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Anatomy and activity patterns in a multifunctional motor neuron and its surrounding circuits

Ashaber, Mária and Tomina, Yusuke and Kassraian, Pegah and Bushong, Eric A. and Kristan, William B. and Ellisman, Mark H. and Wagenaar, Daniel A. (2021) Anatomy and activity patterns in a multifunctional motor neuron and its surrounding circuits. eLife, 10 . Art. No. e61881. ISSN 2050-084X. https://resolver.caltech.edu/CaltechAUTHORS:20200312-124530478

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.7554/eLife.61881DOIArticle
https://doi.org/10.1101/2020.03.09.984013DOIDiscussion Paper
https://github.com/wagenadl/leechem-publicRelated ItemPython modules
https://leechem.caltech.eduRelated ItemNeuroglancer
https://leechem.caltech.edu/emdataRelated ItemSBEMViewer
https://leechem.caltech.edu/emdata/helpRelated ItemAPI
https://doi.org/10.7554/eLife.61881.sa1DOIDecision letter
https://doi.org/10.7554/eLife.61881.sa2DOIAuthor response
ORCID:
AuthorORCID
Ashaber, Mária0000-0002-5586-9585
Tomina, Yusuke0000-0001-9406-1493
Kassraian, Pegah0000-0002-6562-7918
Bushong, Eric A.0000-0001-6195-2433
Ellisman, Mark H.0000-0001-8893-8455
Wagenaar, Daniel A.0000-0002-6222-761X
Alternate Title:Combined membrane potential imaging and connectome of behavioral circuits in an annelid worm, Imaging and connectome of leech ganglion
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.
Funders:
Funding AgencyGrant Number
NIHR01-NS094403
NIHP41GM103412
Japan Society for Promotion of Science (JSPS)201800526
Japan Society for Promotion of Science (JSPS)19K16191
Swiss National Science Foundation (SNSF)P2EZP3_181896
NIH1U24NS120055
Record Number:CaltechAUTHORS:20200312-124530478
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200312-124530478
Official Citation:Anatomy and activity patterns in a multifunctional motor neuron and its surrounding circuits. eLife 2021; 10:e61881; DOI: 10.7554/eLife.61881
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:101894
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:12 Mar 2020 20:12
Last Modified:12 Mar 2021 18:34

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