Comparisons between the ON- and OFF-edge motion pathways in the Drosophila brain
- Janelia Research Campus, Howard Hughes Medical Institute, United States
Abstract
Understanding the circuit mechanisms behind motion detection is a long-standing question in visual neuroscience. In Drosophila melanogaster, recent synapse-level connectomes in the optic lobe, particularly in ON-pathway (T4) receptive-field circuits, in concert with physiological studies, suggest an increasingly intricate motion model compared with the ubiquitous Hassenstein-Reichardt model, while our knowledge of OFF-pathway (T5) has been incomplete. Here we present a conclusive and comprehensive connectome that for the first time integrates detailed connectivity information for inputs to both T4 and T5 pathways in a single EM dataset covering the entire optic lobe. With novel reconstruction methods using automated synapse prediction suited to such a large connectome, we successfully corroborate previous findings in the T4 pathway and comprehensively identify inputs and receptive fields for T5. While the two pathways are likely evolutionarily linked and indeed exhibit many similarities, we uncover interesting differences and interactions that may underlie their distinct functional properties.
Data availability
The raw electron microscopy data, as well as skeletonized neurons and numbers of input and output synapses of T4 and T5 cells used in this study are hosted at a Janelia website: http://emdata.janelia.org/optic-lobe/.
Article and author information
Author details
Kazunori Shinomiya
Ian A Meinertzhagen
Funding
Howard Hughes Medical Institute
- Stephen M Plaza
Kazato Research Foundation (Kazato Research Encouragement Prize)
- Kazunori Shinomiya
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Alexander Borst, Max Planck Institute of Neurobiology, Germany
Publication history
- Received: July 12, 2018
- Accepted: January 2, 2019
- Accepted Manuscript published: January 9, 2019 (version 1)
- Version of Record published: January 18, 2019 (version 2)
Copyright
© 2019, Shinomiya et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 3,989
- Page views
-
- 541
- Downloads
-
- 59
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Comparisons between the ON- and OFF-edge motion pathways in the Drosophila brain
eLife 8:e40025.
https://doi.org/10.7554/eLife.40025
Further reading
-
- Neuroscience
According to the efficient coding hypothesis, sensory neurons are adapted to provide maximal information about the environment, given some biophysical constraints. In early visual areas, stimulus-induced modulations of neural activity (or tunings) are predominantly single-peaked. However, periodic tuning, as exhibited by grid cells, has been linked to a significant increase in decoding performance. Does this imply that the tuning curves in early visual areas are sub-optimal? We argue that the time scale at which neurons encode information is imperative to understand the advantages of single-peaked and periodic tuning curves, respectively. Here, we show that the possibility of catastrophic (large) errors creates a trade-off between decoding time and decoding ability. We investigate how decoding time and stimulus dimensionality affect the optimal shape of tuning curves for removing catastrophic errors. In particular, we focus on the spatial periods of the tuning curves for a class of circular tuning curves. We show an overall trend for minimal decoding time to increase with increasing Fisher information, implying a trade-off between accuracy and speed. This trade-off is reinforced whenever the stimulus dimensionality is high, or there is ongoing activity. Thus, given constraints on processing speed, we present normative arguments for the existence of the single-peaked tuning organization observed in early visual areas.
-
- Genetics and Genomics
- Neuroscience
Aging is a major risk factor for Alzheimer’s disease (AD), and cell-type vulnerability underlies its characteristic clinical manifestations. We have performed longitudinal, single-cell RNA-sequencing in Drosophila with pan-neuronal expression of human tau, which forms AD neurofibrillary tangle pathology. Whereas tau- and aging-induced gene expression strongly overlap (93%), they differ in the affected cell types. In contrast to the broad impact of aging, tau-triggered changes are strongly polarized to excitatory neurons and glia. Further, tau can either activate or suppress innate immune gene expression signatures in a cell-type-specific manner. Integration of cellular abundance and gene expression pinpoints nuclear factor kappa B signaling in neurons as a marker for cellular vulnerability. We also highlight the conservation of cell-type-specific transcriptional patterns between Drosophila and human postmortem brain tissue. Overall, our results create a resource for dissection of dynamic, age-dependent gene expression changes at cellular resolution in a genetically tractable model of tauopathy.
