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A cerebellum-like circuit in the auditory system cancels responses to self-generated sounds

Nature Neuroscience volume 20, pages 943950 (2017) | Download Citation

Abstract

The dorsal cochlear nucleus (DCN) integrates auditory nerve input with a diverse array of sensory and motor signals processed in circuitry similar to that of the cerebellum. Yet how the DCN contributes to early auditory processing has been a longstanding puzzle. Using electrophysiological recordings in mice during licking behavior, we show that DCN neurons are largely unaffected by self-generated sounds while remaining sensitive to external acoustic stimuli. Recordings in deafened mice, together with neural activity manipulations, indicate that self-generated sounds are cancelled by non-auditory signals conveyed by mossy fibers. In addition, DCN neurons exhibit gradual reductions in their responses to acoustic stimuli that are temporally correlated with licking. Together, these findings suggest that DCN may act as an adaptive filter for cancelling self-generated sounds. Adaptive filtering has been established previously for cerebellum-like sensory structures in fish, suggesting a conserved function for such structures across vertebrates.

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Acknowledgements

We thank L. Abbott, C. Bell and T. Jessell for comments on the manuscript. This work was supported by grants from the NIH (DC015449), the Alfred P. Sloan Foundation, the McKnight Endowment Fund for Neuroscience and the Irma T. Hirschl Trust to N.B.S. and an NIH grant (F30DC014174) to S.S.

Author information

Affiliations

  1. Department of Neuroscience and Kavli Institute for Brain Science, Columbia University Medical Center, New York, New York, USA.

    • Shobhit Singla
    • , Conor Dempsey
    • , Richard Warren
    •  & Nathaniel B Sawtell
  2. Department of Biological Sciences, Columbia University, New York, New York, USA.

    • Armen G Enikolopov

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Contributions

S.S. and R.W. performed the experiments and analyzed the data. C.D. designed and performed the analysis. A.G.E. contributed custom software and hardware. N.B.S. and S.S. designed the study and wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Nathaniel B Sawtell.

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    Supplementary Figures 1–6

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Videos

  1. 1.

    Sounds generated by licking behavior in a head-fixed mouse.

    Left, Video of a head-fixed mouse licking a metal spout for water. The lick spout is the small metal tube with a spherical end in the bottom left of the frame. Video was recorded at 300 fps and played back at 30 fps and thus is slowed by a factor of ten. Right, r.m.s. amplitude of microphone recording; dashed line represents the time of the current frame. The microphone is the black object with metallic tip located just above the lick spout. By pausing the video, it is possible to see the relationship between RMS amplitude of the microphone recording and different phases of the licking behavior.

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DOI

https://doi.org/10.1038/nn.4567

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