Skip to main content
Log in

Morphologically accurate reduced order modeling of spiking neurons

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

Abstract

Accurately simulating neurons with realistic morphological structure and synaptic inputs requires the solution of large systems of nonlinear ordinary differential equations. We apply model reduction techniques to recover the complete nonlinear voltage dynamics of a neuron using a system of much lower dimension. Using a proper orthogonal decomposition, we build a reduced-order system from salient snapshots of the full system output, thus reducing the number of state variables. A discrete empirical interpolation method is then used to reduce the complexity of the nonlinear term to be proportional to the number of reduced variables. Together these two techniques allow for up to two orders of magnitude dimension reduction without sacrificing the spatially-distributed input structure, with an associated order of magnitude speed-up in simulation time. We demonstrate that both nonlinear spiking behavior and subthreshold response of realistic cells are accurately captured by these low-dimensional models.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

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

  • Antoulas, A. C., & Sorensen, D. C. (2001). Approximation of large-scale dynamical systems: An overview. International Journal of Applied Math and Computer Science, 11(5), 1093–1121.

    Google Scholar 

  • Ascoli, G. A. (2006). Mobilizing the base of neuroscience data: The case of neuronal morphologies. Nature Reviews. Neuroscience, 7, 318–324.

    Article  CAS  PubMed  Google Scholar 

  • Barrault, M., Maday, Y., Nguyen, N. C., & Patera, A. T. (2004). An ‘empirical interpolation’ method: Application to efficient reduced-basis discretization of partial differential equations. Comptes Rendus de l’Académie des Sciences, Paris, 339, 667–672.

    Google Scholar 

  • Bhalla, U. S., Bilitch, D. H., & Bower, J. M. (1992). Rallpacks: A set of benchmarks for neuronal simulators. Trends in Neuroscience, 15(11), 453–458.

    Article  CAS  Google Scholar 

  • Brunel, N., & Wang, X.-J. (2003). What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. Journal of Neurophysiology, 90, 415–430.

    Article  PubMed  Google Scholar 

  • Chaturantabut, S., & Sorensen, D. C. (2009). Discrete empirical interpolation for nonlinear model reduction. Technical report TR09-05, Department of Computational and Applied Mathematics, Rice University.

  • Chitwood, R. A., Hubbard, A., & Jaffe, D. B. (1999). Passive electrotonic properties of rat hippocampal CA3 interneurones. Journal of Physiology, 515, 743–756.

    Article  CAS  PubMed  Google Scholar 

  • Colbert, C. M., & Pan, E. (2002). Ion channel properties underlying axonal action potential initiation in pyramidal neurons. Nature Neuroscience, 5, 533–538.

    Article  CAS  PubMed  Google Scholar 

  • Furtak, S. C., Moyer, J. R., Jr., & Brown, T. H. (2007). Morphology and ontogeny of rat perirhinal cortical neurons. Journal of Comparative Neurology, 505(5), 493–510.

    Article  PubMed  Google Scholar 

  • Glover, K. (1984). All optimal Hankel-norm approximations of linear multivariable systems and their L  ∞ -error bounds. International Journal of Control, 39, 1115–1193.

    Article  Google Scholar 

  • Golding, N. L., Kath, W. L., & Spruston, N. (2001). Dichotomy of action-potential backpropagation in CA1 pyramidal neuron dendrites. Journal of Neurophysiology, 86, 2998–3010.

    CAS  PubMed  Google Scholar 

  • Golding, N. L., Mickus, T. J., Katz, Y., Kath, W. L., & Spruston, N. (2005). Factors mediating powerful voltage attenuation along CA1 pyramidal neuron dendrites. Journal of Physiology, 568, 69–82.

    Article  CAS  PubMed  Google Scholar 

  • Hines, M. (1984). Efficient computation of branched nerve equations. International Journal of Bio-Medical Computing, 15, 69–76.

    Article  CAS  PubMed  Google Scholar 

  • Kellems, A. R., Roos, D., Xiao, N., & Cox, S. J. (2009). Low-dimensional, morphologically accurate models of subthreshold membrane potential. Journal of Computational Neuroscience, 27, 161–176.

    Article  PubMed  Google Scholar 

  • Kepler, T. B., Abbott, L., & Marder, E. (1992). Reduction of conductance-based neuron models. Biological Cybernetics, 66, 381–387.

    Article  CAS  PubMed  Google Scholar 

  • Kistler, W. M., Gerstner, W., & van Hemmen, J. L. (1997). Reduction of the Hodgkin–Huxley equations to a single-variable threshold model. Neural Computation, 9, 1015–1045.

    Article  Google Scholar 

  • Kole, M. H. P., Ilschner, S. U., Kampa, B. M., Williams, S. R., Ruben, P. C., & Stuart, G. J. (2008). Action potential generation requires a high sodium channel density in the axon initial segment. Nature Neuroscience, 11, 178–186.

    Article  CAS  PubMed  Google Scholar 

  • Kunisch, K., & Volkwein, S. (2002). Galerkin proper orthogonal decomposition methods for a general equation in fluid dynamics. SIAM Journal on Numerical Analysis, 40(2), 492–515.

    Article  Google Scholar 

  • Liang, Y. C., Lee, H. P., Lim, S. P., Lin, W. Z., Lee, K. H., & Wu, C. G. (2002). Proper orthogonal decomposition and its applications—part I: Theory. Journal of Sound and Vibration, 252, 527–544.

    Article  Google Scholar 

  • Mainen, Z. F., & Sejnowski, T. J. (1998). Modeling active dendritic processes in pyramidal neurons. In C. Koch, & I. Segev (Eds.), Methods in neuronal modeling: From ions to networks (2nd ed., pp. 171–210). Cambridge: MIT.

    Google Scholar 

  • Martinez, J. O. (2008). Rice-Baylor archive of neuronal morphology. http://www.caam.rice.edu/~cox/neuromart. Accessed 1 May 2008.

  • Migliore, M., Hoffman, D. A., Magee, J. C., & Johnston, D. (1999). Role of an A-type K +  conductance in the back-propagation of action potentials in the dendrites of hippocampal pyramidal neurons. Journal of Computational Neuroscience, 7, 5–15.

    Article  CAS  PubMed  Google Scholar 

  • NeuroMorpho.org (2008). The neuromorpho.org inventory. http://NeuroMorpho.org. Accessed 11 March 2008.

  • Nguyen, N. C., Patera, A. T., & Peraire, J. (2008). A ‘best points’ interpolation method for efficient approximation of parametrized functions. International Journal for Numerical Methods in Engineering, 73, 521–543.

    Article  Google Scholar 

  • Pinsky, P. F., & Rinzel, J. (1994). Intrinsic and network rhythmogenesis in a reduced Traub model for CA3 neurons. Journal of Computational Neuroscience, 1, 39–60.

    Article  CAS  PubMed  Google Scholar 

  • Rall, W. (1959). Branching dendritic trees and motoneuron membrane resistivity. Experimental Neurology, 1, 491–527.

    Article  CAS  PubMed  Google Scholar 

  • Rihn, L. L., & Claiborne, B. J. (1990). Dendritic growth and regression in rat dentate granule cells during late postnatal development. Brain Research, Developmental Brain Research, 54(1), 115–24.

    Article  CAS  Google Scholar 

  • Toris, C. B., Eiesland, J. L., & Miller, R. F. (1995) Morphology of ganglion cells in the neotenous tiger salamander retina. Journal of Comparative Neurology, 352(4), 535–59.

    Article  CAS  PubMed  Google Scholar 

  • Traub, R. D., & Miles, R. (1991). Neuronal networks of the hippocampus. Cambridge: Cambridge University Press.

    Google Scholar 

Download references

Acknowledgements

The work in this paper is supported by NSF grant DMS-0240058, by a training fellowship from the Keck Center for Interdisciplinary Bioscience Training of the Gulf Coast Consortia (NIBIB Grant No. 1T32EB006350-01A1), by AFOSR grant FA9550-06-1-0245, by AFOSR grant FA9550-09-1-0225, and by NSF grant CCF-0634902

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Steven J. Cox.

Additional information

Action Editor: Wulfram Gerstner

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

(PDF 110 KB)

Appendix

Appendix

The following table contains the information pertaining to the ion channels and gating variable kinetics that allow weakly excitable dendrites. The model is based on that of Migliore et al. (1999) for I Na , \(I_{K_{\text{DR}}}\), \(I_{K_{\text{A}}}\), and \(I_{\text{leak}}\), though there have been some modifications to the time constants for \(l_{\text{prox}}\) and \(l_{\text{dist}}\), which was done to obtain a good fit to the original functions without the need for defining them piecewise. Some of the gating variables in this model have time constants τ which depend on temperature T via a so-called Q 10 factor. When we use this model, we set T = 35°C to match the value used in Migliore et al. (1999).

The complete HH and HHA channel models can be found in the appendix of Kellems et al. (2009).

Table 12 Channel model and kinetics that allow weakly excitable dendrites. For G(x), x is measured in μm from the soma. The model for \(I_{K_{\text{A}}}\) is divided into two components, proximal and distal, which are denoted \(I_{K_{\text{A(prox)}}}\) and \(I_{K_{\text{A(dist)}}}\), respectively

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kellems, A.R., Chaturantabut, S., Sorensen, D.C. et al. Morphologically accurate reduced order modeling of spiking neurons. J Comput Neurosci 28, 477–494 (2010). https://doi.org/10.1007/s10827-010-0229-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10827-010-0229-4

Keywords

Navigation