Lateral presynaptic inhibition mediates gain control in an olfactory circuit

Abstract

Olfactory signals are transduced by a large family of odorant receptor proteins, each of which corresponds to a unique glomerulus in the first olfactory relay of the brain. Crosstalk between glomeruli has been proposed to be important in olfactory processing, but it is not clear how these interactions shape the odour responses of second-order neurons. In the Drosophila antennal lobe (a region analogous to the vertebrate olfactory bulb), we selectively removed most interglomerular input to genetically identified second-order olfactory neurons. Here we show that this broadens the odour tuning of these neurons, implying that interglomerular inhibition dominates over interglomerular excitation. The strength of this inhibitory signal scales with total feedforward input to the entire antennal lobe, and has similar tuning in different glomeruli. A substantial portion of this interglomerular inhibition acts at a presynaptic locus, and our results imply that this is mediated by both ionotropic and metabotropic receptors on the same nerve terminal.

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Figure 1: Removing lateral input disinhibits projection neurons.
Figure 2: Lateral inhibition suppresses spontaneous EPSCs and scales with total ORN input.
Figure 3: Lateral GABAergic suppression of ORN–PN synapses.
Figure 4: Genetic evidence that GABA B receptors inhibit ORN–PN synapses at a presynaptic locus.
Figure 5: GABA receptor antagonists mimic removal of lateral input to a projection neuron.

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Acknowledgements

We thank K. Ito, L. Luo, G. Roman, D. P. Smith, L. M. Stevens and L. B. Vosshall for gifts of fly stocks. We thank G. Laurent, A. W. Liu and members of the Wilson laboratory for conversations. This work was funded by a grant from the NIDCD, the Pew, McKnight, Sloan, and Beckman Foundations (to R.I.W.). S.R.O. was partially supported by a NSF fellowship.

Author Contributions S.R.O. performed the experiments and analysed the data. S.R.O. and R.I.W. designed the experiments and wrote the paper.

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Correspondence to Rachel I. Wilson.

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Olsen, S., Wilson, R. Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452, 956–960 (2008). https://doi.org/10.1038/nature06864

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