Organisation of the Zebrafish Spinal Cord: Distribution of Motoneuron Dendrites and 5-HT containing Cells

Raamsdonk, W. van; Bosch, T. J.; Smit-Onel, M.J.; Maslam, S.

doi:10.1076/ejom.34.2.0065

Cited by 8 publications

(22 citation statements)

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“…Embryonic zebrafish possess a population of 5HT‐containing spinal neurons that express tph1a (Bellipanni et al, ), while larval stage ISNs express tph2 and pet1 , and can be identified by EGFP expression in the Tg(pet1:EGFP) ne0214 line (Montgomery et al, ). Although 5HT‐ir ISNs have been reported in the ventral adult zebrafish SC (Van Raamsdonk et al, ; Barreiro‐Iglesias et al, ), the tph gene expressed by these cells is not known. Examination of sagittal and transverse frozen sections of adult Tg(pet1:EGFP) ne0214 SCs ( n = 6) verified that pet1:EGFP ‐expressing cells were ventrally‐located and colabeled with 5HT antibodies (red; Fig.…”

Section: Resultsmentioning

confidence: 99%

“…This later‐appearing population of ISNs expresses tryptophan hydroxylase 2 ( tph2 ) instead of tph1a and persists until at least 10 dpf (Montgomery et al, ). 5HT‐ir neurons have also been confirmed in the ventral SC of adult zebrafish (Van Raamsdonk et al, ; Kuscha et al, ; Barreiro‐Iglesias et al, ), although tph gene expression in these cells has not been characterized.…”

Section: Introductionmentioning

confidence: 98%

“…The observation that 5HT was not entirely eliminated from the SC after complete, chronic spinal transection from the brain led to the inferred existence of spinally‐intrinsic serotonergic neurons (Carlsson et al, ; Andén et al, ; Shibuya and Anderson, ; Clineschmidt et al, ). Subsequent development of immunohistochemical labeling techniques (Steinbusch et al, ) assisted both in confirming and characterizing intraspinal serotonergic neurons (ISNs) in a wide variety of vertebrates, including teleost and non‐teleost fishes (Parent and Northcutt, ; Ritchie and Leonard, ; Harris‐Warrick et al, ; Van Dongen et al, ; Onstott and Elde, ; Van Raamsdonk et al, ; McLean and Fetcho, ), chicks (Sako et al, ; Wallace et al, ), murids (Newton et al, ; Ballion et al, ), and monkeys (Lamotte et al, ). Robust innervation of the SC with descending serotonergic fibers from the raphe is well‐conserved; however, both the number and location of ISNs are variable between species (Schmidt and Jordan, ; Lillesaar, ).…”

Section: Introductionmentioning

confidence: 99%

“…For example, rats have very few, dorsally‐located ISNs, therefore these ISNs are hypothesized to play an autonomic or nociceptive function (Newton and Hamill, ). In contrast, fish have considerably more numerous ISNs that are typically located in the ventral SC, near the locomotor‐generating circuitry that they are believed to modulate (Harris‐Warrick et al, ; Van Dongen et al, ; Van Raamsdonk et al, ; McLean and Fetcho, ). Consistent with this hypothesis, NMDA‐induced locomotor activity is modulated by selective 5HT reuptake inhibitors (SSRIs) in isolated lamprey SCs (Christenson et al, ; Zhang and Grillner, ), demonstrating that 5HT produced by spinally‐intrinsic sources modulates the spinal locomotor network.…”

Section: Introductionmentioning

confidence: 99%

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Intraspinal serotonergic signaling suppresses locomotor activity in larval zebrafish

Montgomery

Wahlstrom‐Helgren

Wiggin

et al. 2018

Developmental Neurobiology

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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. © 2018 Wiley Periodicals, Inc. Develop Neurobiol, 2018.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Intraspinal serotonergic signaling suppresses locomotor activity in larval zebrafish

Montgomery

Wahlstrom‐Helgren

Wiggin

et al. 2018

Developmental Neurobiology

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“…They arise from a different population of precursor cells (the lateral presomitic cells) than red fibers (Devoto et al, ), and make up the bulk of the trunk musculature. They are innervated by a single primary motor neuron and up to three to four secondary motoneurons, (Westerfield et al, ; Liu and Westerfield, ; De Graaf et al, ; Van Raamsdonk et al, ). The majority of mEPCs from 1.5 dpf white fibers exhibited time courses that were long and variable in length, and were well fit by single exponential decays.…”

Section: Discussionmentioning

confidence: 99%

Nicotinic acetylcholine receptors (nAChRs) at zebrafish red and white muscle show different properties during development

Ahmed

Ali

2015

Developmental Neurobiology

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Nicotinic acetylcholine receptors (nAChRs) are highly expressed at the vertebrate neuromuscular junction (NMJ) where they are required for muscle activation. Understanding the factors that underlie NMJ development is critical for a full understanding of muscle function. In this study we performed whole cell and outside-out patch clamp recordings, and single-cell RT-qPCR from zebrafish red and white muscle to examine the properties of nAChRs during the first 5 days of development. In red fibers miniature endplate currents (mEPCs) exhibit single exponential time courses at 1.5 days postfertilization (dpf) and double exponential time courses from 2 dpf onwards. In white fibers, mEPCs decay relatively slowly, with a single exponential component at 1.5 dpf. By 2 and 3 dpf, mEPC kinetics speed up, and decay with a double exponential component, and by 4 dpf the exponential decay reverts back to a single component. Single channel recordings confirm the presence of two main conductance classes of nAChRs (∼45 pS and ∼65 pS) in red fibers with multiple time courses. Two main conductance classes are also present in white fibers (∼55 pS and ∼73 pS), but they exhibit shorter mean open times by 5 dpf compared with red muscle. RT-qPCR of mRNA for nicotinic receptor subunits supports a switch from γ to ε subunits in white fibers but not in red. Our findings provide a developmental profile of mEPC properties from red and white fibers in embryonic and larval zebrafish, and reveal previously unknown differences between the NMJs of these muscle fibers.© 2015 Wiley Periodicals, Inc. Develop Neurobiol 76: 916-936, 2016.

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Ontogeny and innervation patterns of dopaminergic, noradrenergic, and serotonergic neurons in larval zebrafish

McLean

Fetcho

2004

J of Comparative Neurology

246

272

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We report the development of aminergic neurons from 0-10 days postfertilization (dpf) in zebrafish (Danio rerio). This study was prompted by the lack of information regarding patterns of spinal aminergic innervation at early stages, when the fish are accessible to optical, genetic, and electrophysiological approaches toward understanding neural circuit function. Our findings suggest that aminergic populations with descending processes are among the first to appear during development. Descending aminergic fibers, revealed by antibodies to tyrosine hydroxylase (TH) and serotonin (5-hydroxytryptamine; 5-HT), innervate primarily the ventral (TH, 5-HT), but also the dorsal (5-HT) aspects of the spinal cord by 4 dpf, with the extent of innervation not changing markedly up to 10 dpf. By tracking the spatiotemporal expression of TH, 5-HT, and dopamine beta hydroxylase reactivity, we determined that these fibers likely originate from neurons in the posterior tuberculum (dopamine), the raphe region (5-HT) and, possibly, the locus coeruleus (noradrenaline). In addition, spinal neurons positive for 5-HT emerge between 1-2 dpf, with processes that appeared to descend along the ventrolateral cord for only 1-2 muscle segments. Their overall morphology distinguished these cells from previously described "VeMe" (ventromedial) interneurons, which are also located ventromedially, but have long, multisegmental descending processes. We confirmed the distinction between spinal serotonergic and VeMe interneurons using fish genetically labeled with green fluorescent protein. Our results suggest that the major aminergic systems described in adults are in place shortly after hatching, at a time when zebrafish are accessible to a battery of techniques to test neuronal function during behavior.

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Organisation of the Zebrafish Spinal Cord: Distribution of Motoneuron Dendrites and 5-HT containing Cells

Cited by 8 publications

References 0 publications

Intraspinal serotonergic signaling suppresses locomotor activity in larval zebrafish

Intraspinal serotonergic signaling suppresses locomotor activity in larval zebrafish

Nicotinic acetylcholine receptors (nAChRs) at zebrafish red and white muscle show different properties during development

Ontogeny and innervation patterns of dopaminergic, noradrenergic, and serotonergic neurons in larval zebrafish

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