Scientific Understanding of Consciousness
Dendritic Encoding of Sensory Stimuli by Cortical Interneurons
Nature 457, 1137-1141 (26 February 2009)
Dendritic encoding of sensory stimuli controlled by deep cortical interneurons
Masanori Murayama, Enrique Pérez-Garci, Thomas Nevian, Tobias Bock, Walter Senn & Matthew E. Larkum
Physiologisches Institut, Universität Bern, Bühlplatz 5, CH-3012 Bern, Switzerland
The computational power of single neurons is greatly enhanced by active dendritic conductances that have a large influence on their spike activity. 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 function and switch the cell to burst-firing mode. The apical dendrites are innervated by local excitatory and inhibitory inputs as well as thalamic and corticocortical projections, 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 method 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.
Conscious perception involves a combination of feed-forward and feedback processes that may specifically influence dendritic encoding.
We conclude that the representation of sensory stimuli by cortical output neurons requires active dendrites embedded within highly specialized cortical microcircuitry. Dendritic activity is tightly controlled by interneurons projecting from deep to upper layers (Martinotti cells). These neurons dynamically modulate the slope and threshold of the dendritic response function to match the physiologically relevant input range.
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