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Neuronal filtering of multiplexed odour representations

Abstract

Neuronal activity patterns contain information in their temporal structure, indicating that information transfer between neurons may be optimized by temporal filtering. In the zebrafish olfactory bulb, subsets of output neurons (mitral cells) engage in synchronized oscillations during odour responses, but information about odour identity is contained mostly in non-oscillatory firing rate patterns. Using optogenetic manipulations and odour stimulation, we found that firing rate responses of neurons in the posterior zone of the dorsal telencephalon (Dp), a target area homologous to olfactory cortex, were largely insensitive to oscillatory synchrony of mitral cells because passive membrane properties and synaptic currents act as low-pass filters. Nevertheless, synchrony influenced spike timing. Moreover, Dp neurons responded primarily during the decorrelated steady state of mitral cell activity patterns. Temporal filtering therefore tunes Dp neurons to components of mitral cell activity patterns that are particularly informative about precise odour identity. These results demonstrate how temporal filtering can extract specific information from multiplexed neuronal codes.

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Figure 1: Optogenetic manipulation of mitral cell synchrony and its effect on Dp neurons.
Figure 2: Local field potential responses.
Figure 3: Spiking responses to odours in Dp are driven by slow depolarization.
Figure 4: Intrinsic properties of Dp neurons.
Figure 5: Late responses of Dp neurons.

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Acknowledgements

This work was supported by the Novartis Research Foundation, the Max-Planck-Society, the Swiss National Fonds (SNF), the Deutsche Forschungsgemeinschaft (DFG), the Human Frontier Science Program (HFSP), and the Whitaker Foundation (J.S.). We are grateful to S.-i. Higashijima for vglut2a-GFP transgenic fish and thank T. Frank, A. Lüthi, I. Namekawa and T. Oertner for comments on the manuscript.

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Contributions

F.B. performed electrophysiological experiments, analysed data and wrote part of the manuscript. P.Z. generated transgenic fish, participated in the construction of the DMD device, performed optogenetic experiments, recorded LFPs and analysed data. J.S. constructed the DMD device and performed optogenetic experiments. Y.-P.Z.S. performed electrophysiological experiments, participated in the construction of the DMD device, performed calcium imaging experiments, recorded LFPs and analysed data. E.Y. participated in calcium imaging experiments. K.D. contributed channelrhodopsin-2 constructs. R.W.F. conceived the study, designed equipment, analysed data, performed modelling and wrote the manuscript.

Corresponding author

Correspondence to Rainer W. Friedrich.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-15 with legends and additional references. (PDF 2879 kb)

Supplementary Movie 1

This movie shows an example of an optical stimulus pattern with no synchronization (S = 0), slowed down in time. (AVI 4852 kb)

Supplementary Movie 2

Example of an optical stimulus pattern with high synchronization (S = 10; same spatial pattern as Supplementary Movie 1), slowed down in time. (AVI 4832 kb)

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Blumhagen, F., Zhu, P., Shum, J. et al. Neuronal filtering of multiplexed odour representations. Nature 479, 493–498 (2011). https://doi.org/10.1038/nature10633

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