Intraspinal serotonergic signaling suppresses locomotor activity in larval zebrafish

Jacob E. Montgomery, Sarah Wahlstrom-Helgren, Timothy D. Wiggin, Brittany M. Corwin, Christina Lillesaar, Mark A. Masino

Research output: Contribution to journalArticlepeer-review

6 Scopus citations

Abstract

Serotonin (5HT) is a modulator of many vital processes in the spinal cord (SC), such as production of locomotion. In the larval zebrafish, intraspinal serotonergic neurons (ISNs) are a source of spinal 5HT that, despite the availability of numerous genetic and optical tools, has not yet been directly shown to affect the spinal locomotor network. In order to better understand the functions of ISNs, we used a combination of strategies to investigate ISN development, morphology, and function. ISNs were optically isolated from one another by photoconverting Kaede fluorescent protein in individual cells, permitting morphometric analysis as they developed in vivo. ISN neurite lengths and projection distances exhibited the greatest amount of change between 3 and 4 days post-fertilization (dpf) and appeared to stabilize by 5 dpf. Overall ISN innervation patterns were similar between cells and between SC regions. ISNs possessed rostrally-extending neurites resembling dendrites and a caudally-extending neurite resembling an axon, which terminated with an enlarged growth cone-like structure. Interestingly, these enlargements remained even after neurite extension had ceased. Functionally, application of exogenous 5HT reduced spinally-produced motor nerve bursting. A selective 5HT reuptake inhibitor and ISN activation with channelrhodopsin-2 each produced similar effects to 5HT, indicating that spinally-intrinsic 5HT originating from the ISNs has an inhibitory effect on the spinal locomotor network. Taken together this suggests that the ISNs are morphologically mature by 5 dpf and supports their involvement in modulating the activity of the spinal locomotor network.

Original languageEnglish (US)
Pages (from-to)807-827
Number of pages21
JournalDevelopmental Neurobiology
Volume78
Issue number8
DOIs
StatePublished - Aug 2018

Bibliographical note

Funding Information:
Contract grant sponsor: University of Minnesota Bob Allison Ataxia Research Center (BAARC) and MnDRIVE Brain Conditions (JM). © 2018 Wiley Periodicals, Inc. Published online 2 July 2018 in Wiley Online Library (wileyonli-nelibrary.com). DOI 10.1002/dneu.22606

Funding Information:
Correspondence to: J. E. Montgomery (mont0306@umn.edu) Contract grant sponsor: National Institutes of Health (http:// www.nih.gov/); contract grant number: R01 NS065054 (MAM), R01 NS094176 (MAM), and F31 NS083110 (TDW).

Publisher Copyright:
© 2018 Wiley Periodicals, Inc.

Keywords

  • morphology
  • optogenetic
  • serotonin
  • spinal cord
  • zebrafish

Fingerprint

Dive into the research topics of 'Intraspinal serotonergic signaling suppresses locomotor activity in larval zebrafish'. Together they form a unique fingerprint.

Cite this