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Distinct representations of olfactory information in different cortical centres

Abstract

Sensory information is transmitted to the brain where it must be processed to translate stimulus features into appropriate behavioural output. In the olfactory system, distributed neural activity in the nose is converted into a segregated map in the olfactory bulb1,2,3. Here we investigate how this ordered representation is transformed in higher olfactory centres in mice. We have developed a tracing strategy to define the neural circuits that convey information from individual glomeruli in the olfactory bulb to the piriform cortex and the cortical amygdala. The spatial order in the bulb is discarded in the piriform cortex; axons from individual glomeruli project diffusely to the piriform without apparent spatial preference. In the cortical amygdala, we observe broad patches of projections that are spatially stereotyped for individual glomeruli. These projections to the amygdala are overlapping and afford the opportunity for spatially localized integration of information from multiple glomeruli. The identification of a distributive pattern of projections to the piriform and stereotyped projections to the amygdala provides an anatomical context for the generation of learned and innate behaviours.

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Figure 1: Targeted electroporation of TMR-dextran labels cells that innervate a single glomerulus in the olfactory bulb.
Figure 2: Mitral/tufted cells connected to a single glomerulus show distinct patterns of projections to several areas of the olfactory cortex.
Figure 3: Projections from single glomeruli to piriform cortex are disperse, homogeneous and indistinguishable.
Figure 4: Projections from single glomeruli to the cortical amygdala are broad, patchy and stereotyped.

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Acknowledgements

We thank members of the R.A. and S.R.D. laboratories for comments and advice, B. Shykind for mice with GFP-labelled olfactory receptor neurons, S. X. Luo for image alignment advice, D. M. Bear for cross-correlation analysis advice, D. Padfield for Matlab code, R. Wilson for comments on the manuscript and P. Kisloff for manuscript preparation assistance. Financial support was provided by a Helen Hay Whitney Foundation Fellowship, a Career Award in the Medical Sciences grant from the Burroughs Wellcome Fund, and funding from the National Institutes of Health through the NIH Director’s New Innovator Award Program (DP2-OD-007109) (S.R.D.), a Ruth L. Kirschstein National Research Service Award predoctoral fellowship from the National Institutes of Health (D.L.S.), and the Howard Hughes Medical Institute and a grant from the Foundation for the National Institutes of Health through the Grand Challenges in Global Health initiative (R.A.).

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Contributions

S.R.D., D.L.S. and R.A conceived the project, participated in its development and wrote the manuscript. S.R.D. and D.L.S. developed methods and performed all experiments and data analysis. T.C. generated the MOR1-3 and MOR174-9–IRES–GFP mice. M.L.B. performed mouse husbandry and immunostaining.

Corresponding author

Correspondence to Richard Axel.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Figures 1-12 with legends and Supplementary Tables 1-3. (ZIP 26219 kb)

Supplementary Movie 1

Movie created using a z-stack of images taken using a two-photon microscope of the olfactory bulb of an OMP-IRES-spH mouse after electroporation of a single glomerulus with TMR dextran (red). The imaged plane descends from the glomerular layer (surface) of the olfactory bulb through the mitral cell layer (~300 microns deep) as the movie progresses. (MOV 8246 kb)

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Sosulski, D., Bloom, M., Cutforth, T. et al. Distinct representations of olfactory information in different cortical centres. Nature 472, 213–216 (2011). https://doi.org/10.1038/nature09868

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