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

Ashaber, Mária and Tomina, Yusuke and Kassraian-Fard, Pegah and Bushong, Eric A. and Kristan, William B., Jr. and Ellisman, Mark H. and Wagenaar, Daniel A. (2020) Anatomy and activity patterns in a multifunctional motor neuron and its surrounding circuits. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20200312-124530478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. In swimming, it oscillates at a relatively rapid 2 Hz in antiphase to its Ventral Excitor counterpart (VE-4) and controls the local dorsal flexion phase of the swim rhythm. In crawling, it is active in phase with VE-4 and controls the contraction phase of the crawl rhythm. In "local bending" it operates in tight concert with its contralateral homolog as well as VE-4 to precisely deform the local body wall away from a mechanical stimulus. Without rewiring its anatomical connectivity, how can a motor neuron dynamically switch roles to play its appropriate role in various behaviors? We used voltage-sensitive dye imaging to record from DE-3 and most other neurons in the segmental ganglion of the leech during fictive versions of the three behaviors. Then we re-imaged the same ganglion using serial blockface electron microscopy and traced all of DE-3's processes. Further, we traced back the processes of all 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 of the behaviors were widely distributed over DE-3's branches, yet that functional clusters were different during (fictive) swimming vs. crawling.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2020.03.09.984013DOIDiscussion Paper
https://github.com/wagenadl/leechem-publicRelated ItemData
https://github.com/wagenadl/sbemalignRelated ItemData
https://github.com/wagenadl/sbemviewerRelated ItemData
https://github.com/wagenadl/gvoxRelated ItemData
ORCID:
AuthorORCID
Tomina, Yusuke0000-0001-9406-1493
Kassraian-Fard, Pegah0000-0002-6562-7918
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:The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. Posted August 07, 2020. We thank Evan Miller (Berkeley) for sharing of the VF2.1(OMe).H dye, ArtWetzel (Pittsburgh Supercomputer Center) and Tom Bartol (The Salk Institute) for many useful discussions about image alignment, and Tünde Magyar and Renáta Pop (University of Veterinary Medicine, Department of Anatomy and Histology, Budapest, Hungary) for help with TEM. This work was supported by the National Institute of Neurological Disorders and Stroke (R01-NS094403 to DAW) and by the National Institute of General Medical Sciences (P41GM103412 in support of the National Center for Molecular Imaging Research to MHE). YT was supported by Japan Society for Promotion of Science (Overseas Research Fellowship, Research Fellowship for Young Scientists PD, 201800526 and Grant-in-Aid for Young Scientists, 19K16191). PKF was supported by the Swiss National Science Foundation (P2EZP3-181896). Author contributions: Conceptualization: YT, PKF, MHE, WBK, DAW. Data curation: YT, DAW. Formal analysis: YT, MA, PKF, DAW. Funding acquisition: YT, PKF, MHE, WBK, DAW. Investigation: YT, MA, PKF, EAB. Methodology: All. Software: PKF, DAW. Supervision: MHE, DAW. Visualization: YT, MA, PKF, DAW. Writing—original draft: YT, MA.Writing—review and editing: YT, MA, PKF, DAW. The authors declare no competing interests. Data and materials 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. Included in the package is a file called “demo.py” that demonstrates the use of the modules. Supplemental table S4 lists the available VSD trials. The aligned EM volume may be accessed through the Neuroglancer (Google, 2016) instance at https://leechem.caltech.edu or by pointing SBEMViewer to https://leechem.caltech.edu/emdata. The code used for alignment is available at https://github.com/wagenadl/sbemalign. Our visualization tools SBEMViewer and GVox are at https://github.com/wagenadl/sbemviewer and https://github.com/wagenadl/gvox.
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
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 circuitsGOOGLE. Mária Ashaber, Yusuke Tomina, Pegah Kassraian-Fard, Eric A. Bushong, William B. Kristan Jr., Mark H. Ellisman, Daniel A. Wagenaar. bioRxiv 2020.03.09.984013; doi: https://doi.org/10.1101/2020.03.09.984013
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:11 Aug 2020 16:26

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