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The Journal of Neuroscience, July 1, 2009, 29(26):8595-8603; doi:10.1523/JNEUROSCI.1455-09.2009

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Behavioral/Systems/Cognitive
Odor-Evoked Neural Oscillations in Drosophila Are Mediated by Widely Branching Interneurons

Nobuaki K. Tanaka,¹ Kei Ito,² and Mark Stopfer¹

¹National Institute of Child Health and Human Development–National Institutes of Health, Bethesda, Maryland 20892, and ²Institute of Molecular and Cellular Biosciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-0032, Japan

Correspondence should be addressed to Mark Stopfer, National Institute of Child Health and Human Development–National Institutes of Health, 35 Lincoln Drive, MSC 3715, Bethesda, MD 20892. Email: stopferm{at}mail.nih.gov

Stimulus-evoked oscillatory synchronization of neurons has been observed in a wide range of species. Here, we combined genetic strategies with paired intracellular and local field potential (LFP) recordings from the intact brain of Drosophila to study mechanisms of odor-evoked neural oscillations. We found common food odors at natural concentrations elicited oscillations in LFP recordings made from the mushroom body (MB), a site of sensory integration and analogous to the vertebrate piriform cortex. The oscillations were reversibly abolished by application of the GABA_a blocker picrotoxin. Intracellular recordings from local and projection neurons within the antennal lobe (AL) (analogous to the olfactory bulb) revealed odor-elicited spikes and subthreshold membrane potential oscillations that were tightly phase locked to LFP oscillations recorded downstream in the MBs. These results suggested that, as in locusts, odors may elicit the oscillatory synchronization of AL neurons by means of GABAergic inhibition from local neurons (LNs). An analysis of the morphologies of genetically distinguished LNs revealed two populations of GABAergic neurons in the AL. One population of LNs innervated parts of glomeruli lacking terminals of receptor neurons, whereas the other branched more widely, innervating throughout the glomeruli, suggesting that the two populations might participate in different neural circuits. To test the functional roles of these LNs, we used the temperature-sensitive dynamin mutant gene shibire to conditionally and reversibly block chemical transmission from each or both of these populations of LNs. We found only the more widely branching population of LNs is necessary for generating odor-elicited oscillations.

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Received March 26, 2009; revised May 4, 2009; accepted June 3, 2009.

Correspondence should be addressed to Mark Stopfer, National Institute of Child Health and Human Development–National Institutes of Health, 35 Lincoln Drive, MSC 3715, Bethesda, MD 20892. Email: stopferm{at}mail.nih.gov

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