A Model of the Contribution of Interneuron Diversity to Recurrent Network Oscillation Generation and Information Coding | SpringerLink
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A Model of the Contribution of Interneuron Diversity to Recurrent Network Oscillation Generation and Information Coding

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Brain Informatics (BI 2023)

Abstract

Spiking neural network models that have studied how oscillations are generated by recurrent cortical circuits and how they encode information have been focused on describing the encoding of information about external sensory stimuli carried by feed-forward inputs in a two-population circuit configuration that includes excitatory cells and fast-spiking interneurons. Here we extend these models to explore the contribution of different classes of cortical interneurons to cortical oscillations. We found that in our extended model, the feed-forward stimulus is still mainly encoded in the gamma frequency range, consistent with earlier works using a single interneuron type. However, we also found that the information carried by different regions of the gamma frequency range was larger than the sum of the information carried by the two individual frequencies. This shows that the power values at different frequencies carried information about the feedforward input in a synergistic way. This is in contrast to previous models with only one interneuron type, which mainly led to redundant information between frequencies in the gamma range. These results suggest that interneuron diversity has useful properties for enriching the encoding of information in the gamma frequency range.

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References

  1. Adesnik, H., Bruns, W., Taniguchi, H., Huang, Z.J., Scanziani, M.: A neural circuit for spatial summation in visual cortex. Nature 490(7419), 226–231 (2012)

    Article  Google Scholar 

  2. Angelucci, A., Bijanzadeh, M., Nurminen, L., Federer, F., Merlin, S., Bressloff, P.C.: Circuits and Mechanisms for Surround Modulation in Visual Cortex. Annu. Rev. Neurosci. 40(1), 425–451 (2017)

    Article  Google Scholar 

  3. Barbieri, F., Mazzoni, A., Logothetis, N.K., Panzeri, S., Brunel, N.: Stimulus dependence of local field potential spectra: experiment versus theory. J. Neurosci. 34(44), 14589–14605 (2014)

    Article  Google Scholar 

  4. Belitski, A., et al.: Low-frequency local field potentials and spikes in primary visual cortex convey independent visual information. J. Neurosci. 28(22), 5696–5709 (2008)

    Article  Google Scholar 

  5. Belitski, A., Panzeri, S., Magri, C., Logothetis, N.K., Kayser, C.: Sensory information in local field potentials and spikes from visual and auditory cortices: time scales and frequency bands. J. Comput. Neurosci. 29(3), 533–545 (2010)

    Article  MATH  Google Scholar 

  6. Bertschinger, N., Rauh, J., Olbrich, E., Jost, J., Ay, N.: Quantifying unique information. Entropy 16(4), 2161–2183 (2014)

    Article  MathSciNet  MATH  Google Scholar 

  7. Brette, R., Gerstner, W.: Adaptive exponential integrate-and-fire model as an effective description of neuronal activity. J. Neurophysiol. 94(5), 3637–3642 (2005)

    Article  Google Scholar 

  8. Brunel, N., Wang, X.J.: What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. J. Neurophysiol. 90(1), 415–430 (2003)

    Article  Google Scholar 

  9. Buzsáky, G., Anastassiou, C.A., Koch, C.: The origin of extracellular fields and currents – EEG, ECoG, LFP and spikes. Nat. Rev. Neurosci. 13(6), 407–420 (2012)

    Article  Google Scholar 

  10. Buzsáky, G., Draguhn, A.: Neuronal oscillations in cortical networks. Science 304(5679), 1926–1929 (2004)

    Article  Google Scholar 

  11. Cardin, J.A., et al.: Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459(7247), 663–667 (2009)

    Article  Google Scholar 

  12. Cavallari, S., Panzeri, S., Mazzoni, A.: Comparison of the dynamics of neural interactions between current-based and conductance-based integrate-and-fire recurrent networks. Front. Neural Circ. 8, 12 (2014)

    Google Scholar 

  13. Cover, T.M., Thomas, J.A.: Information theory and statistics. Elements Inf. Theory 1(1), 279–335 (1991)

    MathSciNet  Google Scholar 

  14. DeFelipe, J., et al.: New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat. Rev. Neurosci. 14(3), 202–216 (2013)

    Article  Google Scholar 

  15. Descalzo, V.F., Nowak, L.G., Brumberg, J.C., McCormick, D.A., Sanchez-Vives, M.V.: Slow adaptation in fast-spiking neurons of visual cortex. J. Neurophysiol. 93(2), 1111–1118 (2005)

    Article  Google Scholar 

  16. Einevoll, G.T., Kayser, C., Logothetis, N.K., Panzeri, S.: Modelling and analysis of local field potentials for studying the function of cortical circuits. Nat. Rev. Neurosci. 14(11), 770–785 (2013)

    Article  Google Scholar 

  17. Gewaltig, M.O., Diesmann, M.: NEST (NEural simulation tool). Scholarpedia 2(4), 1430 (2007)

    Article  Google Scholar 

  18. Henrie, J.A., Shapley, R.: LFP power spectra in V1 cortex: the graded effect of stimulus contrast. J. Neurophysiol. 94(1), 479–490 (2005)

    Article  Google Scholar 

  19. Kayser, C., König, P.: Stimulus locking and feature selectivity prevail in complementary frequency ranges of V1 local field potentials. Eur. J. Neurosci. 19(2), 485–489 (2004)

    Article  Google Scholar 

  20. Litwin-Kumar, A., Rosenbaum, R., Doiron, B.: Inhibitory stabilization and visual coding in cortical circuits with multiple interneuron subtypes. J. Neurophysiol. 115(3), 1399–1409 (2016)

    Article  Google Scholar 

  21. Magri, C., Whittingstall, K., Singh, V., Logothetis, N.K., Panzeri, S.: A toolbox for the fast information analysis of multiple-site LFP, EEG and spike train recordings. BMC Neurosci. 10(1), 81 (2009)

    Article  Google Scholar 

  22. Martínez-Cañada, P., Ness, T.V., Einevoll, G.T., Fellin, T., Panzeri, S.: Computation of the electroencephalogram (EEG) from network models of point neurons. PLOS Comput. Biol. 17(4), e1008893 (2021)

    Article  Google Scholar 

  23. Martínez-Cañada, P., Noei, S., Panzeri, S.: Methods for inferring neural circuit interactions and neuromodulation from local field potential and electroencephalogram measures. Brain Inform. 8(1), 27 (2021)

    Article  Google Scholar 

  24. Mazzoni, A., Lindén, H., Cuntz, H., Lansner, A., Panzeri, S., Einevoll, G.T.: Computing the local field potential (LFP) from integrate-and-fire network models. PLOS Comput. Biol. 11(12), e1004584 (2015)

    Article  Google Scholar 

  25. Mazzoni, A., Panzeri, S., Logothetis, N.K., Brunel, N.: Encoding of naturalistic stimuli by local field potential spectra in networks of excitatory and inhibitory neurons. PLoS Comput. Biol. 4(12), e1000239 (2008)

    Article  MathSciNet  Google Scholar 

  26. Mitra, P.: Observed Brain Dynamics. Oxford University Press, Oxford (2007)

    Book  Google Scholar 

  27. Panzeri, S., Schultz, S.R., Treves, A., Rolls, E.T.: Correlations and the encoding of information in the nervous system. Proc. R. Soc. London Ser. B: Biol. Sci. 266(1423), 1001–1012 (1999)

    Google Scholar 

  28. Panzeri, S., Senatore, R., Montemurro, M.A., Petersen, R.S.: Correcting for the sampling bias problem in spike train information measures. J. Neurophysiol. 98(3), 1064–1072 (2007)

    Article  Google Scholar 

  29. Panzeri, S., Treves, A.: Analytical estimates of limited sampling biases in different information measures. Netw. Comput. Neural Syst. 7(1), 87 (1996)

    Article  MATH  Google Scholar 

  30. Pesaran, B., et al.: Investigating large-scale brain dynamics using field potential recordings: analysis and interpretation. Nat. Neurosci. 21(7), 903–919 (2018)

    Article  Google Scholar 

  31. Pfeffer, C.K., Xue, M., He, M., Huang, Z.J., Scanziani, M.: Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat. Neurosci. 16(8), 1068–1076 (2013)

    Article  Google Scholar 

  32. Pola, G., Thiele, A., Hoffmann, K.P., Panzeri, S.: An exact method to quantify the information transmitted by different mechanisms of correlational coding. Netw. Comput. Neural Syst. 14(1), 35–60 (2003)

    Article  Google Scholar 

  33. Roth, A., van Rossum, M.C.W.: Modeling synapses. In: De Schutter, E. (ed.) Computational Modeling Methods for Neuroscientists. The MIT Press (2009)

    Google Scholar 

  34. Schneidman, E., Bialek, W., Berry, M.J.: Synergy, redundancy, and independence in population codes. J. Neurosci. 23(37), 11539–11553 (2003)

    Article  Google Scholar 

  35. Shannon, C.E.: A mathematical theory of communication. Bell Syst. Tech. J. 27(3), 379–423 (1948)

    Article  MathSciNet  MATH  Google Scholar 

  36. Urban-Ciecko, J., Barth, A.L.: Somatostatin-expressing neurons in cortical networks. Nat. Rev. Neurosci. 17(7), 401–409 (2016)

    Article  Google Scholar 

  37. Veit, J., Hakim, R., Jadi, M.P., Sejnowski, T.J., Adesnik, H.: Cortical gamma band synchronization through somatostatin interneurons. Nat. Neurosci. 20(7), 951–959 (2017)

    Article  Google Scholar 

  38. Williams, P.L., Beer, R.D.: Nonnegative Decomposition of Multivariate Information. arXiv preprint arXiv:1004.2515 (2010)

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Correspondence to Gabriel Matías Lorenz .

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Lorenz, G.M., Martínez-Cañada, P., Panzeri, S. (2023). A Model of the Contribution of Interneuron Diversity to Recurrent Network Oscillation Generation and Information Coding. In: Liu, F., Zhang, Y., Kuai, H., Stephen, E.P., Wang, H. (eds) Brain Informatics. BI 2023. Lecture Notes in Computer Science(), vol 13974. Springer, Cham. https://doi.org/10.1007/978-3-031-43075-6_4

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  • DOI: https://doi.org/10.1007/978-3-031-43075-6_4

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