Abstract
ABSTRACTBoth spatial and temporal cues determine the fate of immature neurons. A major challenge at the interface of developmental and systems neuroscience is to relate this spatiotemporal trajectory of maturation to circuit‐level functional organization. This study examined the development of two extraocular motor nuclei (nIII and nIV), structures in which a motoneuron's identity, or choice of muscle partner, defines its behavioral role. We used retro‐orbital dye fills, in combination with fluorescent markers for motoneuron location and birthdate, to probe spatial and temporal organization of the oculomotor (nIII) and trochlear (nIV) nuclei in the larval zebrafish. We describe a dorsoventral organization of the four nIII motoneuron pools, in which inferior and medial rectus motoneurons occupy dorsal nIII, while inferior oblique and superior rectus motoneurons occupy distinct divisions of ventral nIII. Dorsal nIII motoneurons are, moreover, born before motoneurons of ventral nIII and nIV. The order of neurogenesis can therefore account for the dorsoventral organization of nIII and may play a primary role in determining motoneuron identity. We propose that the temporal development of extraocular motoneurons plays a key role in assembling a functional oculomotor circuit. J. Comp. Neurol. 525:65–78, 2017. © 2016 The Authors The Journal of Comparative Neurology Published by Wiley Periodicals, Inc.
Highlights
Both spatial and temporal cues determine the fate of immature neurons
This study found that extraocular motoneurons in cranial nuclei III and IV of the larval zebrafish are spatially organized, in a manner consistent with their birth order
Our data show a spatial organization to nIII pools in the 5–7 dpf zebrafish: inferior/medial rectus (IR/MR) motoneurons are predominantly found in dorsal nIII, while inferior oblique (IO) and superior rectus (SR) motoneurons are predominantly found in ventral nIII (Fig. 9A)
Summary
All protocols and procedures involving zebrafish were approved by the New York University Langone School of Medicine Institutional Animal Care & Use Committee (IACUC). Data collection and analysis Assignation of filled cells as specific motoneurons Larvae were anesthetized in 0.02% MESAB and mounted dorsally in 2% agar for image collection. For each data stack, imaged under identical experimental conditions, the intensity was adjusted to only display values above the floor Applying this minimum intensity display threshold to stacks from homozygous Tg(isl1:GFP) larvae allowed us to distinguish dye-filled GFP– cells from faintly. The first image stack contained red Kaede emission only in neurons that were already postmitotic during the earlier photoconversion, and green emission from both unconverted neurons (Kaede) and extraocular motoneurons (GFP) (Fig. 4B, left column). To establish a threshold for red Kaede signal that corresponded to a postmitotic neuron, rather than basal photoconversion, we used data from stacks of Tg(huC:Kaede);Tg(isl1:GFP) siblings that had not been exposed to light. GFP1 neurons in the final image were placed into the map of nIII/nIV only if they contained supra-threshold red Kaede signal in the initial image
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