Abstract

Animal behaviour arises from computations in neuronal circuits, but our understanding of these computations has been frustrated by the lack of detailed synaptic connection maps, or connectomes. For example, despite intensive investigations over half a century, the neuronal implementation of local motion detection in the insect visual system remains elusive. Here we develop a semi-automated pipeline using electron microscopy to reconstruct a connectome, containing 379 neurons and 8,637 chemical synaptic contacts, within the Drosophila optic medulla. By matching reconstructed neurons to examples from light microscopy, we assigned neurons to cell types and assembled a connectome of the repeating module of the medulla. Within this module, we identified cell types constituting a motion detection circuit, and showed that the connections onto individual motion-sensitive neurons in this circuit were consistent with their direction selectivity. Our results identify cellular targets for future functional investigations, and demonstrate that connectomes can provide key insights into neuronal computations.

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Acknowledgements

We acknowledge the technical support of all members of the Janelia FlyEM project and the Chklovskii group, past and present. We thank S. Laughlin for numerous discussions, and M. Reiser and N. Verma for commenting on the manuscript. We thank A. Borst, C. Desplan, C.-H. Lee, T. Clandinin and L. Zipursky for discussions and granting us access to their data before publication.

Author information

Affiliations

  1. Janelia Farm Research Campus, HHMI, Ashburn, Virginia 20147, USA

    • Shin-ya Takemura
    • , Arjun Bharioke
    • , Zhiyuan Lu
    • , Aljoscha Nern
    • , Shiv Vitaladevuni
    • , Patricia K. Rivlin
    • , William T. Katz
    • , Donald J. Olbris
    • , Stephen M. Plaza
    • , Philip Winston
    • , Ting Zhao
    • , Richard D. Fetter
    • , Satoko Takemura
    • , Katerina Blazek
    • , Lei-Ann Chang
    • , Omotara Ogundeyi
    • , Mathew A. Saunders
    • , Victor Shapiro
    • , Christopher Sigmund
    • , Gerald M. Rubin
    • , Louis K. Scheffer
    • , Ian A. Meinertzhagen
    •  & Dmitri B. Chklovskii
  2. Department of Psychology and Neuroscience, Dalhousie University, Halifax, Nova Scotia B3H 4R2, Canada

    • Zhiyuan Lu
    • , Jane Anne Horne
    •  & Ian A. Meinertzhagen

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Contributions

D.B.C. and I.A.M. designed the research. Z.L., Sh.T. and R.D.F. prepared and imaged the sample. D.J.O., P.W., S.M.P., S.V. and W.T.K., under the guidance of D.B.C. and L.K.S., developed software for the reconstruction. Sh.T. annotated the micrographs, proofread the segmentation, and assembled the connectome, with the help of other proofreaders (Sa.T. K.B., L.-A.C., O.O., M.A.S., V.S. and C.S.), supervised by P.K.R. and J.A.H. A.N. and G.M.R. provided and A.N. analysed light microscopy images. L.K.S. and A.B. performed data analysis and T.Z. aided in visualization. A.B. and D.B.C. studied the motion detection circuit. A.B., D.B.C., I.A.M. and L.K.S. wrote the paper, with contributions from Sh.T. and A.N.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Ian A. Meinertzhagen or Dmitri B. Chklovskii.

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    This file contains Supplementary Figures 1-6, Supplementary Methods, Supplementary Tables 1-3, a full legend to accompany the Supplementary Data file, the full video legend and Supplementary References.

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Videos

  1. 1.

    Neuron reconstructions

    This video shows the EM image stack of the medulla region of interest (Fig. 1c). Images from the stack are progressively removed (directed towards the deeper strata), and reconstructions of 379 neurons are added in succession, in randomly selected colors. The neurons are grouped into six classes, with text describing the class being added simultaneously with the neurons from each class: (1) Photoreceptor terminals, from the retina, and neurons from the lamina that innervate the reference column within the medulla. (2) Neurons receiving direct input from the retina and lamina neurons. (3) Neurons receiving direct input from the neurons in class (2). (4) Neurons that arborize in the reference column, but spread across multiple columns. (5) Tangential neurons, of which often only a fragment passing through the region of interest has been reconstructed. (6) Additional neurons, often of the same class as neurons in classes (1) – (5), but from adjacent columns.

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DOI

https://doi.org/10.1038/nature12450

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