed  CAS  Google Scholar 

  • Thorson J, Biederman-Thorson M (1974) Distributed relaxation processes in sensory adaptation. Science 183:161–172

    Article  PubMed  CAS  Google Scholar 

  • Torkkeli PH, Widmer A, Meisner S (2005) Expression of muscarinic acetylcholine receptors and choline acetyltransferase enzyme in cultured antennal sensory neurons and non-neural cells of the developing moth Manduca sexta. J Neurobiol 62:316–329

    Article  PubMed  CAS  Google Scholar 

  • Trimmer BA (1995) Current excitement from insect muscarinic receptors. Trends Neurosci 18:104–1115

    Article  PubMed  CAS  Google Scholar 

  • Trimmer BA, Weeks JC (1993) Muscarinic acetylcholine receptors modulate the excitability of an identified insect motoneuron. J Neurophysiol 69:1821–1836

    PubMed  CAS  Google Scholar 

  • Van der Zee EA, Luiten PG (1999) Muscarinic acetylcholine receptors in the hippocampus, neocortex and amygdala: a review of immunocytochemical localization in relation to learning and memory. Prog Neurobiol 58:409–471

    Article  PubMed  Google Scholar 

  • Widmer A, Höger U, Meisner S, French AS, Torkkeli PH (2005) Spider peripheral mechanosensory neurons are directly innervated and modulated by octopaminergic efferents. J Neurosci 25:1588–1598

    Article  PubMed  CAS  Google Scholar 

  • Zufall F, Franke Ch, Hatt H (1988) Acetylcholine activates a chloride channel as well as glutamate and GABA. J Comp Physiol [A] 163:609–620

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the Canadian Institutes of Health Research to ASF and PHT and the Natural Sciences and Engineering Research Council of Canada, the Canadian Foundation for Innovation and the Nova Scotia Research and Innovation Trust to PHT. Experiments complied with the “Principles of animal care”, publication No. 86-23, revised 1985 of the National Institute of Health, and they followed protocols approved by the Dalhousie University Committee on Laboratory Animals (I4-28).

Author information

Author notes

  1. Alexandre Widmer

    Present address: Institute of Molecular Biotechnology, Dr. Bohr-Gasse 3-5, 1030, Vienna, Austria

Authors and Affiliations

  1. Department of Physiology and Biophysics, Dalhousie University, B3H 1X5, Halifax, Nova Scotia, Canada

    Alexandre Widmer, Izabela Panek, Ulli Höger, Shannon Meisner, Andrew S. French & Päivi H. Torkkeli

  2. Department of Biophysics, Institute of General and Molecular Biology, N. Copernicus University, 87-100, Torun, Poland

    Izabela Panek

Authors
  1. Alexandre Widmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Izabela Panek
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ulli Höger
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shannon Meisner
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrew S. French
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Päivi H. Torkkeli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Päivi H. Torkkeli.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Widmer, A., Panek, I., Höger, U. et al. Acetylcholine receptors in spider peripheral mechanosensilla. J Comp Physiol A 192, 85–95 (2006). https://doi.org/10.1007/s00359-005-0054-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-005-0054-9

Keywords

Search

Navigation