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Alpha-Frequency Rhythms Desynchronize over Long Cortical Distances: A Modeling Study

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Abstract

Neocortical networks of excitatory and inhibitory neurons can display alpha(α)-frequency rhythms when an animal is in a resting or unfocused state. Unlike some γ- and β-frequency rhythms, experimental observations in cats have shown that these α-frequency rhythms need not synchronize over long cortical distances. Here, we develop a network model of synaptically coupled excitatory and inhibitory cells to study this asynchrony. The cells of the local circuit are modeled on the neurons found in layer V of the neocortex where α-frequency rhythms are thought to originate. Cortical distance is represented by a pair of local circuits coupled with a delay in synaptic propagation. Mathematical analysis of this model reveals that the h and T currents present in layer V pyramidal (excitatory) cells not only produce and regulate the α-frequency rhythm but also lead to the occurrence of spatial asynchrony. In particular, these inward currents cause excitation and inhibition to have nonintuitive effects in the network, with excitation delaying and inhibition advancing the firing time of cells; these reversed effects create the asynchrony. Moreover, increased excitatory to excitatory connections can lead to further desynchronization. However, the local rhythms have the property that, in the absence of excitatory to excitatory connections, if the participating cells are brought close to synchrony (for example, by common input), they will remain close to synchrony for a substantial time.

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References

  • Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ (1998) Cellular and network models for intrathalamic augmenting responses during 10 Hz stimulation. J. Neurophysiol.79:2730-2748.

    Google Scholar 

  • Bose A, Kopell N, Terman D (2000) Almost-synchronous solutions for mutually coupled excitatory neurons. Physica D 140:69-94.

    Google Scholar 

  • Bressler SL, Coppola R, Nakamura R (1993) Episodic multiregional cortical coherence at multiple frequencies during visual task performance. Nature 366:153-156.

    Google Scholar 

  • Castro-Alamancos MA, Connors BW (1996) Cellular mechanisms of the augmenting response: Short-term plasticity in a thalamocotrical pathway. J. Neurosci. 16(23):7742-7756.

    Google Scholar 

  • Castro-Alamancos MA, Connors BW (1996) Short-term plasticity of a thalamacortical pathway dynamically modulated by behavioral state. Science, reprint series, 272:274-277.

    Google Scholar 

  • Connors BW, Amitai Y (1997) Making waves in the neocortex. Neuron 18:347-349.

    Google Scholar 

  • Contreras D, Destexhe A, Sejnowski TJ, Steriade M (1996) Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback. Science 274:771-774.

    Google Scholar 

  • Contreras D, Destexhe A, Sejnowski TJ, Steriade M (1998) Spatiotemporal patterns of spindle oscillations in cortex and thalamus. J. Neurosci. 17(3):1179-1196.

    Google Scholar 

  • Crook SM, Ermentrout GB, Bower JM (1998) Spike frequency adaptation affects the synchronization properties of networks of cortical oscillators. Neural. Comput. 10:837-854.

    Google Scholar 

  • da Silva, LF (1991) Neural mechanisms underlying brain waves: From neural membranes to networks. Electroenceph. Clin. Neurophysiol. 79:81-93.

    Google Scholar 

  • Destexhe A, Babloyantz A, Sejnowski TJ (1993) Ionic mechanisms for intrinsic slow oscillations in thalamic relay neurons. Biophys. J. 65:1538-1552.

    Google Scholar 

  • Destexhe A, Bal T, McCormick DA, Sejnowski TJ (1996) Ionic mechanisms underlying synchronized oscillations and propagating waves in a model of ferret thalamic slices. J. Neurophysiol. 76(3):2049-2070.

    Google Scholar 

  • Destexhe A, Mainen ZF, Sejnowski TJ (1998) Kinetic models of synaptic transmission. In Koch C, Segev I, eds., Methods in Neuronal Modeling (2nd ed.). MIT Press, Cambridge, MA.

    Google Scholar 

  • Destexhe A, Sejnowski TJ (1997) Synchronized oscillations in thalamic networks: Insights from modeling studies. In: Steriade M, Jones EG, McCormick DA, eds., Thalamus: Organization and Function, vol. 1. Elsevier, Oxford.

    Google Scholar 

  • Devaney RL (1992) A First Course in Chaotic Dynamical Systems: Theory and Experiment. Addison-Wesley, Reading, MA.

    Google Scholar 

  • Ermentrout GB, Kopell N (1998) Fine structure of neural spiking and synchronization in the presence of conduction delays. Proc. Natl. Acad. Sci. U.S.A. Neurobiology 95:1259-1264.

    Google Scholar 

  • Farmer SF (1998) Rhythmicity, synchronization and binding in human and primate motor systems. J. Physiol. 509.1:3-14.

    Google Scholar 

  • Flint AC, Connors BW (1996) Two types of network oscillations in neocortex mediated by distinct glutamate receptor subtypes and neuronal populations. J. Neurophysiol. 75(2):951-956.

    Google Scholar 

  • Fries P, Roelfsema PR, Engel AK, König P, Singer W (1997) Synchronization of oscillatory responses in visual cortex correlates with perception in interocular rivalry. Proc. Natl. Acad. Sci. U.S.A. Neurobiol. 94:12699-12704.

    Google Scholar 

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

    Google Scholar 

  • Hansel D, Mato G, Meunier G (1995) Synchrony in excitatory neural networks. Neural Comput. 7:307-337.

    Google Scholar 

  • Hirsh JA, Gilbert CD (1991) Synaptic physiology of horizontal connections in the cat's visual cortex. J. Neurosci. 11(6):1800-1809.

    Google Scholar 

  • Huguenard JR, McCormick DA, Sejnowski TJ (1995) A model of spike initiation in neocortical pyramidal neurons. Neuron 15:1427-1439.

    Google Scholar 

  • McCormick DA, Huguenard JR (1992) A model of the electrophysiological properties of thalamocortical relay neurons. J. Neurophysiol. 68(4):1384-1400.

    Google Scholar 

  • McCormick DA, Pape HC (1990b) Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurons. J. Physiol. 431:291-318.

    Google Scholar 

  • McCormick DA, Pape HC (1990a) Noradrenergic and serotonergic modulation of a hyperpolarization-activation cation current in thalamic relay neurons. J. Physiol. 431:319-342.

    Google Scholar 

  • Pinsky PF, Rinzel J (1994). Intrinsic and network rhythmogenesis in a reduced Traub model for CA3 neurons. J. Comput. Neuro. 1:39-60.

    Google Scholar 

  • Roelfsema P, Engel AK, König P, Singer W (1997) Visuomotor integration is associated with zero time-lag synchronization among cortical areas. Nature 385:157-161.

    Google Scholar 

  • Rubin JE, Terman D (2000) Geometric analysis of population rhythms in synaptically coupled neuronal networks. Neural Comput. 12(3):597-648.

    Google Scholar 

  • Silva LR, Amitai Y, Connors BW (1991) Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. Science 251:432-435.

    Google Scholar 

  • Steriade M, Deschenes M (1984) The thalamus as a neuronal oscillator. Brain Res. Rev. 8:1-63.

    Google Scholar 

  • Terman D, Bose A, Kopell N (1996) Functional reorganization in thalamocortical networks: Transition between spindling and delta sleep rhythms. Proc. Natl. Acad. Sci. USA 93:15417-15422.

    Google Scholar 

  • Traub RD, Whittington MA, Buhl EH, Jefferys JGR, Faulkner HJ (1999) On the mechanism of the γ-β frequency shift in neuronal oscillations induced in rat hippocampal slices by tetanic stimulation. J. Neurosci. 19:1088-1105.

    Google Scholar 

  • Traub RD, Whittington MA, Stanford IM, Jefferys JGR (1996) A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383:621-624.

    Google Scholar 

  • Van Vreeswijk C, Abbott LF, Ermentrout GB (1994) When inhibition not excitation synchronizes neural firing. J. Comp. Neurosci. 1:313-321.

    Google Scholar 

  • von Stein A, Chiang C, König P (1999) The role of alpha and gamma frequency interactions in top-down processing in the cat. Soc. Neurosci. Abstr. 24.

  • von Stein A, Rappelsberger P, Sarnthein J, Petsche H (1999) Synchronization between temporal and parietal cortex during multimodal object processing in man. Cerebral Cortex 9:137-150.

    Google Scholar 

  • Wang XJ, Golomb D, Rinzel J (1995) Emergent spindle oscillations and intermittent burst firing in a thalamic model: Specific neuronal mechanisms. Proc. Natl. Acad. Sci. USA 92:5577-5581.

    Google Scholar 

  • White EL (1989) Cortical Circuits: Synaptic Organization of the Cerebral Cortex. Birkhäuser Boston, Boston.

    Google Scholar 

  • Wong RK, Traub RD, Miles R (1986) Cellular basis of neuronal synchrony in epilepsy. Adv. Neurol. 44:583-593.

    Google Scholar 

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Jones, S.R., Pinto, D.J., Kaper, T.J. et al. Alpha-Frequency Rhythms Desynchronize over Long Cortical Distances: A Modeling Study. J Comput Neurosci 9, 271–291 (2000). https://doi.org/10.1023/A:1026539805445

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