Anatomy and activity patterns in a multifunctional motor neuron and its surrounding circuits
Abstract
Dorsal Excitor motor neuron DE-3 in the medicinal leech plays three very different dynamical roles in three different behaviors. Without rewiring its anatomical connectivity, how can a motor neuron dynamically switch roles to play appropriate roles in various behaviors? We previously used voltage-sensitive dye imaging to record from DE-3 and most other neurons in the leech segmental ganglion during (fictive) swimming, crawling, and local-bend escape (Tomina and Wagenaar, 2017). Here, we repeated that experiment, then re-imaged the same ganglion using serial blockface electron microscopy and traced DE-3's processes. Further, we traced back the processes of DE-3's presynaptic partners to their respective somata. This allowed us to analyze the relationship between circuit anatomy and the activity patterns it sustains. We found that input synapses important for all the behaviors were widely distributed over DE-3's branches, yet that functional clusters were different during (fictive) swimming vs. crawling.
Additional Information
© 2021 Ashaber et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. Received: 07 August 2020; Accepted: 12 February 2021; Published: 15 February 2021. We thank Evan Miller (Berkeley) for sharing of the VF2.1(OMe).H dye, Art Wetzel (Pittsburgh Supercomputer Center) and Tom Bartol (The Salk Institute) for many useful discussions about image alignment, Tunde Magyar and Renata Pop (University of Veterinary Medicine, Department of Anatomy and Histology, Budapest, Hungary) for help with TEM, and Jason Pipkin (Brandeis University) for advice about tracing. Funding: National Institute of Neurological Disorders and Stroke (R01-NS094403), William B Kristan Jnr, Mark H Ellisman, Daniel A Wagenaar. National Institute of General Medical Sciences (P41-GM103412), Mark H Ellisman. Japan Society for the Promotion of Science (201800526), Yusuke Tomina. Japan Society for the Promotion of Science (19K16191), Yusuke Tomina. Swiss National Science Foundation (P2EZP3-181896), Pegah Kassraian. National Institute of Neurological Disorders and Stroke (1U24NS120055), Mark H Ellisman. The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. Data availability: The easiest way to access the raw electrophysiology and voltage-dye data as well as the tracing results used in this paper is through a series of Python modules that we made available at https://github.com/wagenadl/leechem-public (copy archived at https://archive.softwareheritage.org/swh:1:rev:73eee24e387e11c259a3f3fe0bd4e469048b25e6/). Included in the package is a file called "demo.py" that demonstrates the use of the modules. Table 4 lists the available VSD trials. The aligned EM volume may be accessed through the Neuroglancer instance at https://leechem.caltech.edu or by pointing SBEMViewer to https://leechem.caltech.edu/emdata. The API is documented at https://leechem.caltech.edu/emdata/help. Author contributions: Maria Ashaber, Formal analysis, Investigation, Visualization, Methodology, Writing - original draft, Writing - review and editing; Yusuke Tomina, Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Visualization, Methodology, Writing - original draft, Writing - review and editing; Pegah Kassraian, Conceptualization, Software, Formal analysis, Funding acquisition, Investigation, Visualization, Methodology, Writing - original draft, Writing - review and editing; Eric A Bushong, Investigation, Methodology; William B Kristan, Conceptualization, Funding acquisition, Methodology; Mark H Ellisman, Conceptualization, Supervision, Funding acquisition, Methodology, Project administration; Daniel A Wagenaar, Conceptualization, Data curation, Software, Formal analysis, Supervision, Funding acquisition, Visualization, Methodology, Writing - original draft, Project administration, Writing - review and editing.Attached Files
Published - elife-61881-v2.pdf
Submitted - 2020.03.09.984013v3.full.pdf
Supplemental Material - elife-61881-supp-v1.zip
Supplemental Material - elife-61881-transrepform-v2.pdf
Supplemental Material - elife-61881-video1.mp4
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Additional details
- Alternative title
- Combined membrane potential imaging and connectome of behavioral circuits in an annelid worm
- Alternative title
- Imaging and connectome of leech ganglion
- Eprint ID
- 101894
- Resolver ID
- CaltechAUTHORS:20200312-124530478
- R01-NS094403
- NIH
- P41GM103412
- NIH
- 201800526
- Japan Society for Promotion of Science (JSPS)
- 19K16191
- Japan Society for Promotion of Science (JSPS)
- P2EZP3_181896
- Swiss National Science Foundation (SNSF)
- 1U24NS120055
- NIH
- Created
-
2020-03-12Created from EPrint's datestamp field
- Updated
-
2023-06-02Created from EPrint's last_modified field
- Caltech groups
- Division of Biology and Biological Engineering