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Layer-specific modulation of neocortical dendritic inhibition during active wakefulness

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Science  03 Mar 2017:
Vol. 355, Issue 6328, pp. 954-959
DOI: 10.1126/science.aag2599

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Layer-specific interneuron activity

Somatostatin-expressing interneurons are an important group of inhibitory neurons in the brain that target and thus control the dendrites of pyramidal cells. These interneurons have recently been shown to play a role in sensorimotor integration, reinforcement encoding, and selective attention. Muñoz et al. used channelrhodopsin-assisted patching to investigate the spatiotemporal pattern of neocortical dendritic inhibition in vivo. They were able to record the activity of somatostatin-expressing interneurons in all neocortical layers in behaving mice. The results provide a framework for understanding the changes in dendritic inhibition that take place in the neocortex during active behaviors. This framework is very distinct from the view obtained from previous recordings that were restricted to interneurons in the superficial layers of the neocortex.

Science, this issue p. 954

Abstract

γ-Aminobutyric acid (GABA)ergic inputs are strategically positioned to gate synaptic integration along the dendritic arbor of pyramidal cells. However, their spatiotemporal dynamics during behavior are poorly understood. Using an optical-tagging electrophysiological approach to record and label somatostatin-expressing (Sst) interneurons (GABAergic neurons specialized for dendritic inhibition), we discovered a layer-specific modulation of their activity in behaving mice. Sst interneuron subtypes, residing in different cortical layers and innervating complementary laminar domains, exhibited opposite activity changes during transitions to active wakefulness. The relative weight of vasoactive intestinal peptide–expressing (Vip) interneuron–mediated inhibition of distinct Sst interneurons and cholinergic modulation determined their in vivo activity. These results reveal a state-dependent laminar influence of Sst interneuron–mediated inhibition, with implications for the compartmentalized regulation of dendritic signaling in the mammalian neocortex.

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