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The Journal of Neuroscience, September 15, 2004, 24(37):8057-8067; doi:10.1523/JNEUROSCI.2138-04.2004

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Cellular/Molecular
Dopamine Inhibits Mitral/Tufted Granule Cell Synapses in the Frog Olfactory Bulb

Ian G. Davison, Jamie D. Boyd, and Kerry R. Delaney

Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, Canada V5A 1S6

Synaptic interactions between the dendrites of mitral/tufted (MT) and granule cells (GCs) in the olfactory bulb are important for the determination of spatiotemporal firing patterns of MTs, which form an odor representation passed to higher brain centers. These synapses are subject to modulation from several sources originating both within and outside the bulb. We show that dopamine, presumably released by TH-positive local interneurons, reduces synaptic transmission from MTs to GCs. MT neurons express D2-like receptors (D2Rs), and both dopamine and the D2 agonist quinpirole decrease EPSC amplitude at the MT GC synapse. D2R activation also increases paired pulse facilitation and decreases the frequency of action potential-independent spontaneous miniature EPSCs in GCs, consistent with an effect on MT glutamate release downstream from Ca²⁺ influx. Analysis of spike-evoked Ca²⁺ transients in MT lateral dendrites additionally shows that quinpirole reduces Ca²⁺ influx preferentially at distal locations, possibly by reducing dendritic excitability via increased transient K⁺ channel availability. When the OB is activated physiologically by using odor stimuli, blocking D2Rs increases the power of GABA_A-dependent oscillations in the local field potential. This demonstrates a functional role for the dopaminergic circuit during normal odor-evoked responses and for the modulation of dendritic release and excitability in neuronal circuit function. Regulation of spike invasion of lateral dendrites by transient K⁺ currents also may provide a mechanism for local outputs of MTs to be controlled dynamically via other neuromodulators or by postsynaptic potentials.

Key words: reciprocal synapse; mitral cell; lateral dendrite; feedback inhibition; D2; Rana pipiens

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Received June 2, 2004; revised July 19, 2004; accepted July 20, 2004.

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