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.
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.
Ascoli, G. A. (2006). Mobilizing the base of neuroscience data: The case of neuronal morphologies. Nature Reviews. Neuroscience, 7, 318–324.
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.
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.
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.
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.
Colbert, C. M., & Pan, E. (2002). Ion channel properties underlying axonal action potential initiation in pyramidal neurons. Nature Neuroscience, 5, 533–538.
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.
Glover, K. (1984). All optimal Hankel-norm approximations of linear multivariable systems and their L ∞ -error bounds. International Journal of Control, 39, 1115–1193.
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.
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.
Hines, M. (1984). Efficient computation of branched nerve equations. International Journal of Bio-Medical Computing, 15, 69–76.
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.
Kepler, T. B., Abbott, L., & Marder, E. (1992). Reduction of conductance-based neuron models. Biological Cybernetics, 66, 381–387.
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.
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.
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.
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.
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.
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.
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.
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.
Rall, W. (1959). Branching dendritic trees and motoneuron membrane resistivity. Experimental Neurology, 1, 491–527.
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.
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.
Traub, R. D., & Miles, R. (1991). Neuronal networks of the hippocampus. Cambridge: Cambridge University Press.
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
Corresponding author
Additional information
Action Editor: Wulfram Gerstner
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
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).
Rights 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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10827-010-0229-4