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J Neurosci. 2017 Feb 1;37(5):1117-1138. doi: 10.1523/JNEUROSCI.2880-16.2016. Epub 2016 Dec 21.

Olfactory Bulb Deep Short-Axon Cells Mediate Widespread Inhibition of Tufted Cell Apical Dendrites.

Author information

1
Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213.
2
Center for the Neural Basis of Cognition, Pittsburgh, Pennsylvania 15213, and.
3
Department of Neurobiology and.
4
Center for Neuroscience, University of Pittsburgh, Pittsburgh, Pennsylvania 15213.
5
Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, nurban@pitt.edu.

Abstract

In the main olfactory bulb (MOB), the first station of sensory processing in the olfactory system, GABAergic interneuron signaling shapes principal neuron activity to regulate olfaction. However, a lack of known selective markers for MOB interneurons has strongly impeded cell-type-selective investigation of interneuron function. Here, we identify the first selective marker of glomerular layer-projecting deep short-axon cells (GL-dSACs) and investigate systematically the structure, abundance, intrinsic physiology, feedforward sensory input, neuromodulation, synaptic output, and functional role of GL-dSACs in the mouse MOB circuit. GL-dSACs are located in the internal plexiform layer, where they integrate centrifugal cholinergic input with highly convergent feedforward sensory input. GL-dSAC axons arborize extensively across the glomerular layer to provide highly divergent yet selective output onto interneurons and principal tufted cells. GL-dSACs are thus capable of shifting the balance of principal tufted versus mitral cell activity across large expanses of the MOB in response to diverse sensory and top-down neuromodulatory input.

SIGNIFICANCE STATEMENT:

The identification of cell-type-selective molecular markers has fostered tremendous insight into how distinct interneurons shape sensory processing and behavior. In the main olfactory bulb (MOB), inhibitory circuits regulate the activity of principal cells precisely to drive olfactory-guided behavior. However, selective markers for MOB interneurons remain largely unknown, limiting mechanistic understanding of olfaction. Here, we identify the first selective marker of a novel population of deep short-axon cell interneurons with superficial axonal projections to the sensory input layer of the MOB. Using this marker, together with immunohistochemistry, acute slice electrophysiology, and optogenetic circuit mapping, we reveal that this novel interneuron population integrates centrifugal cholinergic input with broadly tuned feedforward sensory input to modulate principal cell activity selectively.

KEYWORDS:

acetylcholine; chrna2; inhibition; interneuron; olfaction; olfactory bulb

PMID:
28003347
PMCID:
PMC5296792
DOI:
10.1523/JNEUROSCI.2880-16.2016
[Indexed for MEDLINE]
Free PMC Article

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