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Origins of correlated activity in an olfactory circuit

Abstract

Multineuronal recordings often reveal synchronized spikes in different neurons. The manner in which correlated spike timing affects neural codes depends on the statistics of correlations, which in turn reflects the connectivity that gives rise to correlations. However, determining the connectivity of neurons recorded in vivo can be difficult. We investigated the origins of correlated activity in genetically labeled neurons of the Drosophila antennal lobe. Dual recordings showed synchronized spontaneous spikes in projection neurons (PNs) postsynaptic to the same type of olfactory receptor neuron (ORN). Odors increased these correlations. The primary origin of correlations lies in the divergence of each ORN onto every PN in its glomerulus. Reciprocal PN–PN connections make a smaller contribution to correlations and PN spike trains in different glomeruli were only weakly correlated. PN axons from the same glomerulus reconverge in the lateral horn, where pooling redundant signals may allow lateral horn neurons to average out noise that arises independently in these PNs.

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Figure 1: Homotypic PNs produce correlated spikes.
Figure 2: Correlations in spontaneous activity.
Figure 3: Correlations in odor-evoked activity.
Figure 4: Each PN receives input from all the ORNs in its glomerulus.
Figure 5: Short-term depression correlates the amplitudes of synchronous EPSCs.
Figure 6: Central circuits contribute to correlated noise.
Figure 7: PNs in the same glomerulus are reciprocally connected.
Figure 8: Axonal projections of homotypic PNs.

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Acknowledgements

We thank K. Ito, L. Luo and B.J. Dickson for gifts of fly stocks, and B.P. Bean for the loan of equipment. We are grateful to V. Jayaraman, A.W. Liu, O. Mazor, M. Meister, M. Stopfer and members of the Wilson laboratory for comments on the manuscript. This work was funded by a postdoctoral fellowship (F32DC009538 to H.K.) and a research project grant (R01DC008174) from the US National Institutes of Health, a Pew Scholar Award, a McKnight Scholar Award, a Sloan Foundation Research Fellowship, and a Beckman Young Investigator Award (to R.I.W.).

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H.K. performed the experiments and analyzed the data. H.K. and R.I.W. designed the experiments and wrote the paper.

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Correspondence to Rachel I Wilson.

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Kazama, H., Wilson, R. Origins of correlated activity in an olfactory circuit. Nat Neurosci 12, 1136–1144 (2009). https://doi.org/10.1038/nn.2376

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