Abstract
Encoding of information in the cortex is thought to depend on synchronous firing of cortical neurons1,2. Inhibitory neurons are known to be critical in the coordination of cortical activity3,4,5, but how interaction among inhibitory cells promotes synchrony is not well understood4,6,7,8,9,10,11,12. To address this issue directly, we have recorded simultaneously from pairs of fast-spiking (FS) cells, a type of γ-aminobutyric acid (GABA)-containing neocortical interneuron13. Here we report a high occurrence of electrical coupling among FS cells. Electrical synapses were not found among pyramidal neurons or between FS cells and other cortical cells. Some FS cells were interconnected by both electrical and GABAergic synapses. We show that communication through electrical synapses allows excitatory signalling among inhibitory cells and promotes their synchronous spiking. These results indicate that electrical synapses establish a network of fast-spiking cells in the neocortex which may play a key role in coordinating cortical activity.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Singer,W. & Gray,C. M. Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18, 555–586 (1995).
Ritz,R. & Sejnowski,T. J. Synchronous oscillatory activity in sensory systems: new vistas on mechanisms. Curr. Opin. Neurobiol. 7, 536–546 (1997).
Lytton,W. W. & Sejnowski,T. J. Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. J. Neurophysiol. 66, 1059–1079 (1991).
Whittington,M. A., Traub,R. D. & Jefferys,J. G. R. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373, 612–615 (1995).
Cobb,S. R., Buhl,E. H., Halasy,K., Paulsen,O. & Somogyi,P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378, 75–78 (1995).
Michelson,H. B. & Wong,R. K. S. Synchronization of inhibitory neurones in the guinea-pig hippocampus in vitro. J. Physiol. (Lond.) 477, 35–45 (1994).
Jefferys,J. G. R., Traub,R. D. & Whittington,M. A. Neuronal networks for induced ‘40 Hz’ rhythms. Trends Neurosci. 19, 202–208 (1996).
Strata,F. et al. A pacemaker current in dye-coupled hilar interneurons contributes to the generation of giant GABAergic potentials in developing hippocampus. J. Neurosci. 17, 1435–1446 (1997).
Benardo,L. S. Recruitment of GABAergic inhibition and synchronization of inhibitory interneurons in rat neocortex. J. Neurophysiol. 77, 3134–3144 (1997).
Tamás,G., Somogyi,P. & Buhl,E. H. Differentially interconnected networks of GABAergic interneurons in the visual cortex of the cat. J. Neurosci. 18, 4255–4270 (1998).
Rinzel,J., Terman,D., Wang,X.-J. & Ermentrout,B. Propagating activity patterns in large-scale inhibitory neuronal networks. Science 279, 1351–1355 (1998).
Zhang,Y. et al. Slow oscillations (≤1 Hz) mediated by GABAergic interneuronal networks in rat hippocampus. J. Neurosci. 18, 9256–9268 (1998).
Kawaguchi,Y. & Kubota,Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7, 476–486 (1997).
Kawaguchi,Y. & Kubota,Y. Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J. Neurophysiol. 70, 387–396 (1993).
Kawaguchi,Y. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J. Neurosci. 15, 2638–2655 (1995).
Galarreta,M. & Hestrin,S. Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nature Neurosci. 1, 587–594 (1998).
Angulo,M. C., Staiger,J. F., Rosier,J. & Audinat,E. Developmental synaptic changes increase the range of integrative capabilities of an identified excitatory neocortical connection. J. Neurosci. 19, 1566–1576 (1999).
Cauli,B. et al. Molecular and physiological diversity of cortical nonpyramidal cells. J. Neurosci. 17, 3894–3906 (1997).
Neyton,J. & Trautmann,A. Single-channel currents of an intercellular junction. Nature 317, 331–335 (1985).
Hubel,D. H. Single unit activity in striate cortex of unrestrained cats. J. Physiol. 147, 226–238 (1959).
Connors,B. W., Benardo,L. S. & Prince,D. A. Coupling between neurons of the developing rat neocortex. J. Neurosci. 3, 773–782 (1983).
Peinado,A., Yuste,R. & Katz,L. C. Extensive dye coupling between rat neocortical neurons during the period of circuit formation. Neuron 10, 103–114 (1993).
Sloper,J. J. Gap junctions between dendrites in the primate neocortex. Brain Res. 44, 641–646 (1972).
Katsumaru,H., Kosaka,T., Heizmann,C. W. & Hama,K. Gap junctions on GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus (CA1 region). Exp. Brain Res. 72, 363–370 (1988).
Bragin,A. et al. Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat. J. Neurosci. 15, 47–60 (1995).
Buhl,E. H., Tamás,G. & Fisahn,A. Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J. Physiol. (Lond.) 513, 117–126 (1998).
Wang,X.-J. & Buzsáki,G. Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J. Neurosci. 16, 6402–6413 (1996).
Traub,R. D., Whittington,M. A., Stanford,I. M. & Jefferys,J. G. R. A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383, 621–624 (1996).
Bush,P. & Sejnowski,T. Inhibition synchronizes sparsely connected cortical neurons within and between columns in realistic networks models. J. Comput. Neurosci. 3, 91–110 (1996).
Stevens,C. F. & Zador,A. M. Input synchrony and the irregular firing of cortical neurons. Nature Neurosci. 1, 210–217 (1998</
Acknowledgements
We thank M. Chang for technical assistance. S.H. was supported by an NIH grant.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Galarreta, M., Hestrin, S. A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402, 72–75 (1999). https://doi.org/10.1038/47029
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/47029
This article is cited by
-
Spatial Distribution of Parvalbumin-Positive Fibers in the Mouse Brain and Their Alterations in Mouse Models of Temporal Lobe Epilepsy and Parkinson’s Disease
Neuroscience Bulletin (2023)
-
The role of inhibitory circuits in hippocampal memory processing
Nature Reviews Neuroscience (2022)
-
Mean-Field Models for EEG/MEG: From Oscillations to Waves
Brain Topography (2022)
-
Highly unstable heterogeneous representations in VIP interneurons of the anterior cingulate cortex
Molecular Psychiatry (2022)
-
Pyramidal cell subtype-dependent cortical oscillatory activity regulates motor learning
Communications Biology (2021)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.