Influence of synchronous and asynchronous signals from pyramidal neurons on synchronization of GABAergic interneuronal networks on the hippocampus


  • S. О. Kochubey Oles Honchar Dnipropetrovsk National University
Keywords: interneuronal network, GABAergic synapses, synchronization, stochastic, synaptic signal

Abstract

We investigated the impact of the level of stochastic excitation of synaptic signals from pyramidal neurons on the generation of oscillations inside the interneuronal networks of the hippocampus with shunting GABAergic synapses. We used a modification of a mathematical model of the interneuronal networks (I. Vida, M. Bartos and P. Jonas, 2006) together with a model of external synaptic signalling with a Poisson distribution of time interval between events. We demonstrated that a completely synchronized synaptic signal when every interneuron in the network was impacted by an electric current with the same amplitude and frequency caused oscillations with a high level of synchronization (k > 0,9) in the network. The increase of synaptic signal frequency led to the respective increasing of oscillation frequency in the network. We demonstrated that a gradual increase of stochastic synaptic current from 0.001 to 0.200 causes reduction of synchronisation of oscillations in the interneuronal network from 0.89 to 0.11 with an equal signal frequency of 6 Hz. The frequency of oscillations in the interneuronal network also decreased from 55.6 to 35.7 Hz respectively for the levels of stochastisity 0.001 to 0.200 and the frequency of excitation of 58 Hz. Decrease of frequency and synchronization of oscillations in the network could be explained by the the inability of shunting GABAergic synapses to synchronize the work of separate interneurons when there is significant increase in stochastic external excitation. Besides this, we demonstrated the existence of a range of frequencies of the incoming signal of 30–40 Hz in the network, of which a significant increase of synchronisation of oscillations in the network takes place regardless of the stages of external stochastic excitation. 

References

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Traub, R.D., Whittington, M.A., Colling, S.B., Buzsaki, G., Jefferys, J.G., 1996. Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J. Physiol. 493(2), 471–484.
Turner, D.A., 1984. Segmental cable evaluation of somatic transients in hippocampal neurons (CA1, CA3, and dentate). Biophys. J. 46(1), 73–84. >> doi:10.1016/S0006-3495(84)84000-X
Van Der Werf, J., Jensen, O., Fries, P., Medendorp, W.P., 2008. Gamma-band activity in human posterior parietal cortex encodes the motor goal during delayed prosaccades and antisaccades. J. Neurosci. 28(34), 8397–8405. >> doi:10.1523/JNEUROSCI.0630-08.2008
Vida, I., Bartos, M., Jonas, P., 2006. Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates. Neuron 49(1), 107–117. >> doi:10.1016/j.neuron.2005.11.036
Wang, X.J., Buzsaki, G., 1996. Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J. Neurosci. 16(20), 6402–6413.
Akam, T., Kullmann, D.M., 2010. Oscillations and filtering networks support flexible routing of information. Neuron 67(2), 308–320.
Bartos, M., Vida, I., Frotscher, M., Geiger, J.R., Jonas, P., 2001. Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J. Neurosci. 21(8), 2687–2698.
Bartos, M., Vida, I., Frotscher, M., Meyer, A., Monyer, H., Geiger, J.R., Jonas, P., 2002. Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc. Natl. Acad. Sci. USA 99(20), 13222–13227. >> doi:10.1073/pnas.192233099
Bibbig, A., Middleton, S., Racca, C., Gillies, M.J., Garner, H., Lebeau, F.E., Davies, C.H., Whittington, M.A., 2007. Beta rhythms (15–20 Hz) generated by nonreciprocal communication in hippocampus. J. Neurophysiol. 97(4), 2812–2823. >> doi:10.1152/jn.01105.2006
Chiappalone, M., Vato, A., Berdondini, L., Koudelka-Hep, M., Martinoia, S., 2007. Network dynamics and synchronous activity in cultured cortical neurons. Int. J. Neural. Syst. 17(2), 87–103. >> doi:10.1142/S0129065707000968
Del Percio, C., Le Pera, D., Arendt-Nielsen, L., Babiloni, C., Brancucci, A., Chen, A.C., De Armas, L., Miliucci, R., Restuccia, D., Valeriani, M., Rossini, P.M., 2006. Distraction affects frontal alpha rhythms related to expectancy of pain: An EEG study. Neuroimage 31(3), 1268–1277. >> doi:10.1016/j.neuroimage.2006.01.013
Engel, D., Endermann, U., Frahm, C., Heinemann, U., Draguhn, A., 2000. Acute effects of gamma-vinyl-GABA on low-magnesium evoked epileptiform activity in vitro. Epilepsy Res. 40(2–3), 99–107. >> doi:10.1016/S0920-1211(00)00112-1
Fries, P., Scheeringa, R., Oostenveld, R., 2008. Finding gamma. Neuron 58(3), 303–305. >> doi:10.1016/j.neuron.2008.04.020
Gulyas, A.I., Megias, M., Emri, Z., Freund, T.F., 1999. Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus. J. Neurosci. 19(22), 10082–10097.
Hines, M.L., Carnevale, N.T., 1997. The NEURON simulation environment. Neural Comput. 9(6), 1179–1209. >> doi:10.1162/neco.1997.9.6.1179
Hodgkin, A.L., Huxley, A.F., 1990. A quantitative description of membrane current and its application to conduction and excitation in nerve. 1952. Bull Math Biol 52(1–2), 25-71; discussion 25–23. >>doi.org/10.1007/BF02459568
>> doi:10.1016/S0092-8240(05)80004-7
Jeong, H.Y., Gutkin, B., 2007. Synchrony of neuronal oscillations controlled by GABAergic reversal potentials. Neural Comput. 19(3), 706–729. >> doi:10.1162/neco.2007.19.3.706
Kochubey, S.O., 2009. Features of synchronization coefficient calculation in neural networks [Osobennosti rascheta kojefficienta sinhronizacii nejronnyh setej] Vìsn. Dnìpropetr. Unìv. Ser. Bìol. Ekol. 17(5), 55–62.
Kochubey, S., Semyanov, A., Savtchenko, L., 2011. Network with shunting synapses as a non-linear frequency modulator. Neural Netw. 24(5), 407–416. >> doi:10.1016/j.neunet.2011.03.005
Kohling, R., Vreugdenhil, M., Bracci, E., Jefferys, J.G., 2000. Ictal epileptiform activity is facilitated by hippocampal GABAA receptor-mediated oscillations. J. Neurosci. 20(18), 6820–6829.
Maex, R., De Schutter, E., 2003. Resonant synchronization in heterogeneous networks of inhibitory neurons. J. Neurosci. 23(33), 10503–10514.
Matyas, F., Freund, T.F., Gulyas, A.I., 2004. Convergence of excitatory and inhibitory inputs onto CCK-containing basket cells in the CA1 area of the rat hippocampus. Eur. J. Neurosci. 19(5), 1243–1256. >> doi:10.1111/j.1460-9568.2004.03225.x
Sik, A., Penttonen, M., Ylinen, A., Buzsaki, G., 1995. Hippocampal CA1 interneurons: An in vivo intracellular labeling study. J. Neurosci. 15(10), 6651–6665.
Sik, A., Tamamaki, N., Freund, T.F., 1993. Complete axon arborization of a single CA3 pyramidal cell in the rat hippocampus, and its relationship with postsynaptic parvalbumin-containing interneurons. Eur. J. Neurosci. 5(12), 1719–1728. >> doi:10.1111/j.1460-9568.1993.tb00239.x
Tallon-Baudry, C., Bertrand, O., 1999. Oscillatory gamma activity in humans and its role in object representation. Trends Cogn. Sci. 3(4), 151–162. >> doi:10.1016/S1364-6613(99)01299-1
Tallon-Baudry, C., Bertrand, O., Delpuech, C., Permier, J., 1997. Oscillatory gamma-band (30–70 Hz) activity induced by a visual search task in humans. J. Neurosci. 17(2), 722–734.
Tallon-Baudry, C., Bertrand, O., Peronnet, F., Pernier, J., 1998. Induced gamma-band activity during the delay of a visual short-term memory task in humans. J. Neurosci. 18(11), 4244–4254.
Tiesinga, P.H., Jose, J.V., 2000. Synchronous clusters in a noisy inhibitory neural network. J. Comput. Neurosci. 9(1), 49–65. >> doi:10.1023/A:1008986311274
Traub, R.D., Whittington, M.A., Colling, S.B., Buzsaki, G., Jefferys, J.G., 1996. Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J. Physiol. 493(2), 471–484.
Turner, D.A., 1984. Segmental cable evaluation of somatic transients in hippocampal neurons (CA1, CA3, and dentate). Biophys. J. 46(1), 73–84. >> doi:10.1016/S0006-3495(84)84000-X
Van Der Werf, J., Jensen, O., Fries, P., Medendorp, W.P., 2008. Gamma-band activity in human posterior parietal cortex encodes the motor goal during delayed prosaccades and antisaccades. J. Neurosci. 28(34), 8397–8405. >> doi:10.1523/JNEUROSCI.0630-08.2008
Vida, I., Bartos, M., Jonas, P., 2006. Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates. Neuron 49(1), 107–117. >> doi:10.1016/j.neuron.2005.11.036
Wang, X.J., Buzsaki, G., 1996. Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J. Neurosci. 16(20), 6402–6413.
Published
2013-12-01
Section
Articles