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Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons

Nature Neuroscience volume 3, pages 366–371 (2000)Cite this article

Abstract

Networks of GABAergic interneurons are implicated in synchronizing cortical activity at gamma frequencies (30–70 Hz). Here we demonstrate that the combined electrical and GABAergic synaptic coupling of basket cells instantaneously entrained gamma-frequency postsynaptic firing in layers 2/3 of rat somatosensory cortex. This entrainment was mediated by rapid curtailment of gap junctional coupling potentials by GABAA receptor-mediated IPSPs. Electron microscopy revealed spatial proximity of gap junctions and GABAergic synapses on somata and dendrites. Electrical coupling alone entrained postsynaptic firing with a phase lag, whereas unitary GABAergic connections were ineffective in gamma-frequency phasing. These observations demonstrate precise spatiotemporal mechanisms underlying action potential timing in oscillating interneuronal networks.

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Figure 1: Differential modulation of postsynaptic firing by presynaptic gamma-frequency activity in two interneuron–interneuron connections.
Figure 2: Electron microscopic evidence for gap junctions between cortical interneurons.
Figure 3: A single presynaptic GABAergic neuron can synchronize postsynaptic firing at gamma-frequency by conjoint action of neighboring gap junctions and chemical synapses (Fig. 4).
Figure 4: Identification of interneurons involved in conjoint electrical and synaptic interaction as shown in Fig. 3.
Figure 5: Classification of postsynaptic interneuron firing behavior by cluster analysis of firing probability in response to gamma-frequency presynaptic firing.

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Acknowledgements

We thank N. Kogo, G. Maccaferri and O. Paulsen for scientific advice and technical help and J. D. B. Roberts and P. Jays for technical assistance. This work was also supported by the James S. McDonnell Foundation (EESI grant No 97-39), the Wellcome Trust, a European Commission Shared Cost RTD Program (No. BIO4CT96-0585) and the Hungarian Scientific Research Fund. G. T. was a Zoltán Magyary and OTKA Scholar during part of this project.

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  1. Eberhard H. Buhl

    Present address: School of Biomedical Sciences, University of Leeds, Worsley Building, Leeds, LS2 9NQ, UK

Authors and Affiliations

  1. Department of Comparative Physiology, University of Szeged, Középfasor 52, H-6726, Szeged, Hungary

    Gábor Tamás & Andrea Lörincz

  2. University Department of Pharmacology, MRC Anatomical Neuropharmacology Unit, University of Oxford, Mansfield Road, Oxford, OX1 3TH, UK

    Gábor Tamás, Eberhard H. Buhl, Andrea Lörincz & Peter Somogyi

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Correspondence to Gábor Tamás.

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Tamás, G., Buhl, E., Lörincz, A. et al. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat Neurosci 3, 366–371 (2000). https://doi.org/10.1038/73936

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