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Dendritic encoding of sensory stimuli controlled by deep cortical interneurons

Abstract

The computational power of single neurons is greatly enhanced by active dendritic conductances1 that have a large influence on their spike activity2,3,4. In cortical output neurons such as the large pyramidal cells of layer 5 (L5), activation of apical dendritic calcium channels leads to plateau potentials that increase the gain of the input/output function5 and switch the cell to burst-firing mode6,7,8,9. The apical dendrites are innervated by local excitatory and inhibitory inputs as well as thalamic10,11,12,13 and corticocortical projections14,15,16, which makes it a formidable task to predict how these inputs influence active dendritic properties in vivo. Here we investigate activity in populations of L5 pyramidal dendrites of the somatosensory cortex in awake and anaesthetized rats following sensory stimulation using a new fibre-optic method17 for recording dendritic calcium changes. We show that the strength of sensory stimulation is encoded in the combined dendritic calcium response of a local population of L5 pyramidal cells in a graded manner. The slope of the stimulus–response function was under the control of a particular subset of inhibitory neurons activated by synaptic inputs predominantly in L5. Recordings from single apical tuft dendrites in vitro showed that activity in L5 pyramidal neurons disynaptically coupled via interneurons directly blocks the initiation of dendritic calcium spikes in neighbouring pyramidal neurons. The results constitute a functional description of a cortical microcircuit in awake animals that relies on the active properties of L5 pyramidal dendrites and their very high sensitivity to inhibition. The microcircuit is organized so that local populations of apical dendrites can adaptively encode bottom-up sensory stimuli linearly across their full dynamic range.

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Figure 1: Graded dendritic population Ca 2+ responses to somatosensory inputs in anaesthetized and awake rats.
Figure 2: Deep-layer control of dendritic activity.
Figure 3: Disynaptic inhibition blocks dendritic Ca2+ spikes in vitro.
Figure 4: Model of microcircuitry with all-or-none dendritic Ca 2+ spikes.

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Acknowledgements

We thank K. Martin, H.-R. Lüscher and Y. Kudo for their comments on the manuscript, O. Gschwend for support in the laboratory, D. Morris for software development, D. Limoges and J. Burkhalter for their expert technical support and K. Fischer for Neurolucida reconstructions of the biocytin-filled neurons. We also thank Sumitomo Electric Industries for their generous donation of the optical fibre. This work was supported by the Swiss National Science Foundation (grant no. PP00A-102721/1).

Author Contributions M.M. and M.E.L. designed the study. M.M. performed the periscope experiments in vivo, E.P.-G. performed the in vitro experiments, and T.N. and M.M. performed the in vivo two-photon experiments. W.S. and T.B. made the model and the supplementary model description. M.M. and M.E.L. prepared the manuscript.

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Correspondence to Matthew E. Larkum.

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This file contains Supplementary Figures 1-5 with Legends and Supplementary Data with Supplementary Figures M1-M7 with Legends, Supplementary Tables 1-2 and Supplementary References (PDF 829 kb)

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Murayama, M., Pérez-Garci, E., Nevian, T. et al. Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature 457, 1137–1141 (2009). https://doi.org/10.1038/nature07663

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