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Gaze-stabilizing central vestibular neurons project asymmetrically to extraocular motoneuron pools

Schoppik, David and Bianco, Isaac H. and Prober, David A. and Douglass, Adam D. and Robson, Drew N. and Li, Jennifer M. B. and Greenwood, Joel S. F. and Soucy, Edward and Engert, Florian and Schier, Alexander F. (2017) Gaze-stabilizing central vestibular neurons project asymmetrically to extraocular motoneuron pools. Journal of Neuroscience, 37 (47). pp. 11353-11365. ISSN 0270-6474. PMCID PMC5700419. https://resolver.caltech.edu/CaltechAUTHORS:20171009-110032062

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Abstract

Within reflex circuits, specific anatomical projections allow central neurons to relay sensations to effectors that generate movements. A major challenge is to relate anatomical features of central neural populations, such as asymmetric connectivity, to the computations the populations perform. To address this problem, we mapped the anatomy, modeled the function, and discovered a new behavioral role for a genetically defined population of central vestibular neurons in rhombomeres 5–7 of larval zebrafish. First, we found that neurons within this central population project preferentially to motoneurons that move the eyes downward. Concordantly, when the entire population of asymmetrically projecting neurons was stimulated collectively, only downward eye rotations were observed, demonstrating a functional correlate of the anatomical bias. When these neurons are ablated, fish failed to rotate their eyes following either nose-up or nose-down body tilts. This asymmetrically projecting central population thus participates in both upward and downward gaze stabilization. In addition to projecting to motoneurons, central vestibular neurons also receive direct sensory input from peripheral afferents. To infer whether asymmetric projections can facilitate sensory encoding or motor output, we modeled differentially projecting sets of central vestibular neurons. Whereas motor command strength was independent of projection allocation, asymmetric projections enabled more accurate representation of nose-up stimuli. The model shows how asymmetric connectivity could enhance the representation of imbalance during nose-up postures while preserving gaze stabilization performance. Finally, we found that central vestibular neurons were necessary for a vital behavior requiring maintenance of a nose-up posture: swim bladder inflation. These observations suggest that asymmetric connectivity in the vestibular system facilitates representation of ethologically relevant stimuli without compromising reflexive behavior.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1523/JNEUROSCI.1711-17.2017DOIArticle
http://www.jneurosci.org/content/37/47/11353PublisherArticle
https://www.biorxiv.org/content/early/2017/08/25/151548OrganizationDiscussion Paper
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5700419PubMed CentralArticle
ORCID:
AuthorORCID
Schoppik, David0000-0001-7969-9632
Prober, David A.0000-0002-7371-4675
Robson, Drew N.0000-0002-0150-1515
Soucy, Edward0000-0002-1187-5596
Additional Information:© 2017 Schoppik et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. Received: 19 June 2017; Revised: 15 September 2017; Accepted: 19 September 2017; Published: 29 September 2017. D.S. was supported by a Helen Hay Whitney Postdoctoral Fellowship and National Institute on Deafness and Communication Disorders of the National Institutes of Health Awards K99DC012775 and 5R00DC012775. I.H.B. was supported by Wellcome Trust Sir Henry Wellcome Postdoctoral Fellowship. This work was supported by National Institutes of Health Grants 1R01DA030304 and 1RC2NS069407 to F.E. and Grant R01HL109525 to A.F.S. We thank Robert Baker for inspiration and extensive insights; Omi Ma for discussions and help with retro-orbital fills; Ian Woods for help with transgenesis; Bill Harris for generously providing the atoh7th241/th241; Tg(atoh7:gap43-RFP) line; Clemens Riegler for maintaining the Tg(5×UAS:sypb-GCaMP3) line; Albert Pan for maintaining the Tg(UAS-E1b:Kaede)s1999t line; the Zebrafish International Resource Center for the Et(E1b:Gal4-VP16)s1101t line; Minoru Koyama for insights into focal lesions; Steve Zimmerman, Karen Hurley, and Jessica Miller for fish care; Bernhard Goetze, Doug Richardson, and Casey Kraft for help with microscopy; Dorothy Barr for library services; and Katherine Nagel and the members of the F.E., A.F.S., and D.S. laboratories, particularly David Ehrlich, Marie Greaney (who provided the fish schematic in Fig. 1), Katherine Harmon, Alix Lacoste, Owen Randlett, and Martin Haesemeyer for helpful discussions. The authors declare no competing financial interests.
Funders:
Funding AgencyGrant Number
Helen Hay Whitney FoundationUNSPECIFIED
NIHK99DC012775
NIH5R00DC012775
Wellcome TrustUNSPECIFIED
NIH1R01DA030304
NIH1RC2NS069407
NIHR01HL109525
Subject Keywords:anatomy; asymmetry; motoneuron; reflex; vestibular; zebrafish
Issue or Number:47
PubMed Central ID:PMC5700419
Record Number:CaltechAUTHORS:20171009-110032062
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20171009-110032062
Official Citation:Gaze-Stabilizing Central Vestibular Neurons Project Asymmetrically to Extraocular Motoneuron Pools David Schoppik, Isaac H. Bianco, David A. Prober, Adam D. Douglass, Drew N. Robson, Jennifer M.B. Li, Joel S.F. Greenwood, Edward Soucy, Florian Engert, Alexander F. Schier Journal of Neuroscience 22 November 2017, 37 (47) 11353-11365; DOI: 10.1523/JNEUROSCI.1711-17.2017
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:82209
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:09 Oct 2017 18:14
Last Modified:03 Oct 2019 18:52

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