Fully-Automatic Synapse Prediction and Validation on a Large Data Set

Extracting a connectome from an electron microscopy (EM) data set requires identification of neurons and determination of connections (synapses) between neurons. As manual extraction of this information is very time-consuming, there has been extensive research efforts to automatically segment the neurons to help guide and eventually replace manual tracing. Until recently, there has been comparatively little research on automatic detection of the actual synapses between neurons. This discrepancy can, in part, be attributed to several factors: obtaining neuronal shapes is a prerequisite for the first step in extracting a connectome, manual tracing is much more time-consuming than annotating synapses, and neuronal contact area can be used as a proxy for synapses in determining connections. However, recent research has demonstrated that contact area alone is not a sufficient predictor of a synaptic connection. Moreover, as segmentation improved, we observed that synapse annotation consumes a more significant fraction of overall reconstruction time (upwards of 50% of total effort). This ratio will only get worse as segmentation improves, gating the overall possible speed-up. Therefore, we address this problem by developing algorithms that automatically detect presynaptic neurons and their postsynaptic partners. In particular, presynaptic structures are detected using a U-Net convolutional neural network (CNN), and postsynaptic partners are detected using a multilayer perceptron (MLP) with features conditioned on the local segmentation. This work is novel because it requires minimal amount of training, leverages advances in image segmentation directly, and provides a complete solution for polyadic synapse detection. We further introduce novel metrics to evaluate our algorithm on connectomes of meaningful size. When applied to the output of our method on EM data from Drosphila, these metrics demonstrate that a completely automatic prediction can be used to effectively characterize most of the connectivity correctly.

[1]  Thomas Brox,et al.  U-Net: Convolutional Networks for Biomedical Image Segmentation , 2015, MICCAI.

[2]  B. S. Manjunath,et al.  Synapse classification and localization in Electron Micrographs , 2014, Pattern Recognit. Lett..

[3]  Patrick van der Smagt,et al.  SynEM, automated synapse detection for connectomics , 2017, eLife.

[4]  Louis K. Scheffer,et al.  A visual motion detection circuit suggested by Drosophila connectomics , 2013, Nature.

[5]  Gary B. Huang,et al.  Identifying Synapses Using Deep and Wide Multiscale Recursive Networks , 2014, ArXiv.

[6]  Stephan Saalfeld,et al.  Synaptic Cleft Segmentation in Non-Isotropic Volume Electron Microscopy of the Complete Drosophila Brain , 2018, MICCAI.

[7]  G. Urban,et al.  Automated synaptic connectivity inference for volume electron microscopy , 2017, Nature Methods.

[8]  Eric T. Trautman,et al.  A Complete Electron Microscopy Volume of the Brain of Adult Drosophila melanogaster , 2017, Cell.

[9]  Fred A. Hamprecht,et al.  Automated Detection and Segmentation of Synaptic Contacts in Nearly Isotropic Serial Electron Microscopy Images , 2011, PloS one.

[10]  Fred A. Hamprecht,et al.  Who Is Talking to Whom: Synaptic Partner Detection in Anisotropic Volumes of Insect Brain , 2015, MICCAI.

[11]  Louis K. Scheffer,et al.  Synaptic circuits and their variations within different columns in the visual system of Drosophila , 2015, Proceedings of the National Academy of Sciences.

[12]  Viren Jain,et al.  Deep and Wide Multiscale Recursive Networks for Robust Image Labeling , 2013, ICLR.

[13]  Pascal Fua,et al.  Learning Context Cues for Synapse Segmentation , 2013, IEEE Transactions on Medical Imaging.

[14]  Philipp Otto,et al.  webKnossos: efficient online 3D data annotation for connectomics , 2017, Nature Methods.

[15]  Louis K. Scheffer,et al.  A connectome of a learning and memory center in the adult Drosophila brain , 2017, eLife.

[16]  A. Cardona,et al.  An Integrated Micro- and Macroarchitectural Analysis of the Drosophila Brain by Computer-Assisted Serial Section Electron Microscopy , 2010, PLoS biology.

[17]  Gregory D. Hager,et al.  VESICLE: Volumetric Evaluation of Synaptic Inferfaces using Computer Vision at Large Scale , 2014, BMVC.

[18]  Ziv Bar-Joseph,et al.  A high-throughput framework to detect synapses in electron microscopy images , 2013, Bioinform..

[19]  Toufiq Parag,et al.  Annotating Synapses in Large EM Datasets , 2014, ArXiv.

[20]  Fred A. Hamprecht,et al.  Automated Detection of Synapses in Serial Section Transmission Electron Microscopy Image Stacks , 2014, PloS one.