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Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons

Abstract

At the first stage of olfactory processing in the brain, synchronous firing across glomeruli may help to temporally bind multiple and spatially distributed input streams activated by a given odor. This hypothesis, however, has never been tested in an organism in which the odor-tuning properties of several spatially identifiable glomeruli are known. Using the sphinx moth, an insect that meets these specific criteria, we recorded odor-evoked responses simultaneously from pairs of projection neurons (PNs) innervating the same or different glomeruli in the macroglomerular complex (MGC), which is involved in processing pheromonal information. PNs that branched in the same glomerulus and were activated by the same pheromone component also showed the strongest coincident responses to each odor pulse. Glomerulus-specific PN pairs were also inhibited by the pheromone component that selectively activated PNs in the neighboring glomerulus, and about 70% of all intraglomerular pairs showed increased synchronization when stimulated with a mixture of the two odorants. Thus, when two adjacent glomeruli receive their inputs simultaneously, the temporal tuning of output from each glomerulus is enhanced by reciprocal and inhibitory interglomerular interactions.

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Figure 1: PNs innervating the same glomerulus responded selectively to the same odorant and showed stimulus-synchronized responses to repetitive stimulation.
Figure 2: Time-series analysis of responses to repeated odor pulses recorded simultaneously from pairs of PNs.
Figure 3: Time course of synchronous firing between PNs.
Figure 4: Blend-enhanced synchronization of PNs innervating the same glomerulus.
Figure 5: Correlation between PNs in one glomerulus is modulated by inhibitory input from the neighboring glomerulus.

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Acknowledgements

We thank K. Daly, V. Pawlowski and B. Smith for discussions and comments and H. Stein and A.A. Osman for technical assistance. Supported by grants and contracts from National Institutes of Health (NIDCD).

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Correspondence to Thomas A. Christensen.

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Lei, H., Christensen, T. & Hildebrand, J. Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons. Nat Neurosci 5, 557–565 (2002). https://doi.org/10.1038/nn0602-859

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