Skip to main content
SpringerLink
Log in

Co-variation of ionic conductances supports phase maintenance in stomatogastric neurons

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

Abstract

Neuronal networks produce reliable functional output throughout the lifespan of an animal despite ceaseless molecular turnover and a constantly changing environment. Central pattern generators, such as those of the crustacean stomatogastric ganglion (STG), are able to robustly maintain their functionality over a wide range of burst periods. Previous experimental work involving extracellular recordings of the pyloric pattern of the STG has demonstrated that as the burst period varies, the inter-neuronal delays are altered proportionally, resulting in burst phases that are roughly invariant. The question whether spike delays within bursts are also proportional to pyloric period has not been explored in detail. The mechanism by which the pyloric neurons accomplish phase maintenance is currently not obvious. Previous studies suggest that the co-regulation of certain ion channel properties may play a role in governing neuronal activity. Here, we observed in long-term recordings of the pyloric rhythm that spike delays can vary proportionally with burst period, so that spike phase is maintained. We then used a conductance-based model neuron to determine whether co-varying ionic membrane conductances results in neural output that emulates the experimentally observed phenomenon of spike phase maintenance. Next, we utilized a model neuron database to determine whether conductance correlations exist in model neuron populations with highly maintained spike phases. We found that co-varying certain conductances, including the sodium and transient calcium conductance pair, causes the model neuron to maintain a specific spike phase pattern. Results indicate a possible relationship between conductance co-regulation and phase maintenance in STG neurons.

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
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Achard, P., & De Schutter, E. (2006). Complex parameter landscape for a complex neuron model. PLoS Computational Biology, 2(7), e94. doi:10.1371/journal.pcbi.0020094.

    Article  PubMed  Google Scholar 

  • Ball, J. M., Franklin, C. C., Tobin, A. E., Schulz, D. J., & Nair, S. S. (2010). Coregulation of ion channel conductances preserves output in a computational model of a crustacean cardiac motor neuron. Journal of Neuroscience, 30(25), 8637–8649.

    Article  PubMed  CAS  Google Scholar 

  • Baro, D. J., Levini, R. M., Kim, M. T., Willms, A. R., Lanning, C. C., Rodriguez, H. E., et al. (1997). Quantitative single-cell-reverse transcription-PCR demonstrates that A-current magnitude varies as a linear function of shal gene expression in identified stomatogastric neurons. Journal of Neuroscience, 17(17), 6597–6610.

    PubMed  CAS  Google Scholar 

  • Brochini, L., Carelli, P. V., & Pinto, R. D. (2011). Single synapse information coding in intraburst spike patterns of central pattern generator motor neurons. Journal of Neuroscience, 31(34), 12297–12306.

    Article  PubMed  CAS  Google Scholar 

  • Bucher, D., Prinz, A. A., & Marder, E. (2005). Animal-to-animal variability in motor pattern production in adults and during growth. Journal of Neuroscience, 25(7), 1611–1619.

    Article  PubMed  CAS  Google Scholar 

  • Dayan, P., & Abbott, L. F. (2001). Theoretical neuroscience. Cambridge: MIT Press.

    Google Scholar 

  • Goldman, M. S., Golowasch, J., Marder, E., & Abbott, L. F. (2001). Global structure, robustness, and modulation of neuronal models. Journal of Neuroscience, 21(14), 5229–5238.

    PubMed  CAS  Google Scholar 

  • Golowasch, J., Goldman, M. S., Abbott, L. F., & Marder, E. (2002). Failure of averaging in the construction of a conductance-based neuron model. Journal of Neurophysiology, 87(2), 1129–1131.

    PubMed  Google Scholar 

  • Graubard, K. (1978). Synaptic transmission without action potentials: input–output properties of a nonspiking presynaptic neuron. Journal of Neurophysiology, 41(4), 1014–1025.

    PubMed  CAS  Google Scholar 

  • Hooper, S. L. (1997a). Phase maintenance in the pyloric pattern of the lobster (Panulirus interruptus) stomatogastric ganglion. Journal of Computational Neuroscience, 4(3), 191–205.

    Article  PubMed  CAS  Google Scholar 

  • Hooper, S. L. (1997b). The pyloric pattern of the lobster (Panulirus interruptus) stomatogastric ganglion comprises two phase-maintaining subsets. Journal of Computational Neuroscience, 4(3), 207–219.

    Article  PubMed  CAS  Google Scholar 

  • Hooper, S. L., & Weaver, A. L. (2000). Motor neuron activity is often insufficient to predict motor response. Current Opinion in Neurobiology, 10(6), 676–682.

    Article  PubMed  CAS  Google Scholar 

  • Hudson, A. E., & Prinz, A. A. (2010). Conductance ratios and cellular identity. PLoS Computational Biology, 6(7), e1000838. doi:10.1371/journal.pcbi.1000838.

    Article  PubMed  Google Scholar 

  • Huguenard, J. R., & McCormick, D. A. (1992). Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons. Journal of Neurophysiology, 68(4), 1373–1383.

    PubMed  CAS  Google Scholar 

  • Khorkova, O., & Golowasch, J. (2007). Neuromodulators, not activity, control coordinated expression of ionic currents. Journal of Neuroscience, 27(32), 8709–8718.

    Article  PubMed  CAS  Google Scholar 

  • Lago-Fernandez, L. F. (2007). Spike alignment in bursting neurons. Neurocomputing, 70, 1788–1791.

    Article  Google Scholar 

  • Latorre, R., Rodriguez, F. B., & Varona, P. (2006). Neural signatures: multiple coding in spiking-bursting cells. Biological Cybernetics, 95(2), 169–183.

    Article  PubMed  Google Scholar 

  • LeMasson, G., Marder, E., & Abbott, L. F. (1993). Activity-dependent regulation of conductances in model neurons. Science, 259(5103), 1915–1917.

    Article  PubMed  CAS  Google Scholar 

  • Levitan, I. B. (1988). Modulation of ion channels in neurons and other cells. Annual Review of Neuroscience, 11, 119–136.

    Article  PubMed  CAS  Google Scholar 

  • Liu, Z., Golowasch, J., Marder, E., & Abbott, L. F. (1998). A model neuron with activity-dependent conductances regulated by multiple calcium sensors. Journal of Neuroscience, 18(7), 2309–2320.

    PubMed  CAS  Google Scholar 

  • MacLean, J. N., Zhang, Y., Johnson, B. R., & Harris-Warrick, R. M. (2003). Activity-independent homeostasis in rhythmically active neurons. Neuron, 37(1), 109–120.

    Article  PubMed  CAS  Google Scholar 

  • MacLean, J. N., Zhang, Y., Goeritz, M. L., Casey, R., Oliva, R., Guckenheimer, J., et al. (2005). Activity-independent coregulation of IA and Ih in rhythmically active neurons. Journal of Neurophysiology, 94(5), 3601–3617.

    Article  PubMed  Google Scholar 

  • Marder, E. (1997). Computational dynamics in rhythmic neural circuits. The Neuroscientist, 3, 295–302.

    Google Scholar 

  • Marder, E., & Bucher, D. (2007). Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annual Review of Physiology, 69, 291–316.

    Article  PubMed  CAS  Google Scholar 

  • Morris, L. G., & Hooper, S. L. (1997). Muscle response to changing neuronal input in the lobster (Panulirus interruptus) stomatogastric system: spike number- versus spike frequency-dependent domains. Journal of Neuroscience, 17(15), 5956–5971.

    PubMed  CAS  Google Scholar 

  • Morris, L. G., Thuma, J. B., & Hooper, S. L. (2000). Muscles express motor patterns of non-innervating neural networks by filtering broad-band input. Nature Neuroscience, 3(3), 245–250.

    Article  PubMed  CAS  Google Scholar 

  • Prinz, A. A., Billimoria, C. P., & Marder, E. (2003a). Alternative to hand-tuning conductance-based models: construction and analysis of databases of model neurons. Journal of Neurophysiology, 90(6), 3998–4015.

    Article  Google Scholar 

  • Prinz, A. A., Thirumalai, V., & Marder, E. (2003b). The functional consequences of changes in the strength and duration of synaptic inputs to oscillatory neurons. Journal of Neuroscience, 23(3), 943–954.

    CAS  Google Scholar 

  • Prinz, A. A., Bucher, D., & Marder, E. (2004). Similar network activity from disparate circuit parameters. Nature Neuroscience, 7(12), 1345–1352.

    Article  PubMed  CAS  Google Scholar 

  • Raper, J. A. (1979). Nonimpulse-mediated synaptic transmission during the generation of a cyclic motor program. Science, 205(4403), 304–306.

    Article  PubMed  CAS  Google Scholar 

  • Schulz, D. J., Goaillard, J. M., & Marder, E. (2006). Variable channel expression in identified single and electrically coupled neurons in different animals. Nature Neuroscience, 9(3), 356–362.

    Article  PubMed  CAS  Google Scholar 

  • Schulz, D. J., Goaillard, J. M., & Marder, E. E. (2007). Quantitative expression profiling of identified neurons reveals cell-specific constraints on highly variable levels of gene expression. Proceedings of the National Academy of Sciences of the United States of America, 104(32), 13187–13191.

    Article  PubMed  Google Scholar 

  • Selverston, A. I. (2010). Invertebrate central pattern generator circuits. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 365(1551), 2329–2345.

    Article  PubMed  Google Scholar 

  • Selverston, A. I., & Moulins, M. (1985). Oscillatory neural networks. Annual Review of Physiology, 47, 29–48.

    Article  PubMed  CAS  Google Scholar 

  • Swensen, A. M., & Bean, B. P. (2003). Ionic mechanisms of burst firing in dissociated Purkinje neurons. Journal of Neuroscience, 23(29), 9650–9663.

    PubMed  CAS  Google Scholar 

  • Swensen, A. M., & Bean, B. P. (2005). Robustness of burst firing in dissociated purkinje neurons with acute or long-term reductions in sodium conductance. Journal of Neuroscience, 25(14), 3509–3520.

    Article  PubMed  CAS  Google Scholar 

  • Szucs, A., Pinto, R. D., Rabinovich, M. I., Abarbanel, H. D., & Selverston, A. I. (2003). Synaptic modulation of the interspike interval signatures of bursting pyloric neurons. Journal of Neurophysiology, 89(3), 1363–1377.

    Article  PubMed  Google Scholar 

  • Tobin, A. E., Cruz-Bermúdez, N. D., Marder, E., & Schulz, D. J. (2009). Correlations in ion channel mRNA in rhythmically active neurons. PLoS One, 4(8), e6742. doi:10.1371/journal.pone.0006742.

    Article  PubMed  Google Scholar 

  • Turrigiano, G., LeMasson, G., & Marder, E. (1995). Selective regulation of current densities underlies spontaneous changes in the activity of cultured neurons. Journal of Neuroscience, 15(5 Pt 1), 3640–3652.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Amber Hudson for informative discussions and valuable comments on the manuscript. We also thank the reviewers of the manuscript for their constructive criticism. This work was supported by grants from the National Institute of Health/National Institute of Neurological Disorders and Stroke (1F31NS071834-01 to SA and R01 NS054911 to AP), two National Science Foundation IGERT awards (to SA and WS), and a National Science Foundation Graduate Research Fellowship (to WS).

Conflicts of interest

The authors declare that no conflicts of interest exist.

Author information

Authors and Affiliations

  1. Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology/Emory University, 313 Ferst Drive, Atlanta, GA, 30332, USA

    Wafa Soofi

  2. Department of Biology, Emory University, 1510 Clifton Rd NE, Atlanta, GA, 30322, USA

    Santiago Archila & Astrid A. Prinz

Authors
  1. Wafa Soofi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Santiago Archila
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Astrid A. Prinz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wafa Soofi.

Additional information

Action Editor: Frances K. Skinner

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 411 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Soofi, W., Archila, S. & Prinz, A.A. Co-variation of ionic conductances supports phase maintenance in stomatogastric neurons. J Comput Neurosci 33, 77–95 (2012). https://doi.org/10.1007/s10827-011-0375-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10827-011-0375-3

Keywords

Search

Navigation