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The Conserved Dopaminergic Diencephalospinal Tract Mediates Vertebrate Locomotor Development in Zebrafish Larvae
Open accessAbstract
The most conserved part of the vertebrate dopaminergic system is the orthopedia ( otp )-expressing diencephalic neuronal population that constitutes the dopaminergic diencephalospinal tract (DDT). Although studies in the neonatal murine spinal cord in vitro suggest an early locomotor role of the DDT, the function of the DDT in developing vertebrates in vivo remains unknown. Here, we investigated the role of the DDT in the locomotor development of zebrafish larvae. To assess the development of the behavioral and neural locomotor pattern, we used high-throughput video tracking in combination with peripheral nerve recordings. We found a behavioral and neural correspondence in the developmental switch from an immature to mature locomotor pattern. Blocking endogenous dopamine receptor 4 (D 4 R) signaling in vivo either before or after the developmental switch prevented or reversed the switch, respectively. Spinal transections of post-switch larvae reestablished the immature locomotor pattern, which was rescued to a mature-like pattern via spinal D 4 R agonism. Selective chemogenetic ablation of otp b ( otpb ) neurons that contribute to the DDT perpetuated the immature locomotor pattern in vivo . This phenotype was recapitulated by diencephalic transections that removed the dopaminergic otpb population and was rescued to a mature-like locomotor pattern by D 4 R agonism. We conclude that the dopaminergic otpb population, via the DDT, is responsible for spinal D 4 R signaling to mediate the developmental switch to the mature locomotor pattern of zebrafish. These results, integrated with the mammalian literature, suggest that the DDT represents an evolutionarily conserved neuromodulatory system that is necessary for normal vertebrate locomotor development.
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“Blocking D4 dopamine receptors at 3 dpf prevents the transition from burst to beat-and-glide swimming (Lambert et al., 2012), suggesting that dopamine from supraspinal sources plays a role in setting the beat-and-glide phenotype by shortening swimming episode duration.”
From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Lambert et al., 2012
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“Beat-and-glide swimming can be produced in isolated larval zebrafish spinal cord preparations by NMDA application (Lambert et al., 2012; McDearmid and Drapeau, 2006; Wiggin et al., 2012) or by optogenetic stimulation of excitatory spinal neurons (Wahlstrom-Helgren et al., 2019).”
From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Lambert et al., 2012
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“Blocking D4 dopamine receptors at 3 dpf prevents the transition from burst to beat-and-glide swimming (Lambert et al., 2012), suggesting that dopamine from supraspinal sources plays a role in setting the beat-and-glide phenotype by shortening swimming episode duration.”
From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Lambert et al., 2012
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Zebrafish Behavioral Profiling Links Drugs to Biological Targets and Rest/Wake Regulation
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Randlett, O., Wee, C. L., Naumann, E. A., Nnaemeka, O., Schoppik, D., Fitzgerald, J. E., Portugues, R., Lacoste, A. M. B., Riegler, C., Engert, F., et al. (2015) · Nature Methods · doi:10.1038/nmeth.3581 · Cited by 528
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Metadata
- Authors
- Lambert, A. M., Bonkowsky, J. L., & Masino, M. A.
- Affiliations
- University of Minnesota (US)
- University of Utah (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2012-09-26
- Volume
- 32
- Issue
- 39
- Pages
- 13488-13500
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3481997
- OpenAlex
- W2074791476
- Cited by
- 152
- References
- 47
- Citations by year
- 2026: 7 · 2025: 13 · 2024: 6 · 2023: 5 · 2022: 9 · 2021: 13 · 2020: 22 · 2019: 11 · 2018: 13 · 2017: 12 · 2016: 10 · 2015: 12 · 2014: 12 · 2013: 6 · 2012: 1
- FWCI
- 4.70
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Minnesota
- Vlaamse regering
- National Institutes of Health
- National Institute of Mental Health (DP2MH100008)
- National Institute on Drug Abuse (T32DA022616, K08DA024753)
- National Institute of Neurological Disorders and Stroke (R01NS065054)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- locomotor development, zebrafish larvae, spinal cord, neuromodulation
- MeSH terms
- Analysis of Variance, Animals, Diencephalon, Dopamine, Dose-Response Relationship, Drug, Electrophysiology, Larva, Locomotion, Metronidazole, Neural Pathways, Neurons, Nitroreductases, Peripheral Nervous System Diseases, Peripheral Nerves, Spinal Cord, Transcription Factors, Video Recording, Zebrafish, Dopamine Agents, Signal Transduction, N-Methylaspartate, Excitatory Amino Acid Agonists, In Situ Nick-End Labeling, Zebrafish Proteins, Animals, Genetically Modified, Green Fluorescent Proteins, Receptors, Dopamine D4
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