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The Journal of Neuroscience, November 1, 1999, 19(21):9180-9191
Multiple and Opposing Roles of Cholinergic Transmission in the
Main Olfactory Bulb
Pablo E.
Castillo1, 2,
Alan
Carleton1,
Jean-Didier
Vincent1, and
Pierre-Marie
Lledo1
1 Centre National de la Recherche Scientifique,
Institut Alfred Fessard, 91198 Gif-sur-Yvette Cedex, France, and
2 Departamento de Fisiologia, Facultad de Medicina,
Universidad de la Republica, 11800 Montevideo, Uruguay
The main olfactory bulb is a critical relay step between the
olfactory epithelium and the olfactory cortex. A marked feature of the
bulb is its massive innervation by cholinergic inputs from the basal
forebrain. In this study, we addressed the functional interaction
between cholinergic inputs and intrinsic bulbar circuitry. Determining
the roles of acetylcholine (ACh) requires the characterization of
cholinergic effects on both neural excitability and synaptic transmission. For this purpose, we used electrophysiological techniques to localize and characterize the diverse roles of ACh in mouse olfactory bulb slices. We found that cholinergic inputs have a surprising number of target receptor populations that are expressed on
three different neuronal types in the bulb. Specifically, nicotinic acetylcholine receptors excite both the output neurons of the bulb,
i.e., the mitral cells, as well as interneurons located in the
periglomerular regions. These nicotine-induced responses in
interneurons are short lasting, whereas responses in mitral cells are
long lasting. In contrast, muscarinic receptors have an inhibitory
effect on the firing rate of interneurons from a deeper layer, granule
cells, while at the same time they increase the degree of
activity-independent transmitter release from these cells onto mitral cells.
Cholinergic signaling thus was found to have multiple and opposing
roles in the olfactory bulb. These dual cholinergic effects on mitral
cells and interneurons may be important in modulating olfactory bulb
output to central structures required for driven behaviors and may be
relevant to understanding mechanisms underlying the perturbations of
cholinergic inputs to cortex that occur in Alzheimer's disease.
Key words:
mitral cells; inhibitory interneurons; basal forebrain; GABA; nicotinic receptors; muscarinic receptors; olfaction
Copyright © 1999 Society for Neuroscience 0270-6474/99/19219180-12$05.00/0
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