nach oben

Journal of Computational Neuroscience

Erschienen in:

01.12.2009

Generating oscillatory bursts from a network of regular spiking neurons without inhibition

verfasst von: Jing Shao, Dihui Lai, Ulrike Meyer, Harald Luksch, Ralf Wessel

Erschienen in: Journal of Computational Neuroscience | Ausgabe 3/2009

Einloggen

Aktivieren Sie unsere intelligente Suche, um passende Fachinhalte oder Patente zu finden.

search-config

KI-gestützte Suche

Aus

Abstract

Avian nucleus isthmi pars parvocellularis (Ipc) neurons are reciprocally connected with the layer 10 (L10) neurons in the optic tectum and respond with oscillatory bursts to visual stimulation. Our in vitro experiments show that both neuron types respond with regular spiking to somatic current injection and that the feedforward and feedback synaptic connections are excitatory, but of different strength and time course. To elucidate mechanisms of oscillatory bursting in this network of regularly spiking neurons, we investigated an experimentally constrained model of coupled leaky integrate-and-fire neurons with spike-rate adaptation. The model reproduces the observed Ipc oscillatory bursting in response to simulated visual stimulation. A scan through the model parameter volume reveals that Ipc oscillatory burst generation can be caused by strong and brief feedforward synaptic conductance changes. The mechanism is sensitive to the parameter values of spike-rate adaptation. In conclusion, we show that a network of regular-spiking neurons with feedforward excitation and spike-rate adaptation can generate oscillatory bursting in response to a constant input.

Vorheriger Artikel Crossover inhibition in the retina: circuitry that compensates for nonlinear rectifying synaptic transmission

Nächster Artikel Recurrent networks with short term synaptic depression

Sie haben noch keine Lizenz? Dann Informieren Sie sich jetzt über unsere Produkte:

Springer Professional "Wirtschaft+Technik"

Online-Abonnement

Mit Springer Professional "Wirtschaft+Technik" erhalten Sie Zugriff auf:

über 102.000 Bücher
über 537 Zeitschriften

aus folgenden Fachgebieten:

Automobil + Motoren
Bauwesen + Immobilien
Business IT + Informatik
Elektrotechnik + Elektronik
Energie + Nachhaltigkeit
Finance + Banking
Management + Führung
Marketing + Vertrieb
Maschinenbau + Werkstoffe
Versicherung + Risiko

Jetzt Wissensvorsprung sichern!

Jetzt informieren

Springer Professional "Wirtschaft"

Online-Abonnement

Mit Springer Professional "Wirtschaft" erhalten Sie Zugriff auf:

über 67.000 Bücher
über 340 Zeitschriften

aus folgenden Fachgebieten:

Bauwesen + Immobilien
Business IT + Informatik
Finance + Banking
Management + Führung
Marketing + Vertrieb
Versicherung + Risiko

Jetzt Wissensvorsprung sichern!

Jetzt informieren

Springer Professional "Technik"

Online-Abonnement

Mit Springer Professional "Technik" erhalten Sie Zugriff auf:

über 67.000 Bücher
über 390 Zeitschriften

aus folgenden Fachgebieten:

Automobil + Motoren
Bauwesen + Immobilien
Business IT + Informatik
Elektrotechnik + Elektronik
Energie + Nachhaltigkeit
Maschinenbau + Werkstoffe

Jetzt Wissensvorsprung sichern!

Jetzt informieren

Nur mit Berechtigung zugänglich

Abbott, L. F., & Dayan, P. (1999). The effect of correlated variability on the accuracy of a population code. Neural Computation, 11, 91–101.CrossRefPubMed

Averbeck, B. B., Latham, P. E., & Pouget, A. (2006). Neural correlations, population coding and computation. Nature Reviews Neuroscience, 7, 358–366.CrossRefPubMed

Bagnoli, P., Fontanesi, G., Alesci, R., & Erichsen, J. (1992). Distribution of neuopeptide Y, substance P, and choline acetyltransferase in the developing visual system of the pigeon and effects of unilateral retina removal. Journal of Comparative Neurology, 318, 392–414.CrossRefPubMed

Brandt, S. F., & Wessel, R. (2007). Winner-take-all selection in a neural system with delayed feedback. Biol Cybernetics, 97, 221–228.CrossRef

Brandt, S. F., Pelster, A., & Wessel, R. (2006). Variational calculation of the limit cycle and its frequency in a two-neuron model with delay. Phys Rev E, 74, 036201.CrossRef

Brandt, S. F., Pelster, A., & Wessel, R. (2007). Synchronization in a neuronal feedback loop through asymmetric temporal delays. Europhysics Letters, 79, 38001.CrossRef

Britto, L. R., Keyser, K. T., Lindstrom, J. M., & Karten, H. J. (1992). Immunohistochemical localization of nicotinic acetylcholine receptor subunits in the mesencephalon and diencephalon of the chick (Gallus gallus). Journal of Comparative Neurology, 317, 325–340.CrossRefPubMed

Brown, D. A., Gähwiler, B. H., Griffith, W. H., & Halliwell, J. V. (1990). Membrane currents in hippocampal neurons. Progress in Brain Research, 83, 141–160.CrossRefPubMed

Brownstone, R. M. (2006). Beginning at the end: repetitive firing properties in the final common pathway. Progress in Neurobiology, 78, 156–172.CrossRefPubMed

Buzsaki, G. (2006). Rhythms of the brain. Oxford University Press.

Chacron, M. J., & Bastian, J. (2008). Population coding by electrosensory neurons. Journal of Neurophysiology, 99, 1825–1835.CrossRefPubMed

Chacron, M. J., Longtin, A., & Maler, L. (2005). Delayed excitatory and inhibitory feedback shape neural information transmission. Physical Review E, 72, 051917.CrossRef

Chance, F. S., Abbott, L. F., & Reyes, A. D. (2002). Gain modulation from background synaptic input. Neuron, 35, 773–782.CrossRefPubMed

Cook, R. G. (2001). Avian visual cognition. Available on-line at: www.pigeon.psy.tufts.edu/avc/.

Coombes, S., & Bressloff, P. C. (2005). Bursting: The genesis of rhythm in the nervous system. World Scientific.

Crick, F., & Koch, C. (1998). Constraints on cortical and thalamic projections: the no-strong-loops hypothesis. Nature, 391, 245–250.CrossRefPubMed

Destexhe, A., & Contreras, D. (2006). Neuronal computations with stochastic network states. Science, 314, 85–90.CrossRefPubMed

Destexhe, A., & Rudolph, M. (2009). Neuronal noise. Springer.

Destexhe, A., Mainen, Z. F., & Sejnowski, T. J. (1994). Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. Journal of Computational Neuroscience, 1, 195–230.CrossRefPubMed

Doiron, B., Chacron, M. J., Maler, L., Longtin, A., & Bastian, J. (2003). Inhibitory feedback required for network oscillatory responses to communication but not to prey stimuli. Nature, 421, 539–543.CrossRefPubMed

Doiron, B., Oswald, A. M. M., & Maler, L. (2007). Interval coding. II. Dendrite-dependent mechanisms. Journal of Neurophysiology, 97, 2744–2757.CrossRefPubMed

Dudkin, E. A., & Gruberg, E. R. (2003). Nucleus isthmi enhances calcium influx into optic nerve fiber terminals in Rana pipiens. Brain Research, 969, 44–52.CrossRefPubMed

Dye, J. C., & Karten, H. J. (1996). An in vitro study of retinotectal transmission in the chick: role of glutamate and GABA in evoked field potentials. Visual Neuroscience, 13, 747–758.CrossRefPubMed

Feller, M. B. (1999). Spontaneous correlated activity in developing neural circuits. Neuron, 22, 653–656.CrossRefPubMed

Fox, M. D., Snyder, A. Z., Zacks, J. M., & Raichle, M. E. (2006). Coherent spontaneous activity accounts for trial-to-trial variability in human evoked brain responses. Nature Neuroscience, 9, 23–25.CrossRefPubMed

Gabbiani, F., Metzner, W., Wessel, R., & Koch, C. (1996). From stimulus encoding to feature extraction in weakly electric fish. Nature, 384, 564–567.CrossRefPubMed

Gruberg, E. R., Hughes, T. E., & Karten, H. J. (1994). Synaptic interrelationships between the optic tectum and ipsilateral nucleus isthmi in Rana pipiens. Journal of Comparative Neurology, 339, 353–364.CrossRefPubMed

Hansel, D., Mato, G., & Meunier, C. (1995). Synchrony in excitatory neural networks. Neural Computation, 7, 307–337.CrossRefPubMed

Hellmann, B., Manns, M., & Güntürkün, O. (2001). Nucleus isthmi, pars semilunaris as a key component of the tectofugal visual system in pigegons. Journal of Comparative Neurology, 436, 153–166.CrossRefPubMed

Higgs, M. H., & Spain, W. J. (2009). Conditional bursting enhances resonant firing in neocortical layer 2–3 pyramidal neurons. Journal of Neuroscience, 29, 1285–1299.CrossRefPubMed

Holden, A. L. (1980). Field potentials evoked in the avian optic tectum by diffuse and punctiform luminous stimuli. Experimental Brain Research, 39, 427–432.

Izhikevich, E. M. (2007). Dynamical systems in neuroscience: The geometry of excitability and bursting. Cambridge: The MIT.

Izhikevich, E. M., Desai, N. S., Walcott, E. C., & Hoppensteadt, F. C. (2003). Bursts as a unit of neural information: selective communication via resonance. Trends in Neuroscience, 26, 161–167.CrossRef

Jolivet, R., Lewis, T. J., & Gerstner, W. (2004). Generalized integrate-and-fire models of neuronal activity approximate spike trains of a detailed model to a high degree of accuracy. Journal of Neurophysiology, 92, 959–976.CrossRefPubMed

Kawai, H., Lazar, R., & Metherate, R. (2007). Nicotinic control of axon excitability regulates thalamocortical transmission. Nature Neuroscience, 10, 1168–1175.CrossRefPubMed

Khanbabaie, R., Mahani, A., & Wessel, R. (2007). Contextual interaction of GABAergic circuitry with dynamic synapses. Journal of Neurophysiology, 97, 2802–2811.CrossRefPubMed

Knudsen, E. I. (1982). Auditory and visual maps of spaces in the optic tectum of the owl. Journal of Neuroscience, 2, 1177–1194.PubMed

Koch, C. (1999). Biophysics of computation: Information processing in single neurons (pp. 85–116). Oxford University Press: New York.

Kohn, A. (2007). Visual adaptation: physiology, mechanisms, and functional benefits. Journal of Neurophysiology, 97, 3155–3164.CrossRefPubMed

Krahe, R., & Gabbiani, F. (2004). Burst firing in sensory systems. Nature Review Neuroscience, 5, 13–23.CrossRef

Laing, C. R., & Longtin, A. (2003). Dynamics of deterministic and stochastic paired excitatory–inhibitory delayed feedback. Neural Computation, 15, 2779–2822.CrossRefPubMed

Lesica, N. A., & Stanley, G. B. (2004). Encoding of natural scene movies by tonic and burst spikes in the lateral geniculate nucleus. Journal of Neuroscience, 24, 10731–10740.CrossRefPubMed

Letelier, J. C., Mpodozis, J., Marin, G., Morales, D., Rozas, C., Madrid, C. (2000). Spatiotemporal profile of synaptic activation produced by the electrical and visual stimulation of retinal inputs to the optic tectum: a current source density analysis in the pigeon (Columbia livia). European Journal of Neuroscience, 12, 47–57.CrossRefPubMed

Lewis, D. V., Huguenard, J. R., Anderson, W. W., & Wilson, W. A. (1986). Membrane currents underlying bursting pacemaker activity and spike frequency adaptation in invertebrates. Advances in Neurology, 44, 235–261.PubMed

Lisman, J. (1997). Bursts as a unit of neural information: making unreliable synapses reliable. Trends in Neuroscience, 20, 38–43.CrossRef

Luksch, H., & Golz, S. (2003). Anatomy and physiology of horizontal cells in layer 5b of the chicken optic tectum. Journal of Chemical Neuroanatomy, 25, 185–194.CrossRefPubMed

Luksch, H., Cox, K., & Karten, H. J. (1998). Bottlebrush dendritic endings and large dendritic fields: motion-detecting neurons in the tectofugal pathway. Journal of Comparative Neurology, 396, 399–414.CrossRefPubMed

Luksch, H., Karten, H. J., Kleinfeld, D., & Wessel, R. (2001). Chattering and differential signal processing in identified motion sensitive neurons of parallel visual pathways in chick tectum. Journal of Neuroscience, 21, 6440–6446.PubMed

Luksch, H., Khanbabaie, R., & Wessel, R. (2004). Synaptic dynamics mediate sensitivity to motion independent of stimulus details. Nature Neuroscience, 7, 380–388.CrossRefPubMed

Maczko, K. A., Knudsen, P. F., & Knudsen, E. I. (2006). Auditory and visual space maps in the cholinergic nucleus isthmi pars parvocellularis in the barn owl. Journal of Neuroscience, 26, 12799–12806.CrossRefPubMed

Mahani, A. S., Khanbabaie, R., Luksch, H., & Wessel, R. (2006). Sparse spatial sampling for the computation of motion in multiple stages. Biological Cybernetics, 94, 276–287.CrossRefPubMed

Marder, E., & Calabrese, R. (1996). Principles of rhythmic motor pattern generation. Physiological Reviews, 76, 687–717.PubMed

Marin, G., Letelier, J. C., Henny, P., Sentis, E., Farfan, G., Fredes, F. (2003). Spatial organization of the pigeon tecto-rotundal pathway: An interdigitating topographic arrangement. Journal of Comparative Neurology, 458, 361–380.CrossRefPubMed

Marin, G., Mpdozis, J., Sentis, E., Ossandon, T., & Letelier, J. C. (2005). Oscillatory bursts in the optic Tectum of birds represent re-entrant signals from the nucleus isthmi pars parvocellularis. Journal of Neuroscience, 25, 7081–7089.CrossRefPubMed

Marin, G., Salas, C., Sentic, E., Rojas, X., Letelier, J. C., & Mpodozis, J. (2007). A cholinergic gating mechanism controlled by competitive interactions in the optic tectum of the pigeon. Journal of Neuroscience, 27, 8112–8121.CrossRefPubMed

McCormick, D. A., & Huguenard, J. R. (1992). A model of the electrophysiological properties of thalamocortical relay neurons. Journal of Neurophysiology, 68, 1384–1400.PubMed

Medina, L., & Reiner, A. (1994). Distribution of choline acetyltransferase immunoreativity in the pigeon brain. Journal of Comparative Neurology, 342, 497–537.CrossRefPubMed

Meyer, U., Shao, J., Chakrabarty, S., Brandt, S. F., Luksch, H., & Wessel, R. (2008). Distributed delays stabilize neural feedback systems. Biological Cybernetics, 99, 79–87.CrossRefPubMed

Milton, J. (1996). Dynamics of small neural populations. CRM Monograph Series.

Nesse, W. H., Borisyuk, A., & Bressloff, P. C. (2008). Fluctuation-driven rhythmogenesis in an excitatory neuronal network with slow adaptation. Journal of Computational Neuroscience, 25, 317–333.CrossRefPubMed

Neuenschwander, S., & Varela, F. J. (1993). Visually triggered neuronal oscillations in the pigeon: an autocorrelation study of tectal activity. European Journal of Neuroscience, 5, 870–881.CrossRefPubMed

Neuenschwander, S., Engel, A. K., Konig, P., Singer, W., & Varela, F. J. (1996). Synchronization of neuronal responses in the optic tectum of awake pigeons. Visual Neuroscience, 13, 575–584.CrossRefPubMed

O’Donovan, M. J. (1999). The origin of spontaneous activity in developing networks of the vertebrate nervous system. Current Opinion in Neurobiology, 9, 94–104.CrossRefPubMed

Oswald, A. M., Chacron, M. J., Doiron, B., Bastian, J., & Maler, L. (2004). Parallel processing of sensory input by bursts and isolated spikes. Journal of Neuroscience, 24, 4351–4362.CrossRefPubMed

Paninski, L., Pillow, J. W., & Simoncelli, E. P. (2004). Maximum likelihood estimation of a stochastic integrate-and-fire neural encoding model. Neural Computation, 16, 2533–2561.CrossRefPubMed

Pillow, J. W., Paninski, L., Uzzell, V. J., Simoncelli, E. P., & Chichilnisky, E. J. (2005). Prediction and decoding of retinal ganglion cell responses with a probabilistic spiking model. Journal of Neuroscience, 25, 11003–11013.CrossRefPubMed

Reinagel, P., Godwin, D., Sherman, S. M., & Koch, C. (1999). Encoding of visual information by LGN bursts. Journal of Neurophysiology, 81, 2558–2569.PubMed

Rinzel, J., & Ermentrout, B. (1998). Analysis of neural excitability and oscillations. In C. Koch & I. Segev (Eds.), Methods of neuronal modeling: From Synapses to networks (2nd ed., pp. 252–291). Cambridge: Bradford.

Sargent, P. B., Pike, S. H., Nadel, D. B., & Lindstrom, J. M. (1989). Nicotinic acetylcholine receptor-like molecules in the retina, retinotectal pathway, and optic tectum of the frog. Journal of Neuroscience, 9, 565–573.PubMed

Schnitzler, A., & Gross, J. (2005). Normal and pathological oscillatory communication in the brain. Nature Reviews Neuroscience, 6, 285–296.CrossRefPubMed

Sereno, M. I., & Ulinski, P. S. (1987). Caudal topographic nucleus isthmi and the rostral nontopographic nucleus isthmi in the turtle, Pseudemys scripta. Journal of Comparative Neurology, 261, 319–346.CrossRefPubMed

Sherk, H. (1979). A comparison of visual-response properties in cat’s parabigeminal nucleus and superior colliculus. Journal of Neurophysiology, 42, 1640–1655.PubMed

Sherman, S. M. (2001). Tonic and burst firing: dual modes of thalamocortical relay. Trends in Neurosciences, 24, 122–126.CrossRefPubMed

Sillito, A. M., & Jones, H. E. (2002). Corticothalamic interactions in the transfer of visual information. The Philosophical Transactions of the Royal Society B, 357, 1739–1752.CrossRef

Smith, J. C., Ellenberger, H. H., Ballanyi, K., Richter, D. W., & Feldman, J. L. (1991). Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science, 254, 726–729.CrossRefPubMed

Sorenson, E. M., Parkinson, D., Dahl, J. L., & Chiappinelli, V. A. (1989). Immunohistochemical localization of choline acetyltransferase in the chicken mesencephalon. Journal of Comparative Neurology, 281, 641–657.CrossRefPubMed

Storm, J. F. (1990). Potassium currents in hippocampal pyramidal cells. Progress in Brain Research, 83, 161–187.CrossRefPubMed

Tabak, J., & Rinzel, J. (2005). Bursting in excitatory neural networks. In: S. Coombes, & P. C. Bressloff (Eds.), Bursting: The genesis of rhythm in the nervous system. Hackensack World Scientific, pp. 273–301.

Tabak, J., Senn, W., O’Donovan, M. J., & Rinzel, J. (2000). Modeling of spontaneous activity in developing spinal cord using activity-dependent depression in an excitatory network. Journal of Neuroscience, 20, 3041–3056.PubMed

Traub, R. D., Bibbig, A., LeBeau, F. E. N., Buhl, E. H., & Whittington, M. A. (2004). Cellular mechanisms of neuronal population oscillations in the hippocampus in vitro. Annual Review of Neuroscience, 27, 247–248.CrossRefPubMed

Van Vreeswijk, C., & Hansel, D. (2001). Patterns of synchrony in neural networks with spike adaptation. Neural Computation, 13, 959–992.CrossRefPubMed

Vladimirski, B. B., Tabak, J., O’Donovan, M. J., & Rinzel, J. (2008). Episodic activity in a heterogeneous excitatory network, from spiking neurons to mean field. Journal of Computational Neuroscience, 25, 39–63.CrossRefPubMed

Wang, X. J. (1994). Multiple dynamic modes of thalamic relay neurons: rhythmic bursting and intermittent phase-locking. Neuroscience, 59, 21–31.CrossRefPubMed

Wang, S. R. (2003). The nucleus isthmi and dual modulation of the receptive field of tectal neurons in non-mammals. Brain Research Reviews, 41, 13–25.CrossRefPubMed

Wang, X. J., & Rinzel, J. (2003). Oscillatory and bursting properties of neurons. In: M. A. Arbib (ed.), Handbook of brain theory and neural networks. MIT, pp. 835–840.

Wang, Y., Major, D. E., & Karten, H. J. (2004). Morphology and connections of nucleus isthmi pars magnocellularis in chicks (gallus gallus). Journal of Comparative Neurology, 469, 275–297.CrossRefPubMed

Wang, Y., Luksch, H., Brecha, N. C., & Karten, H. J. (2006). Columnar projections from the cholinergic nucleus isthmi to the optic tectum in chicks (gallus gallus): a possible substrate for synchronizing tectal channels. Journal Comparative Neurology, 494, 7–35.CrossRef

Wolfart, J., Debay, D., LeMasson, G., Destexhe, A., & Bal, T. (2005). Synaptic background activity controls spike transfer from thalamus to cortex. Nature Neuroscience, 8, 1760–1767.CrossRefPubMed

Zhan, X. J., Cox, C., Rinzel, J., & Sherman, S. M. (1999). Current clamp and modeling studies of low threshold calcium spikes in cells of the cat’s lateral geniculate nucleus. Journal of Neurophysiology, 81, 2360–2373.PubMed

Titel: Generating oscillatory bursts from a network of regular spiking neurons without inhibition
verfasst von: Jing Shao
Dihui Lai
Ulrike Meyer
Harald Luksch
Ralf Wessel
Publikationsdatum: 01.12.2009
Verlag: Springer US
Erschienen in: Journal of Computational Neuroscience / Ausgabe 3/2009
Print ISSN: 0929-5313
Elektronische ISSN: 1573-6873
DOI: https://doi.org/10.1007/s10827-009-0171-5

Springer Professional

Abstract

Bitte loggen Sie sich ein, um Zugang zu Ihrer Lizenz zu erhalten.

Sie haben noch keine Lizenz? Dann Informieren Sie sich jetzt über unsere Produkte:

Springer Professional "Wirtschaft+Technik"

Springer Professional "Wirtschaft"

Springer Professional "Technik"

Weitere Artikel der Ausgabe 3/2009

Dissecting cooperative calmodulin binding to CaM kinase II: a detailed stochastic model

Variability of bursting patterns in a neuron model in the presence of noise

Crossover inhibition in the retina: circuitry that compensates for nonlinear rectifying synaptic transmission

Transitions to spike-wave oscillations and epileptic dynamics in a human cortico-thalamic mean-field model

Derivation of cable parameters for a reduced model that retains asymmetric voltage attenuation of reconstructed spinal motor neuron dendrites

Implications of gain modulation in brainstem circuits: VOR control system