Skip to main content
Log in

Dynamics of Spiking Neurons Connected by Both Inhibitory and Electrical Coupling

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

We study the dynamics of a pair of intrinsically oscillating leaky integrate-and-fire neurons (identical and noise-free) connected by combinations of electrical and inhibitory coupling. We use the theory of weakly coupled oscillators to examine how synchronization patterns are influenced by cellular properties (intrinsic frequency and the strength of spikes) and coupling parameters (speed of synapses and coupling strengths). We find that, when inhibitory synapses are fast and the electrotonic effect of the suprathreshold portion of the spike is large, increasing the strength of weak electrical coupling promotes synchrony. Conversely, when inhibitory synapses are slow and the electrotonic effect of the suprathreshold portion of the spike is small, increasing the strength of weak electrical coupling promotes antisynchrony (see Fig. 10). Furthermore, our results indicate that, given a fixed total coupling strength, either electrical coupling alone or inhibition alone is better at enhancing neural synchrony than a combination of electrical and inhibitory coupling. We also show that these results extend to moderate coupling strengths.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alvarez VA, Chow CC, VanBockstaele EJ, Williams JT (2002) Frequency-dependent synchrony in the locus ceruleus: Role of electrical coupling. Proc. Natl. Acad. Sci. USA 99: 4032-4036.

    Article  PubMed  Google Scholar 

  • Amitai Y, Gibson JR, Beierlein M, Patrick SL, Ho AM, Connors BW, Golumb D (2002) Spatial dimensions of electrically coupled networks of interneurons in neocortex. J. Neurosci. 22: 4142-4152.

    PubMed  Google Scholar 

  • Beierlein M, Gibson JR, Connors BW (2000) A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat. Neurosci. 3: 904-910.

    Article  PubMed  Google Scholar 

  • Bem T, LeFeuvre Y, Simmers J, Meyrand P (2002) Electrical coupling can prevent expression of adult-like properties in an embryonic neural circuit. J. Neurophysiol. 87: 538-547.

    PubMed  Google Scholar 

  • Benardo LS (1997) Recruitment of GABAergic inhibition and synchronization of inhibitory interneurons in rat neocortex. J. Neurophysiol. 77: 3134-3144.

    PubMed  Google Scholar 

  • Bressloff PC, Coombes S (1997) Synchrony in an array of integrate-and-fire neurons with dendritic structure. Phys. Rev. Lett. 78: 4665-4668.

    Article  Google Scholar 

  • Bressloff PC, Coombes S (2000) A dynamical theory of spike train transitions in networks of integrate-and-fire oscillators. SIAM J. Appl. Math. 60: 820-841.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Buzsáki G, Chrobak JJ (1995) Temporal structure in spatially organized neuronal ensembles: A role for interneuronal networks. Curr. Opin. Neurobiol. 5: 504-510.

    Article  PubMed  Google Scholar 

  • Chow CC (1998) Phase-locking in weakly heterogeneous neuronal networks. Physica D 118: 343-370.

    Google Scholar 

  • Chow CC, Kopell N (2000) Dynamics of spiking neurons with electrical coupling. Neural Comp. 12: 1643-1678.

    Article  Google Scholar 

  • Crook SM, Ermentrout GB, Bower JM (1998) Dendritic and synaptic effects in systems of coupled cortical oscillators. J. Comput. Neurosci. 5: 315-329.

    Article  PubMed  Google Scholar 

  • Erisir A, Lau D, Rudy B, Leonard S (1999) Function of specific K + channels in sustained high-frequency firing of fast-spiking neocortical cells. J. Neurophysiol. 82: 2476-2489.

    PubMed  Google Scholar 

  • Ermentrout GB (1996) Type I Membranes, phase resetting curves and synchrony. Neural Comp. 8: 979-1001.

    Google Scholar 

  • Ermentrout GB, Kleinfeld D (2001) Traveling electrical waves in cortex: Insights from phase dynamics and speculation on computational role. Neuron 29: 33-44.

    Article  PubMed  Google Scholar 

  • Ermentrout GB, Kopell N (1991) Multiple pulse interation and averaging in coupled neural oscillators. J. Math. Biol. 29: 195-217.

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Fisahn A, Pike F, Buhl EH, Paulsen O (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394: 186-189.

    Article  PubMed  Google Scholar 

  • Galarreta M, Hestrin S (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402: 72-75.

    Article  PubMed  Google Scholar 

  • Galarreta M, Hestrin S (2001a) Electrical synapses between GABAreleasing interneurons. Nat. Rev. Neurosci. 2: 425-433.

    Article  PubMed  Google Scholar 

  • Galarreta M, Hestrin S (2001b) Spike transmission and synchrony detection in networks of GABAergic interneurons. Science 292: 2295-2299.

    Article  PubMed  Google Scholar 

  • Gerstner W (1995) Time structure of the activity in neural network models. Phys. Rev. E 51: 738-758.

    Article  Google Scholar 

  • Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402: 75-79.

    Article  PubMed  Google Scholar 

  • Golomb D, Hansel D, Mato G (2001) Mechanisms of synchrony of neural activity in large networks. In: F Moss, S Gielen, eds. Handbook of Biological Physics, Vol. 4: Neuro-Informatics and Neural Modelling. Elsevier, Amsterdam. pp. 887-968.

    Google Scholar 

  • Golomb D, Wang X, Rinzel J (1994) Synchronization properties of spindle oscillations in a thalamic reticular nucleus model. J. Neurophysiol. 72: 1109-1126.

    PubMed  Google Scholar 

  • Grannan ER, Kleinfeld D, Sompolinsky H (1993) Stimulus dependent synchronization of neuronal assemblies. Neural Comp. 5: 550-569.

    Google Scholar 

  • Gupta A, Wang Y, Markram H (2000) Organization principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287: 273-278.

    Article  PubMed  Google Scholar 

  • Han SK, Kurrer C, Kuramoto Y (1995) Dephasing and bursting in coupled neural oscillators. Phys. Rev. Lett. 75: 3190-3193.

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Kopell N (1988) Toward a theory of modeling central pattern generators. In: A Cohen, ed. Neural Control of Rhythmic Movements in Vertebrates. John Wiley, New York. pp. 396-413.

    Google Scholar 

  • Kuramoto Y (1984) Chemical Oscillations, Waves, and Turbulence. Springer-Verlag, Berlin.

    Google Scholar 

  • Lewis TJ, Gibson JR, Connors BW, Rinzel J (2001) Dynamics of neurons connected by inhibitory and electrical synapses. Society for Neuroscience Abstract 504: 16.

    Google Scholar 

  • McBain CJ, Fisahn A (2001) Interneurons unbound. Nat. Rev. Neurosci. 2: 11-23.

    Article  PubMed  Google Scholar 

  • Michelson HB, Wong RK (1994) Synchronization of inhibitory neurones in the guinea-pig hippocampus in vitro. J. Physiol. (Lond) 92: 35-45.

    Google Scholar 

  • Neltner L, Hansel D, Mato G, Meunier C (2000) Synchrony in hetergeneous networks of spiking neurons. Neural Comp. 12: 1607-1641.

    Article  Google Scholar 

  • Oviedo H, Reyes AD (2002) Boosting of neuronal firing evoked with asynchronous and synchronous inputs in the dendrite. Nat. Neurosci. 5: 261-266.

    Article  PubMed  Google Scholar 

  • Rinzel J, Ermentrout GB (1998) Analysis of neural excitability and oscillations. In: C Koch, I Segev, eds. Methods in Neuronal Modeling: From Synapse to Networks. MIT Press, Cambridge, MA. pp. 251-292.

    Google Scholar 

  • Ritz R, Sejnowski TJ (1997) Synchronous oscillatory activity in sensory systems: New vistas on mechanism. Curr. Opin. Neurobiol. 7: 536-546.

    Article  PubMed  Google Scholar 

  • Sherman A, Rinzel J (1994) Rhythmogenic effects of weak electrotonic coupling in neuronal models. Proc. Natl. Acad. Sci. USA 89: 2471-2474.

    Google Scholar 

  • Skinner FK, Zhang Y, Velazquez JLP, Carlen PL (1999) Bursting in inhibitory interneuronal networks: A role for gap-junctional coupling. J. Neurophysiol. 81: 1274-1283.

    PubMed  Google Scholar 

  • Stuart G, Sakmann B (1995) Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron 15: 1065-1076.

    Article  PubMed  Google Scholar 

  • Swadlow HA, Beloozerova IN, Sirota MG (1998) Sharp, local synchrony among putative feed-forward inhibitory interneurons of rabbit somatosensory cortex. J. Neurophysiol. 79: 567-582.

    PubMed  Google Scholar 

  • Tamás G, Buhl EH, Lörinz A, Somogyi P (2000) Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat. Neurosci. 3: 366-371.

    Article  PubMed  Google Scholar 

  • Traub RD (1995) Model of synchronized population bursts in electrically coupled interneurons containing active dendrites. J. Comput. Neurosci. 2: 283-289.

    PubMed  Google Scholar 

  • Traub RD, Kopell N, Bibbig A, Buhl EH, LeBeau FEN, Whittington MA (2001) Gap junctions between interneuron dendrites can enhance synchrony of gamma oscillations in distibuted networks. J. Neurosci. 21: 9478-9488.

    PubMed  Google Scholar 

  • Usher M, Cohen JD, Servan-Schreiber D, Rajkowski J, Aston-Jones G (1999) The role of Locus Coeruleus in the regulation of cognitive performance. Science 283: 549-554.

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Various (1999) Reviews on the binding problem. Neuron 24: 7-125.

    Article  PubMed  Google Scholar 

  • Wang X, Buzsáki G (1996) Gamma oscillations by synaptic inhibition in an interneuronal network model. J. Neurosci. 16: 6402-6413.

    PubMed  Google Scholar 

  • Wang X, Rinzel J (1992) Alternating and synchronous rhythms in reciprocally inhibitory model neurons. Neural Comp. 4: 84-97.

    Google Scholar 

  • White JA, Chow CC, Ritt J, Soto-Trevino C, Kopell N (1998) Synchronization and oscillatory dynamics in heterogeneous, mutually inhibitory neurons. J. Comput. Neurosci. 5: 5-16.

    Article  PubMed  Google Scholar 

  • Whittington MA, Standford IM, Traub RD, Jefferys JG (1997) Spatiotemporal patterns of gamma frequency oscillations tetanically induced in the rat hippocampual slice. J. Physiol. (Lond) 502: 591-602.

    Article  Google Scholar 

  • Whittington MA, Traub RD, Jefferys JG (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373: 612-615.

    Article  PubMed  Google Scholar 

  • Ylinen A, Bragin A, Nádasdy Z, Jandó G, Szabó I, Sik A, Buzsáki G (1995) Sharp wave-associated high-frequency oscillations (200 Hz) in the intact hippocampus: Network and intracellular mechanisms. J. Neurosci. 15: 30-46.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lewis, T.J., Rinzel, J. Dynamics of Spiking Neurons Connected by Both Inhibitory and Electrical Coupling. J Comput Neurosci 14, 283–309 (2003). https://doi.org/10.1023/A:1023265027714

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1023265027714

Navigation