×

An empirical model for reliable spiking activity. (English) Zbl 1414.92124

Summary: Understanding a neuron’s transfer function, which relates a neuron’s inputs to its outputs, is essential for understanding the computational role of single neurons. Recently, statistical models, based on point processes and using generalized linear model (GLM) technology, have been widely applied to predict dynamic neuronal transfer functions. However, the standard version of these models fails to capture important features of neural activity, such as responses to stimuli that elicit highly reliable trial-to-trial spiking. Here, we consider a generalization of the usual GLM that incorporates nonlinearity by modeling reliable and nonreliable spikes as being generated by distinct stimulus features. We develop and apply these models to spike trains from olfactory bulb mitral cells recorded in vitro. We find that spike generation in these neurons is better modeled when reliable and unreliable spikes are considered separately and that this effect is most pronounced for neurons with a large number of both reliable and unreliable spikes.

MSC:

92C20 Neural biology

Software:

ElemStatLearn
Full Text: DOI

References:

[1] Agüera y Arcas, B., & Fairhall, A. L. (2003). What causes a neuron to spike? Neural Computation, 15(8), 1789-1807. , · Zbl 1046.92006
[2] Agüera y Arcas, B., Fairhall, A. L., & Bialek, W. (2003). Computation in a single neuron: Hodgkin and Huxley revisited. Neural Computation, 15(8), 1715-1749. , · Zbl 1085.68609
[3] Angelo, K., & Margrie, T. W. (2011). Population diversity and function of hyperpolarization-activated current in olfactory bulb mitral cells. Scientific Reports, 1.
[4] Angelo, K., Rancz, E. A., Pimentel, D., Hundahl, C., Hannibal, J., Fleischmann, A., … Margrie, T. W. (2012). A biophysical signature of network affiliation and sensory processing in mitral cells. Nature, 488(7411), 375-378. ,
[5] Badel, L., Lefort, S., Berger, T., Petersen, C., Gerstner, W., & Richardson, M. (2008). Extracting non-linear integrate-and-fire models from experimental data using dynamic I-V curves. Biological Cybernetics, 99(4), 361-370. , · Zbl 1161.92005
[6] Bryant, H. L., & Segundo, J. P. (1976). Spike initiation by transmembrane current: A white-noise analysis. Journal of Physiology, 260(2), 279-314. ,
[7] Burton, S. D., & Urban, N. N. (2014). Greater excitability and firing irregularity of tufted cells underlies distinct afferent-evoked activity of olfactory bulb mitral and tufted cells. Journal of Physiology, 592(10), 2097-2118. ,
[8] Butts, D. A., Weng, C., Jin, J., Alonso, J.-M., & Paninski, L. (2011). Temporal precision in the visual pathway through the interplay of excitation and stimulus-driven suppression. Journal of Neuroscience, 31(31), 11313-11327. ,
[9] Butts, D. A., Weng, C., Jin, J., Yeh, C.-I., Lesica, N. A., Alonso, J.-M., & Stanley, G. B. (2007). Temporal precision in the neural code and the timescales of natural vision. Nature, 449(7158), 92-95. ,
[10] Calabrese, A., Schumacher, J. W., Schneider, D. M., Paninski, L., & Woolley, S. M. N. (2011). A generalized linear model for estimating spectrotemporal receptive fields from responses to natural sounds. PLoS ONE, 6(1), e16104. ,
[11] Doya, K. (2011). Bayesian brain: Probabilistic approaches to neural coding. Cambridge, MA: MIT Press. · Zbl 1137.91015
[12] Escola, S., Fontanini, A., Katz, D., & Paninski, L. (2011). Hidden Markov models for the stimulus-response relationships of multistate neural systems. Neural Computation, 23(5), 1071-1132. , · Zbl 1217.92026
[13] Galán, R. F., Ermentrout, G. B., & Urban, N. N. (2008). Optimal time scale for spike-time reliability: Theory, simulations, and experiments. Journal of Neurophysiology, 99(1), 277-283. ,
[14] Giridhar, S., Doiron, B., & Urban, N. N. (2011). Timescale-dependent shaping of correlation by olfactory bulb lateral inhibition. Proceedings of the National Academy of Sciences, 108, 5843-5848. ,
[15] Hastie, T., Tibshirani, R., & Friedman, J. (2011). The elements of statistical learning: Data mining, inference, and prediction (2nd ed.). New York: Springer. · Zbl 0973.62007
[16] Hodgkin, A. L., & Huxley, A. F. (1952). A quantitative description of membrane current and its application to conduction and excitation in nerve. Journal of Physiology, 117(4), 500-544. ,
[17] Izhikevich, E. M. (2010). Dynamical systems in neuroscience: The geometry of excitability and bursting. Cambridge, MA: MIT Press.
[18] Kass, R. E., Eden, U., & Brown, E. N. (2014). Analysis of neural data. New York: Springer. , · Zbl 1404.62002
[19] Kass, R. E., & Ventura, V. (2001). A spike-train probability model. Neural Computation, 13(8), 1713-1720. , · Zbl 0985.92017
[20] Kelly, R. C., Smith, M. A., Kass, R. E., & Lee, T. S. (2010). Local field potentials indicate network state and account for neuronal response variability. Journal of Computational Neuroscience, 29, 567-579. , · Zbl 1446.92057
[21] Koch, C. (1999). Biophysics of computation: Information processing in single neurons. New York: Oxford University Press.
[22] Mainen, Z. F., & Sejnowski, T. J. (1995). Reliability of spike timing in neocortical neurons. Science, 268(5216), 1503-1506. ,
[23] Mensi, S., Naud, R., Pozzorini, C., Avermann, M., Petersen, C. C. H., & Gerstner, W. (2012). Parameter extraction and classification of three cortical neuron types reveals two distinct adaptation mechanisms. Journal of Neurophysiology, 107(6), 1756-1775. ,
[24] Ostojic, S., & Brunel, N. (2011). From spiking neuron models to linear-nonlinear models. PLoS Computational Biology, 7(1), e1001056. ,
[25] Padmanabhan, K., & Urban, N. N. (2010). Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content. Nature Neuroscience, 13(10), 1276-1282. ,
[26] Padmanabhan, K., & Urban, N. N. (2014). Disrupting information coding via block of 4-AP sensitive potassium channels. Journal of Neurophysiology, 12, 1054-1066. ,
[27] Paninski, L. (2004). Maximum likelihood estimation of cascade point-process neural encoding models. Network, 15(4), 243-262. ,
[28] Paninski, L., Pillow, J. W., & Simoncelli, E. P. (2004). Maximum likelihood estimation of a stochastic integrate-and-fire neural encoding model. Neural Computation, 16(12), 2533-2561. , · Zbl 1180.62179
[29] Pillow, J. W., Shlens, J., Paninski, L., Sher, A., Litke, A. M., Chichilnisky, E. J., & Simoncelli, E. P. (2008). Spatio-temporal correlations and visual signalling in a complete neuronal population. Nature, 454(7207), 995-999. ,
[30] Schwartz, O., Pillow, J. W., Rust, N. C., & Simoncelli, E. P. (2006). Spike-triggered neural characterization. Journal of Vision, 6(4), 484-507. ,
[31] Tiesinga, P., Fellous, J.-M., & Sejnowski, T. J. (2008). Regulation of spike timing in visual cortical circuits. Nature Reviews Neuroscience, 9(2), 97-107. ,
[32] Tripathy, S. J., Padmanabhan, K., Gerkin, R. C., and Urban, N. N. (2013). Intermediate intrinsic diversity enhances neural population coding. Proceedings of the National Academy of Sciences, 110(20), 8248-8253. ,
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.