Skip to main content
SpringerLink
Log in

Computational Study of Enhanced Excitability in Hermissenda: Membrane Conductances Modulated by 5-HT

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

Serotonin (5-HT) applied to the exposed but otherwise intact nervous system results in enhanced excitability of Hermissenda type-B photoreceptors. Several ion currents in the type-B photoreceptors are modulated by 5-HT, including the A-type K+ current (IK,A), sustained Ca2+ current (ICa,S), Ca-dependent K+ current (IK,Ca), and a hyperpolarization-activated inward rectifier current (Ih). In this study, we developed a computational model that reproduces physiological characteristics of type B photoreceptors, e.g. resting membrane potential, dark-adapted spike activity, spike width, and the amplitude difference between somatic and axonal spikes. We then used the model to investigate the contribution of different ion currents modulated by 5-HT to the magnitudes of enhanced excitability produced by 5-HT. Ion currents were systematically varied within limits observed experimentally, both individually and in combinations. A reduction of IK,A or IK,Ca, or an increase in Ih enhanced excitability by 20–50%. Decreasing ICa,S produced a dramatic decrease in excitability. Reductions of IK,V produced only minimal increases in excitability, suggesting that IK,V probably plays a minor role in 5-HT induced enhanced excitability. Combinations of changes in IK,A, IK,Ca, Ih and ICa,S produced increases in excitability comparable to experimental observations. After 5-HT application, the cell's depolarization force is shifted from the Ih–ICa,S combination to predominantly Ih.

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

Similar content being viewed by others

References

  • Acosta-Urquidi J, Crow T (1993) Differential modulation of voltagedependent currents in Hermissenda typeBphotoreceptors by serotonin. J. Neurophysiol. 70: 541-548.

    PubMed  Google Scholar 

  • Acosta-Urquidi J, Crow T (1995) Characterization of voltagedependent currents in Hermissenda type B photoreceptors. J. Neurosci. 15: 319-332.

    PubMed  Google Scholar 

  • Alkon DL, Fuortes MGF (1972) Responses of photoreceptors in Hermissenda. J. Gen. Physiol. 60: 631-649.

    Article  PubMed  Google Scholar 

  • Baxter DA, Cai Y, Brembs B, Byrne JH (2000) Simulating physiological and morphological properties of neurons with SNNAP (Simulator for Neural Networks and Action Potentials). Soc. Neurosci. Abstr. 26: 45.

    Google Scholar 

  • Blackwell KT (1999) Dynamics of light-induced current in Hermissenda. Neurocomputing 26/27: 61-67.

    Article  Google Scholar 

  • Blackwell KT (2000) Evidence for a distinct light-induced calciumdependent potassium current in Hermissenda Crassicornis. J. Comput. Neurosci. 9: 149-170.

    Article  PubMed  Google Scholar 

  • Cai Y, Baxter DA, Crow T (2000) Computational model of Hermissenda type-B photoreceptors. Soc. Neurosci. Abstr. 26: 2032.

    Google Scholar 

  • Cai Y, Baxter DA, Crow T (2001) Computational model of Hermissenda type-B photoreceptors. I: Ionic currents underlying changes in excitability produced by one-trial conditioning. Soc. Neurosci. Abstr. 27: 2532.

    Google Scholar 

  • Connor JA, Stevens CF (1971) Prediction of repetitive firing behaviour from voltage clamp data on an isolated neurone soma. J. Physiol. 213: 31-53.

    PubMed  Google Scholar 

  • Crow T (1985) Conditioned modification of phototactic behavior in Hermissenda. II. Differential adaptation of B-photoreceptors. J. Neurosci. 5: 215-223.

    PubMed  Google Scholar 

  • Crow T, Bridge MS (1985) Serotonin modulates photoresponses in Hermissenda type-B photoreceptors. Neurosci. Lett. 60: 83-88.

    Article  PubMed  Google Scholar 

  • Crow T, Forrester J (1986) Light paired with serotonin mimics the effect of conditioning on phototactic behavior of Hermissenda. Proceedings of the National Academy of Sciences of USA 83: 7975-7978.

    Google Scholar 

  • Crow T, Forrester J (1991) Light paied with serotonin in vivo produces both short-and long-term enhancement of generator potentials of identified B-photoreceptors in Hermissenda. J. Neurosci. 11: 608-617.

    PubMed  Google Scholar 

  • Crow T, Heldman E, Hacopian V, Enos R, Alkon DL (1979) Ultrastructure of photoreceptors in the eye of Hermissenda labelled with intracellular injections of horseradish peroxidase. J. Neurocytol. 8: 181-195.

    PubMed  Google Scholar 

  • Crow T, Siddiqi V (1997) Time-dependent changes in excitability after one-trial conditioning of Hermissenda. J. Neurophysiol. 78: 3460-3464.

    PubMed  Google Scholar 

  • Crow T, Xue-Bian J-J, Siddiqi V (1999) Protein synthesis-dependent and mRNA synthesis-independent intermediate phase of memory in Hermissenda. J. Neurophysiol. 82: 495-500.

    PubMed  Google Scholar 

  • Eakin RM, Westfall JA, Dennis MJ (1967) Fine structure of the eye of a Nudibranch Mollusc, Hermissenda crassicornis. J. Cell Sci. 2: 349-358.

    PubMed  Google Scholar 

  • Flynn M, Cai Y, Baxter DA, Crow T (2003) A computational study of the role of spike broadening in synaptic facilitation of Hermissenda. J. Comput. Neurosci. 15: 29-41.

    Article  PubMed  Google Scholar 

  • Fost JW, Clark GA (1996) Modeling Hermissenda: I. Differential contribution of IA and IC to type-B cell plasticity. J. Comput. Neurosci. 3: 137-153.

    PubMed  Google Scholar 

  • Gandhi CC, Matzel LD (2000) Modulation of presynaptic action potential kinetics underlies synaptic facilitation of type B photoreceptors after associative conditioning in Hermissenda. J. Neurosci. 20: 2022-2035.

    Google Scholar 

  • Hayes RD, Byrne JH, Baxter DA (2003) Neurosimulation: Tools and resources. In: Arbib MA ed. The Handbook of Brain Theory and Neural Networks. Second Edition, MIT Press, Cmbridge, pp. 776-780.

    Google Scholar 

  • Goh Y, Alkon DL (1984) Sensory, interneuronal, and motor interactions within Hermissenda visual pathway. J. Neurophysiol. 52: 156-169.

    PubMed  Google Scholar 

  • Ito E, Oka K, Collin C, Schreurs BG, Sakakibara M, Alkon DL (1994) Intracellular calcium signals are enhanced for days after Pavlovian conditioning. J. Neurochem. 62: 1337-1344.

    PubMed  Google Scholar 

  • Jack JJB, Noble D, Tsien RW (1983) Electrical Current Flow in Excitable Cells. Oxford, Oxford.

    Google Scholar 

  • Koch C (1999) Biophysics of Computation: Information Processing in Single Neurons. Oxford, New York.

    Google Scholar 

  • Mainen ZF, Sejnowski TJ (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382: 363-366.

    Article  PubMed  Google Scholar 

  • Major G, Larkman AU, Jonas P, Sakmann B, Jack JJ (1994) Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices. J. Neurosci. 14: 4613-4638.

    PubMed  Google Scholar 

  • McEwan JR, Farnsworth PN (1987) Regional resistivity variations in lens homogenates. Exp. Eye Res. 44: 567-576.

    PubMed  Google Scholar 

  • Muzzio IA, Talk AC, Matzel LD (1998) Intracellular Ca2+ and adaptation of voltage responses to light in Hermissenda photoceceptors. Neuroreport 9: 1625-1631.

    PubMed  Google Scholar 

  • Richieri GV, Mel HC (1986) Membrane and cytoplasmic resistivity properties of normal and sivkle red blood cells. Cell Biophysics. 8: 243-258.

    PubMed  Google Scholar 

  • Rush ME, Rinzel J (1995) The potassium A-current, low firing rates and rebound excitation in Hodgkin-Huxley models. Bull. Math. Biol. 57: 899-929.

    PubMed  Google Scholar 

  • Sahley CL, Crow T (1998) Invertebrate learning: Current perspectives. In: JL Martinez Jr. and RP Kesnok, eds. Neurobiology of Learning and Memory. Academic, New York, pp. 177-209.

    Google Scholar 

  • Sakakibara M, Ikeno H, Usui S, Collin C, Alkon DL (1993) Reconstruction of ionic currents in a Molluscan photoreceptor. Biophys. J. 65: 519-527.

    PubMed  Google Scholar 

  • Senft SL, Allen RD, Crow T, Alkon DL (1982). Optical sectioning of HRP-stained molluscan neurons. J. Neurosci. Meth. 5: 153-159.

    Article  Google Scholar 

  • Stensaas LJ, Stensaas SS, Trujillo-Cenoz O (1969) Some morphological aspects of the visual system of Hermissenda crassicornis (Mollusca: Nudibranchia). J. Ultra. Res. 27: 510-532.

    Google Scholar 

  • Thurbon D, Field A, Redman S (1994) Electrotonic profiles of interneurons in stratum pyramidale of the CA1 region of rat hippocampus. J. Neurophysiol. 71: 1948-1958.

    PubMed  Google Scholar 

  • Yamoah EN, Crow T (1994) Two components of calcium currents in the soma of photoreceptors of Hermissenda. J. Neurophysiol. 72: 1327-1336.

    PubMed  Google Scholar 

  • Yamoah EN, Crow T (1995) Evidence for a contribution of ICa to serotonergic modulation of IK, Ca in Hermissenda photoreceptors. J. Neurophysiol. 74: 1349-1354.

    PubMed  Google Scholar 

  • Yamoah EN, Crow T (1996) Protein kinase and G-protein regulation of Ca2+ currents in Hermissenda photoreceptors by 5-HT and GABA. J. Neurosci. 16: 4799-4809.

    PubMed  Google Scholar 

  • Yamoah EN, Matzel L, Crow T (1998) Expression of different types of inward rectifier currents confers specificity of light and dark responses in type A and B photoreceptors of Hermissenda. J. Neurosci. 18: 6501-6511.

    PubMed  Google Scholar 

  • Ziv I, Baxter DA, Byrne JH (1994) Simulator for neural networks and action potentials: Description and application. J. Neurophysiol. 71: 294-308.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurobiology and Anatomy, University of Texas at Houston Medical School, Houston, Texas, 77030, USA

    Yidao Cai, Douglas A. Baxter & Terry Crow

Authors
  1. Yidao Cai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Douglas A. Baxter
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Terry Crow
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cai, Y., Baxter, D.A. & Crow, T. Computational Study of Enhanced Excitability in Hermissenda: Membrane Conductances Modulated by 5-HT. J Comput Neurosci 15, 105–121 (2003). https://doi.org/10.1023/A:1024479020420

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1024479020420

Search

Navigation