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A temporal basis for predicting the sensory consequences of motor commands in an electric fish

Nature Neuroscience volume 17, pages 416422 (2014) | Download Citation

Abstract

Mormyrid electric fish are a model system for understanding how neural circuits predict the sensory consequences of motor acts. Medium ganglion cells in the electrosensory lobe create negative images that predict sensory input resulting from the fish's electric organ discharge (EOD). Previous studies have shown that negative images can be created through plasticity at granule cell–medium ganglion cell synapses, provided that granule cell responses to the brief EOD command are sufficiently varied and prolonged. Here we show that granule cells indeed provide such a temporal basis and that it is well-matched to the temporal structure of self-generated sensory inputs, allowing rapid and accurate sensory cancellation and explaining paradoxical features of negative images. We also demonstrate an unexpected and critical role of unipolar brush cells (UBCs) in generating the required delayed responses. These results provide a mechanistic account of how copies of motor commands are transformed into sensory predictions.

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Acknowledgements

This work was supported by grants from the US National Science Foundation (1025849), US National Institutes of Health (NIH; NS075023), Alfred P. Sloan Foundation and the McKnight Endowment Fund for Neuroscience to N.B.S.; NIH grant (MH093338) to L.F.A.; and a Howard Hughes Medical Institute International Student Research Fellowship to P.K.; A.K. was supported by NIH training grant T32NS064929. Additional support was provided by the Gatsby Foundation, the Swartz Foundation and the Kavli Institute for Brain Science at Columbia University. We thank R. Axel and T. Jessell for comments on the manuscript, and K. Zhang for assistance with histology.

Author information

Author notes

    • Greg Wayne
    •  & Patrick Kaifosh

    These authors contributed equally to this work.

Affiliations

  1. Department of Neuroscience, Columbia University, New York, New York, USA.

    • Ann Kennedy
    • , Greg Wayne
    • , Patrick Kaifosh
    • , Karina Alviña
    • , L F Abbott
    •  & Nathaniel B Sawtell
  2. Department of Physiology and Cellular Biophysics, Columbia University, New York, New York, USA.

    • L F Abbott

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Contributions

N.B.S. and K.A. performed the experiments. A.K., G.W. and P.K. performed the modeling. N.B.S., L.F.A., A.K., G.W. and P.K. wrote the manuscript. N.B.S. and L.F.A. designed and supervised the project.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Nathaniel B Sawtell.

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DOI

https://doi.org/10.1038/nn.3650

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