Nature 457, 1137-1141 (26 February 2009) | doi:10.1038/nature07663; Received 31 July 2008; Accepted 18 November 2008; Published online 18 January 2009

Dendritic encoding of sensory stimuli controlled by deep cortical interneurons

Masanori Murayama1, Enrique Pérez-Garci1, Thomas Nevian1, Tobias Bock1, Walter Senn1 & Matthew E. Larkum1

  1. Physiologisches Institut, Universität Bern, Bühlplatz 5, CH-3012 Bern, Switzerland

Correspondence to: Matthew E. Larkum1 Correspondence and requests for materials should be addressed to M.E.L. (Email: larkum@pyl.unibe.ch).

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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