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Oscillations and Synchrony in Large-scale Cortical Network Models

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Abstract

Intrinsic neuronal and circuit properties control the responses of large ensembles of neurons by creating spatiotemporal patterns of activity that are used for sensory processing, memory formation, and other cognitive tasks. The modeling of such systems requires computationally efficient single-neuron models capable of displaying realistic response properties. We developed a set of reduced models based on difference equations (map-based models) to simulate the intrinsic dynamics of biological neurons. These phenomenological models were designed to capture the main response properties of specific types of neurons while ensuring realistic model behavior across a sufficient dynamic range of inputs. This approach allows for fast simulations and efficient parameter space analysis of networks containing hundreds of thousands of neurons of different types using a conventional workstation. Drawing on results obtained using large-scale networks of map-based neurons, we discuss spatiotemporal cortical network dynamics as a function of parameters that affect synaptic interactions and intrinsic states of the neurons.

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Notes

  1. More often than not, neuronal dynamics is simulated using differential equations rather than difference equations (for example, the Hodgkin–Huxley model [1], the IF model [1719], and the Izhikevich model [22]). However, it is important to emphasize that to solve a differential equation numerically, it is usually rewritten in the form of a difference equation (e.g., using the Euler scheme, the time derivative dV/dt is replaced by (V n + 1 − V n )/τ).

  2. One can simplify the condition for the threshold by introducing a new control parameter \(\sigma^{\mathrm{new}}= \sigma - 2+\sqrt{\alpha/(1-\mu)}\). In this case, the threshold value occurs at \(\sigma^{\mathrm{new}}_{\mathrm{th}}=0\). In this paper, we do not use this change of the control parameter.

References

  1. Hodgkin, A.L, Huxley, A.F.: A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. (Lond.) 117, 500–544 (1952)

    Google Scholar 

  2. Bazhenov, M., Timofeev, I., Steriade, M., Sejnowski, T.J.: Model of thalamocortical slow-wave sleep oscillations and transitions to activated states. J. Neurosci. 22, 8691–8704 (2002)

    Google Scholar 

  3. Golomb, D.: Models of neuronal transient synchrony during propagation of activity through neocortical circuitry. J. Neurophysiol. 79, 1–12 (1998)

    Google Scholar 

  4. Golomb, D., Amitai, Y.: Propagating neuronal discharges in neocortical slices: computational and experimental study. J. Neurophysiol. 78, 1199–1211 (1997)

    Google Scholar 

  5. Houweling, A.R., Bazhenov, M., Timofeev, I., Grenier, F., Steriade, M., Sejnowski, T.J.: Frequency-selective augmenting responses by short-term synaptic depression in cat neocortex. J. Physiol. 542, 599–617 (2002)

    Article  Google Scholar 

  6. Mainen, Z.F., Sejnowski, T.J.: Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382, 363–366 (1996)

    Article  ADS  Google Scholar 

  7. Bazhenov, M., Timofeev, I., Steriade, M., Sejnowski, T.: Patterns of spiking-bursting activity in the thalamic reticular nucleus initiate sequences of spindle oscillations in thalamic network. J. Neurophysiol. 84, 1076–1087 (2000)

    Google Scholar 

  8. Bazhenov, M., Timofeev, I., Steriade, M., Sejnowski, T.J.: Computational models of thalamocortical augmenting responses. J. Neurosci. 18, 6444–6465 (1998)

    Google Scholar 

  9. Destexhe, A., Bal, T., McCormick, D.A., Sejnowski, T.J.: Ionic mechanisms underlying synchronized and propagating waves in a model of ferret thalamic slices. J. Neurophysiol. 76, 2049–2070 (1996)

    Google Scholar 

  10. Bazhenov, M., Timofeev, I., Steriade, M., Sejnowski, T.J.: Self-sustained rhythmic activity in the thalamic reticular nucleus mediated by depolarizing GABAA receptor potentials. Nat. Neurosci. 2, 168–174 (1999)

    Article  Google Scholar 

  11. Destexhe, A., Contreras, D., Sejnowski, T.J., Steriade, M.: A model of spindle rhythmicity in the isolated thalamic reticular nucleus. J. Neurophysiol. 72, 803–818 (1994)

    Google Scholar 

  12. Golomb, D., Wang, X.-J., Rinzel, J.: Propagation of spindle waves in a thalamic slice model. J. Neurophysiol. 75, 750–769 (1996)

    Google Scholar 

  13. Traub, R.D., Jefferys, J.G., Whittington, M.A.: Simulation of gamma rhythms in networks of interneurons and pyramidal cells. J. Comput. Neurosci. 4, 141–150 (1997)

    Article  MATH  Google Scholar 

  14. Traub, R.D., Whittington, M.A., Colling, S.B., Buzsaki, G., Jefferys, J.G.: Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J. Physiol. 493(Pt. 2), 471–484 (1996)

    Google Scholar 

  15. Bazhenov, M., Stopfer, M., Rabinovich, M., Abarbanel, H.D., Sejnowski, T.J., Laurent, G.: Model of cellular and network mechanisms for odor-evoked temporal patterning in the locust antennal lobe. Neuron 30, 569–581 (2001)

    Article  Google Scholar 

  16. Bazhenov, M., Stopfer, M., Rabinovich, M., Huerta, R., Abarbanel, H.D., Sejnowski, T.J., Laurent, G.: Model of transient oscillatory synchronization in the locust antennal lobe. Neuron 30, 553–567 (2001)

    Article  Google Scholar 

  17. Knight, B.W.: Dynamics of encoding in a population of neurons. J. Gen. Physiol. 59, 734–766 (1972)

    Article  Google Scholar 

  18. Stein, R.B.: The frequency of nerve action potentials generated by applied currents. Proc. R. Soc. Lond., B Biol. Sci. 167, 64–86 (1967)

    Article  ADS  Google Scholar 

  19. Tuckwell, H.C.: Introduction to Theoretical Neurobiology, vol. 2. Nonlinear and Stochastic Theories. Cambridge University Press, Cambridge (1988)

    Google Scholar 

  20. Casti, A.R., Omurtag, A., Sornborger, A., Kaplan, E., Knight, B., Victor, J., Sirovich, L.: A population study of integrate-and-fire-or-burst neurons. Neural Comput. 14, 957–986 (2002)

    Article  MATH  Google Scholar 

  21. Smith, G.D., Cox, C.L., Sherman, S.M., Rinzel, J.: Fourier analysis of sinusoidally driven thalamocortical relay neurons and a minimal integrate-and-fire-or-burst model. J. Neurophysiol. 83, 588–610 (2000)

    Google Scholar 

  22. Izhikevich, E.M.: Simple model of spiking neurons. IEEE Trans. Neural Netw. 14, 1569–1572 (2003)

    Article  Google Scholar 

  23. Rulkov, N.F., Timofeev, I., Bazhenov, M.: Oscillations in large-scale cortical networks: map-based model. J. Comput. Neurosci. 17, 203 (2004)

    Article  Google Scholar 

  24. Rulkov, N.F.: Modeling of spiking-bursting neural behavior using two-dimensional map. Phys. Rev. E 65, 041922 (2002).

    Article  ADS  MathSciNet  Google Scholar 

  25. Bazhenov, M., Rulkov, N.F., Fellous, J.M., Timofeev, I.: Role of network dynamics in shaping spike timing reliability. Phys. Rev. E 72, 041903 (2005)

    Article  ADS  MathSciNet  Google Scholar 

  26. Shilnikov, A.L., Rulkov, N.F.: Origin of chaos in a two-dimensional map modeling spiking-bursting neural activity. Int. J. Bifurc. Chaos 13, 3325 (2003).

    Article  MATH  MathSciNet  Google Scholar 

  27. Kuznetsov, Y.A.: Elements of Applied Bifurcation Theory, 3rd edn. Springer, New York (2004)

    MATH  Google Scholar 

  28. Rinzel, J., Ermentrout, B.: Analysis of neural excitability and oscillations. In: Koch, C., Segev, I. (eds.) Methods in Neural Modeling. From Ions to Networks. MIT, Cambridge (1998)

    Google Scholar 

  29. Elson, R.C., Selverston, A.I., Huerta, R., Rulkov, N.F., Rabinovich, M.I., Abarbanel, H.D.I.: Synchronous behavior of two coupled biological neurons. Phys. Rev. Lett. 81, 5692 (1998)

    Article  ADS  Google Scholar 

  30. Selverston, A.I.: Structural and functional basis of motor pattern generation in the stomatogastric ganglion of the lobster. Am. Zool. 14, 957 (1974)

    Google Scholar 

  31. Protopapas, A.D., Vanier, M., Bower, J.M.: Simulating of lagre networks of neurons. In: Koch, Ch., Segev, I. (eds.) Methods in Neuronal Modeling: from Ions to Networks, p. 461. MIT, Cambridge (1998)

    Google Scholar 

  32. Bacci, A., Rudolph, U., Huguenard, J.R., Prince, D.A.: Major differences in inhibitory synaptic transmission onto two neocortical interneuron subclasses. J. Neurosci. 23(29), 9664–9674 (2003)

    Google Scholar 

  33. McCormick, D.A., Pape, H.C.: Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J. Physiol. 431, 291–318 (1990)

    Google Scholar 

  34. Nuñez, A., Amzica, F., Steriade, M.: Electrophysiology of cat association cortical cells in vitro: intrinsic properies and synaptic responses. J. Neurophysiol. 70, 418–430 (1993)

    Google Scholar 

  35. Timofeev, I., Bazhenov, M.: In: Columbus, F. (ed.) Trends in Chronobiology Research, pp. 1–47. Nova, Commack (2005)

    Google Scholar 

  36. Fellous, J.M., Houweling, A.R., Modi, R.H., Rao, R.P., Tiesinga, P.H., Sejnowski, T.J.: Frequency dependence of spike timing reliability in cortical pyramidal cells and interneurons. J. Neurophysiol. 85, 1782–1787 (2001)

    Google Scholar 

  37. Schreiber, S., Fellous, J.M., Tiesinga, P., Sejnowski, T.J.: Influence of ionic conductances on spike timing reliability of cortical neurons for suprathreshold rhythmic inputs. J. Neurophysiol. 91, 194–205 (2004)

    Article  Google Scholar 

  38. Rougeul-Buser, A., Bouyer, J.J., Buser, P.: From attentiveness to sleep. A topographical analysis of localized “synchronized” activities on the cortex of normal cat and monkey. Acta Neurobiol. Exp. (Warsz) 35, 805–819 (1975)

    Google Scholar 

  39. Gray, C.M., Konig, P., Engel, A.K., Singer, W.: Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338, 334–337 (1989)

    Article  ADS  Google Scholar 

  40. Llinas, R., Ribary, U.: Coherent 40-Hz oscillation characterizes dream state in humans. Proc. Natl. Acad. Sci. U. S. A. 90, 2078–2081 (1993)

    Article  ADS  Google Scholar 

  41. Singer, W., Gray, C.M.: Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18, 555–586 (1995)

    Article  Google Scholar 

  42. Gabriel, A., Eckhorn, R.: A multi-channel correlation method detects traveling gamma-waves in monkey visual cortex. J. Neurosci. Methods 131, 171–184 (2003)

    Article  Google Scholar 

  43. Eckhorn, R., Gail, A., Bruns, A., Gabriel, A., Al-Shaikhli, B., Saam, M.: Neural mechanisms of visual associative processing. Acta Neurobiol. Exp. (Wars) 64, 239–252 (2004)

    Google Scholar 

  44. Buhl, E.H., Tamas, G., Fisahn, A.: Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J. Physiol. (Lond.) 513, 117–126 (1998)

    Article  Google Scholar 

  45. Whittington, M.A., Stanford, I.M., Colling, S.B., Jefferys, J.G., Traub, R.D.: Spatiotemporal patterns of gamma frequency oscillations tetanically induced in the rat hippocampal slice. J. Physiol. 502(Pt. 3), 591–607 (1997)

    Article  Google Scholar 

  46. Casado, J.M.: Transient activation in a network of coupled map neurons. Phys. Rev. Lett. 91, 208102 (2003)

    Article  ADS  Google Scholar 

  47. Casado, J.M., Ibarz, B., Sanjuan, M.A.F.: Winnerless competition in networks of coupled map neurons. Mod. Phys. Lett. B 18, 1347–1366 (2004)

    Article  ADS  Google Scholar 

  48. Ivanchenko, M.V., Osipov, G.V., Shalfeev, V.D., Kurths, J.: Synchronized bursts following instability of synchronous spiking in chaotic neuronal networks. Los Alamos National Laboratory, Los Alamos, nlin.CD/0601023 (2006)

    Google Scholar 

  49. Nowotny, T., Huerta, R., Abarbanel, H.D., Rabinovich, M.I.: Self-organization in the olfactory system: one shot odor recognition in insects. Biol. Cybern. 93, 436–446 (2005)

    Article  MATH  MathSciNet  Google Scholar 

  50. Osipov, G.V., Ivanchenko, M.V., Kurths, J., Hu, B.: Synchronized chaotic intermittent and spiking behavior in coupled map chains. Phys. Rev. E 71, 056209 (2005)

    Article  ADS  Google Scholar 

  51. Assisi, C., Stopfer, M., Laurent, G., Bazhenov, M.: Adaptive regulation of sparseness by feedforward inhibition. Nat. Neurosci. 10(9), 1176–1184 (2007)

    Article  Google Scholar 

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Acknowledgement

Partially supported by grant from ONR, N00014-07-1-0741 (NR) and by grant from NIDCD (MB).

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Correspondence to Nikolai F. Rulkov.

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Rulkov, N.F., Bazhenov, M. Oscillations and Synchrony in Large-scale Cortical Network Models. J Biol Phys 34, 279–299 (2008). https://doi.org/10.1007/s10867-008-9079-y

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