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The Journal of Neuroscience, October 5, 2005, 25(40):9069-9079; doi:10.1523/JNEUROSCI.2070-05.2005

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Behavioral/Systems/Cognitive
Role of GABAergic Inhibition in Shaping Odor-Evoked Spatiotemporal Patterns in the Drosophila Antennal Lobe

Rachel I. Wilson^1,2 and Gilles Laurent²

¹Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115, and ²Division of Biology 139-74, California Institute of Technology, Pasadena, California 92115

Drosophila olfactory receptor neurons project to the antennal lobe, the insect analog of the mammalian olfactory bulb. GABAergic synaptic inhibition is thought to play a critical role in olfactory processing in the antennal lobe and olfactory bulb. However, the properties of GABAergic neurons and the cellular effects of GABA have not been described in Drosophila, an important model organism for olfaction research. We have used whole-cell patch-clamp recording, pharmacology, immunohistochemistry, and genetic markers to investigate how GABAergic inhibition affects olfactory processing in the Drosophila antennal lobe. We show that many axonless local neurons (LNs) in the adult antennal lobe are GABAergic. GABA hyperpolarizes antennal lobe projection neurons (PNs) via two distinct conductances, blocked by a GABA_A- and GABA_B-type antagonist, respectively. Whereas GABA_A receptors shape PN odor responses during the early phase of odor responses, GABA_B receptors mediate odor-evoked inhibition on longer time scales. The patterns of odor-evoked GABA_B-mediated inhibition differ across glomeruli and across odors. Finally, we show that LNs display broad but diverse morphologies and odor preferences, suggesting a cellular basis for odor- and glomerulus-dependent patterns of inhibition. Together, these results are consistent with a model in which odors elicit stimulus-specific spatial patterns of GABA release, and as a result, GABAergic inhibition increases the degree of difference between the neural representations of different odors.

Key words: olfactory; antennal lobe; GABA; GABA_B receptor; synaptic transmission; interneurons

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Received May 23, 2005; revised August 24, 2005; accepted August 25, 2005.

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