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.
Similar content being viewed by others
Notes
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 [17–19], 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).
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
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)
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)
Golomb, D.: Models of neuronal transient synchrony during propagation of activity through neocortical circuitry. J. Neurophysiol. 79, 1–12 (1998)
Golomb, D., Amitai, Y.: Propagating neuronal discharges in neocortical slices: computational and experimental study. J. Neurophysiol. 78, 1199–1211 (1997)
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)
Mainen, Z.F., Sejnowski, T.J.: Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382, 363–366 (1996)
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)
Bazhenov, M., Timofeev, I., Steriade, M., Sejnowski, T.J.: Computational models of thalamocortical augmenting responses. J. Neurosci. 18, 6444–6465 (1998)
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)
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)
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)
Golomb, D., Wang, X.-J., Rinzel, J.: Propagation of spindle waves in a thalamic slice model. J. Neurophysiol. 75, 750–769 (1996)
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)
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)
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)
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)
Knight, B.W.: Dynamics of encoding in a population of neurons. J. Gen. Physiol. 59, 734–766 (1972)
Stein, R.B.: The frequency of nerve action potentials generated by applied currents. Proc. R. Soc. Lond., B Biol. Sci. 167, 64–86 (1967)
Tuckwell, H.C.: Introduction to Theoretical Neurobiology, vol. 2. Nonlinear and Stochastic Theories. Cambridge University Press, Cambridge (1988)
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)
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)
Izhikevich, E.M.: Simple model of spiking neurons. IEEE Trans. Neural Netw. 14, 1569–1572 (2003)
Rulkov, N.F., Timofeev, I., Bazhenov, M.: Oscillations in large-scale cortical networks: map-based model. J. Comput. Neurosci. 17, 203 (2004)
Rulkov, N.F.: Modeling of spiking-bursting neural behavior using two-dimensional map. Phys. Rev. E 65, 041922 (2002).
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)
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).
Kuznetsov, Y.A.: Elements of Applied Bifurcation Theory, 3rd edn. Springer, New York (2004)
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)
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)
Selverston, A.I.: Structural and functional basis of motor pattern generation in the stomatogastric ganglion of the lobster. Am. Zool. 14, 957 (1974)
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)
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)
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)
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)
Timofeev, I., Bazhenov, M.: In: Columbus, F. (ed.) Trends in Chronobiology Research, pp. 1–47. Nova, Commack (2005)
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)
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)
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)
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)
Llinas, R., Ribary, U.: Coherent 40-Hz oscillation characterizes dream state in humans. Proc. Natl. Acad. Sci. U. S. A. 90, 2078–2081 (1993)
Singer, W., Gray, C.M.: Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18, 555–586 (1995)
Gabriel, A., Eckhorn, R.: A multi-channel correlation method detects traveling gamma-waves in monkey visual cortex. J. Neurosci. Methods 131, 171–184 (2003)
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)
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)
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)
Casado, J.M.: Transient activation in a network of coupled map neurons. Phys. Rev. Lett. 91, 208102 (2003)
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)
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)
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)
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)
Assisi, C., Stopfer, M., Laurent, G., Bazhenov, M.: Adaptive regulation of sparseness by feedforward inhibition. Nat. Neurosci. 10(9), 1176–1184 (2007)
Acknowledgement
Partially supported by grant from ONR, N00014-07-1-0741 (NR) and by grant from NIDCD (MB).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10867-008-9079-y