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A visual motion detection circuit suggested by Drosophila connectomics

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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Figure 1: Motion detection and the Drosophila visual system.
Figure 2: Connectome reconstruction using serial-section electron microscopy.
Figure 3: Medulla connectome module.
Figure 4: Spatial displacement of Mi1- and Tm3-mediated inputs onto a single T4 cell (T4-12).
Figure 5: Computed displacements for all T4 cells.
Figure 6: Orientation of medulla dendritic arbors of T4 neurons correlates with axon terminal arborization layer in the lobula plate.

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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

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Authors

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.

Corresponding authors

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

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

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. (PDF 6359 kb)

Supplementary Figure

This file contains the full version of Supplementary Figure 1 (see Supplementary Information file p.1 for full legend). (PDF 8306 kb)

Supplementary Table 1

This file contains the full version of Supplementary Table 1 (see Supplementary Information file p.16 for legend). (XLS 5614 kb)

Supplementary Data

This zipped file contains Supplementary Data 1 – see Supplementary Information file p.23 for legend). (ZIP 18850 kb)

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. (MP4 29558 kb)

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Takemura, Sy., Bharioke, A., Lu, Z. et al. A visual motion detection circuit suggested by Drosophila connectomics. Nature 500, 175–181 (2013). https://doi.org/10.1038/nature12450

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