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The organization of two new cortical interneuronal circuits

A Corrigendum to this article was published on 22 November 2013

This article has been updated

Abstract

Deciphering the interneuronal circuitry is central to understanding brain functions, yet it remains a challenging task in neurobiology. Using simultaneous quadruple-octuple in vitro and dual in vivo whole-cell recordings, we found two previously unknown interneuronal circuits that link cortical layer 1–3 (L1–3) interneurons and L5 pyramidal neurons in the rat neocortex. L1 single-bouquet cells (SBCs) preferentially formed unidirectional inhibitory connections on L2/3 interneurons that inhibited the entire dendritic-somato-axonal axis of 1% of L5 pyramidal neurons located in the same column. In contrast, L1 elongated neurogliaform cells (ENGCs) frequently formed mutual inhibitory and electric connections with L2/3 interneurons, and these L1-3 interneurons inhibited the distal apical dendrite of >60% of L5 pyramidal neurons across multiple columns. Functionally, SBC→L2/3 interneuron→L5 pyramidal neuronal circuits disinhibited and ENGC↔L2/3 interneuron→L5 pyramidal neuronal circuits inhibited the initiation of dendritic complex spikes in L5 pyramidal neurons. As dendritic complex spikes can serve coincidence detection, these cortical interneuronal circuits may be essential for salience selection.

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Figure 1: L1 interneurons SBCs and ENGCs differ in preferential spiking patterns.
Figure 2: L1–3 interneurons form two distinct inhibitory circuits.
Figure 3: SBCs form inhibitory circuits in single columns.
Figure 4: ENGCs form inhibitory circuits across multiple columns.
Figure 5: L2/3 interneurons exhibit distinctive axonal arborization patterns.
Figure 6: L2/3 interneurons target different compartments of L5 pyramidal neurons.
Figure 7: SBC→ and ENGC↔L2/3I→L5 pyramidal neuronal circuits serve different functions.
Figure 8: SBC→ and ENGC↔L2/3I→L5 pyramidal neuronal circuits differ in function in vivo.

Change history

  • 03 March 2013

    In the version of this article initially published, in Figure 8a under L1 Spontaneous, the last 400 ms of trace 4 was a duplicate of trace 3; for Figure 8c, the legend referred to a scale bar of 2 mV instead of 4 mV; in Figure 8e, incidence on the y axis was plotted in units of 0–0.8 Hz instead of 0–4%; and in Figure 7b the insets were not described. The insets show the sequences of soma/axon-dendrite-soma/axon-initiated events in the dendritic complex spikes at a timescale expanded by a factor of 2.5, with arrows indicating the timing of initiation of the dendritic slow potentials and second somatic action potentials. The errors have been corrected in the HTML and PDF versions of the article.

  • 03 March 2013

    In the version of this supplementary file originally posted online, in Supplementary Figure 7a under SBC, the last 400 ms of trace 3 was a duplicate of trace 2; also, the corresponding legend referred to main-text Figure 7a,b instead of to Figure 8a,b. The errors have been corrected in this file as of 3 March 2013.

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Acknowledgements

We thank E. Callaway, A. Erisir, J. Huang, J. Kapur and G. Tamas for technical advice and invaluable discussions, and members of the Zhu laboratory for comments and technical assistance. This study was supported in part by a postdoctoral fellowship from the Epilepsy Foundation (X.J.), a small research grant from the College of Arts and Sciences of the University of Virginia (A.J.L.) and the US National Institutes of Health.

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Contributions

X.J., G.W. and J.J.Z. designed and developed the mechanics (X.J. and J.J.Z.), electronics and software programs (G.W. and J.J.Z.) for the stable octuple whole-cell recording technology. X.J., G.W., R.L.S. and J.J.Z. developed the immunostaining, neuronal morphology and/or ultrastructural analysis procedures. X.J., G.W., A.J.L. and J.J.Z. performed the experiments and data analysis. X.J., G.W., A.J.L., R.L.S. and J.J.Z. wrote the manuscript.

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Correspondence to J Julius Zhu.

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Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–8 and Supplementary Tables 1–4 (PDF 1981 kb)

Supplementary Movie 1

3D reconstruction reveals distinguished axonal anatomy of SBCs and ENGCs. (AVI 5394 kb)

Supplementary Movie 2

3D reconstruction reveals distinguished axonal anatomy of L2/3 interneurons. (AVI 20012 kb)

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Jiang, X., Wang, G., Lee, A. et al. The organization of two new cortical interneuronal circuits. Nat Neurosci 16, 210–218 (2013). https://doi.org/10.1038/nn.3305

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