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Representation and transformation of sensory information in the mouse accessory olfactory system

Abstract

In mice, nonvolatile social cues are detected and analyzed by the accessory olfactory system (AOS). Here we provide a first view of information processing in the AOS with respect to individual chemical cues. 12 sulfated steroids, recently discovered mouse AOS ligands, caused widespread activity among vomeronasal sensory neurons (VSNs), yet VSN responses clustered into a small number of repeated functional patterns or processing streams. Downstream neurons in the accessory olfactory bulb (AOB) responded to these ligands with enhanced signal/noise compared to VSNs. Although the dendritic connectivity of AOB mitral cells suggests the capacity for broad integration, most sulfated steroid responses were well-modeled by linear excitatory drive from just one VSN processing stream. However, a substantial minority demonstrated multi-stream integration. Most VSN excitation patterns were also observed in the AOB, but excitation by estradiol sulfate processing streams was rare, suggesting AOB circuit organization is specific to the biological relevance of sensed cues.

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Figure 1: AOB cells respond strongly to sulfated steroids.
Figure 2: AOB cell population responses to synthetic sulfated steroids.
Figure 3: VSN population responses to synthetic sulfated steroids.
Figure 4: Sensory responses to sulfated steroids can be grouped into functional categories.
Figure 5: A linear integration model indicates that most AOB neurons receive functional input from a single defined processing stream.
Figure 6: Residuals of model fitting reveal input patterns missing in the VSN dataset.
Figure 7: Summary of observed response patterns in AOB neurons.

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Acknowledgements

We thank D. Kerschensteiner for comments and suggestions and all members of the Holy laboratory for helpful feedback. We acknowledge the generous support of the G. Harold and Leila Y. Mathers Foundation (T.E.H.), the US National Institute for Deafness and Other Communication Disorders (R01DC005964 and R01DC010381 to T.E.H.; F32DC009352 to J.P.M.) and the W. M. Keck Foundation (J.P.M.).

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Authors

Contributions

J.P.M. performed all of the experiments and analyses involving the AOB and most of the VSN recordings. H.A.A. performed and analyzed the experiments shown in Figure 6a. J.P.M. and T.E.H. wrote the manuscript.

Corresponding author

Correspondence to Timothy E Holy.

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The authors declare no competing financial interests.

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Supplementary Figures 1–6 and Supplementary Table 1 (PDF 1861 kb)

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Meeks, J., Arnson, H. & Holy, T. Representation and transformation of sensory information in the mouse accessory olfactory system. Nat Neurosci 13, 723–730 (2010). https://doi.org/10.1038/nn.2546

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