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.
“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
In Results, under “Blocking endogenous D4 receptor signaling prevents maturation of the locomotor pattern” (page unavailable), the authors report that D4 antagonism during 3–4 dpf prevented the normal shift to short swimming episodes at 4 dpf. The Introduction describes the developmental change as a shift from long to short episodes of beat-and-glide swimming, not a transition from burst swimming to beat-and-glide swimming. (LLM, conf=0.85)
Experimental — accuracy not yet measuredBeat-and-glide swimming can be produced in isolated larval zebrafish spinal cord preparations by NMDA application or by optogenetic stimulation of excitatory spinal neurons.
“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
Dopamine from supraspinal sources plays a role in setting the beat-and-glide phenotype by shortening swimming episode duration.
“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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The Tol2kit: A multisite gateway‐based construction kit for Tol2 transposon transgenesis constructs
Kwan, K. M., Fujimoto, E., Grabher, C., Mangum, B. D., Hardy, M., Campbell, D. S., Parant, J. M., Yost, H. J., Kanki, J. P., & Chien, C.-B. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21343 · Cited by 1,778 · see citing works
Zebrafish Behavioral Profiling Links Drugs to Biological Targets and Rest/Wake Regulation
Rihel, J., Prober, D. A., Arvanites, A. C., Lam, K., Zimmerman, S., Jang, S., Haggarty, S. J., Kokel, D., Rubin, L. L., Peterson, R. T., et al. (2010) · Science · doi:10.1126/science.1183090 · Cited by 782 · see citing works
High-throughput ethomics in large groups of Drosophila
Branson, K. M., Robie, A. A., Bender, J. A., Perona, P., & Dickinson, M. H. (2009) · Nature Methods · doi:10.1038/nmeth.1328 · Cited by 781 · see citing works
Rapid behavior-based identification of neuroactive small molecules in the zebrafish
Kokel, D., Bryan, J., Laggner, C., White, R., Cheung, C. Y. J., Mateus, R., Healey, D., Kim, S. N., Werdich, A. A., Haggarty, S. J., et al. (2010) · Nature Chemical Biology · doi:10.1038/nchembio.307 · Cited by 536 · see citing works
Curado, S., Stainier, D. Y. R., & Anderson, R. M. (2008) · Nature Protocols · doi:10.1038/nprot.2008.58 · Cited by 440 · see citing works
(1998) · doi:10.1016/s0165-0173(98)00016-2 · Cited by 398 · see citing works
Catecholamine systems in the brain of vertebrates: new perspectives through a comparative approach
Smeets, W. J. A. J., & González, A. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(00)00034-5 · Cited by 385 · see citing works
Tay, T. L., Ronneberger, O., Ryu, S., Nitschke, R., & Driever, W. (2011) · Nature Communications · doi:10.1038/ncomms1171 · Cited by 307 · see citing works
Holzschuh, J., Ryu, S., Aberger, F., & Driever, W. (2001) · Mechanisms of Development · doi:10.1016/s0925-4773(01)00287-8 · Cited by 280 · see citing works
McLean, D. L., & Fetcho, J. R. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20280 · Cited by 267 · see citing works
Müller, U. K., Stamhuis, E. J., & Videler, J. J. (2000) · Journal of Experimental Biology · doi:10.1242/jeb.203.2.193 · Cited by 231 · see citing works
Behavioural assessments of neurotoxic effects and neurodegeneration in zebrafish
Tierney, K. B. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2010.10.011 · Cited by 218 · see citing works
Orthopedia Homeodomain Protein Is Essential for Diencephalic Dopaminergic Neuron Development
Ryu, S., Mahler, J., Acampora, D., Holzschuh, J., Erhardt, S., Omodei, D., Simeone, A., & Driever, W. (2007) · Current Biology · doi:10.1016/j.cub.2007.04.003 · Cited by 193 · see citing works
Prey capture by larval zebrafish: evidence for fine axial motor control
Borla, M. A., Palecek, B., Budick, S., & O’Malley, D. M. (2002) · Brain, Behavior and Evolution · doi:10.1159/000066699 · Cited by 180 · cited 1× · see citing works
“A developmental switch in the episodic locomotor pattern from long to short swimming episodes is observed between 3 and 4 days postfertilization (dpf) (Buss and Drapeau, 2001), which is concurrent with increased locomotion and the advent of foraging (Borla et al., 2002).”
BackgroundSynaptic drive to motoneurons during fictive swimming in the developing zebrafish
Buss, R. R., & Drapeau, P. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.1.197 · Cited by 177 · see citing works
Ontogeny of routine swimming activity and performance in zebra danios (Teleostei: Cyprinidae)
Fuiman, L. A., & Webb, P. W. (1988) · Animal Behaviour · doi:10.1016/s0003-3472(88)80268-9 · Cited by 171 · see citing works
Evolution and expression of D2 and D3 dopamine receptor genes in zebrafish
Boehmler, W., Obrecht‐Pflumio, S., Canfield, V. A., Thisse, C., Thisse, B., & Levenson, R. G. (2004) · Developmental Dynamics · doi:10.1002/dvdy.20075 · Cited by 170 · see citing works
Fictive Swimming Motor Patterns in Wild Type and Mutant Larval Zebrafish
Masino, M. A., & Fetcho, J. R. (2005) · Journal of Neurophysiology · doi:10.1152/jn.01248.2004 · Cited by 164 · see citing works
Self-citationBoehmler, W., Carr, T., Thisse, C., Thisse, B., Canfield, V. A., & Levenson, R. G. (2006) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2006.00243.x · Cited by 146 · see citing works
Projections of diencephalic dopamine neurons into the spinal cord in mice
Qu, S., Ondo, W. G., Zhang, X., Xie, W., Pan, T. H., & Le, W. D. (2005) · Experimental Brain Research · doi:10.1007/s00221-005-0075-1 · Cited by 134 · see citing works
Lindsey, B. W., Smith, F. M., & Croll, R. P. (2010) · Zebrafish · doi:10.1089/zeb.2009.0616 · Cited by 130 · see citing works
Endogenous Dopamine Suppresses Initiation of Swimming in Prefeeding Zebrafish Larvae
Thirumalai, V., & Cline, H. T. (2008) · Journal of Neurophysiology · doi:10.1152/jn.90568.2008 · Cited by 128 · see citing works
Brustein, E., Chong, M., Holmqvist, B., & Drapeau, P. (2003) · Journal of Neurobiology · doi:10.1002/neu.10292 · Cited by 126 · see citing works
McLean, D. L., & Fetcho, J. R. (2004) · Journal of Comparative Neurology · doi:10.1002/cne.20281 · Cited by 124 · see citing works
Kastenhuber, E., Kratochwil, C. F., Ryu, S., Schweitzer, J., & Driever, W. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22214 · Cited by 120 · see citing works
Pathophysiological concepts of restless legs syndrome
Paulus, W., Dowling, P., Rijsman, R. M., Stiasny‐Kolster, K., Trenkwalder, C., & de Weerd, A. (2007) · Movement Disorders · doi:10.1002/mds.21533 · Cited by 118 · see citing works
Locomotion Is Increased in A11-Lesioned Mice With Iron Deprivation
Qu, S., Le, W., Zhang, X., Xie, W., Zhang, A., & Ondo, W. G. (2007) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e3180517b5f · Cited by 112 · see citing works
Dopaminergic Modulation of Spinal Neuronal Excitability
Han, P., Nakanishi, S. T., Tran, M. A., & Whelan, P. J. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1279-07.2007 · Cited by 112 · see citing works
Zhu, H., Clemens, S., Sawchuk, M. A., & Hochman, S. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.07.052 · Cited by 106 · see citing works
Taniguchi, W., Nakatsuka, T., Miyazaki, N., Yamada, H., Takeda, D., Fujita, T., Kumamoto, E., & Yoshida, M. (2010) · Pain · doi:10.1016/j.pain.2010.09.034 · Cited by 105 · see citing works
Zhao, H., Zhu, W., Pan, T., Xie, W., Zhang, A., Ondo, W. G., & Le, W. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21207 · Cited by 104 · see citing works
Antipsychotics produce locomotor impairment in larval zebrafish
Giacomini, N. J., Rose, B. T., Kobayashi, K., & Guo, S. (2006) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.01.013 · Cited by 102 · see citing works
Souza, B. R., Romano‐Silva, M. A., & Tropepe, V. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5548-10.2011 · Cited by 84 · see citing works
Nitroreductase-Mediated Cell Ablation in Transgenic Zebrafish Embryos
Pisharath, H., & Parsons, M. J. (2009) · Methods in molecular biology · doi:10.1007/978-1-60327-977-2_9 · Cited by 83 · see citing works
Rhythmic motor activity evoked by NMDA in the spinal zebrafish larva
McDearmid, J. R., & Drapeau, P. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00844.2005 · Cited by 79 · see citing works
Motmot, an open-source toolkit for realtime video acquisition and analysis
Straw, A. D., & Dickinson, M. H. (2009) · Source Code for Biology and Medicine · doi:10.1186/1751-0473-4-5 · Cited by 76 · see citing works
Single thalamic dopaminergic neurons project to both the neocortex and spinal cord
Takada, M., Li, Z. K., & Hattori, T. (1988) · Brain Research · doi:10.1016/0006-8993(88)90093-5 · Cited by 68 · see citing works
Farrell, T. C., Cario, C. L., Milanese, C., Vogt, A., Jeong, J., & Burton, E. A. (2011) · Neurobiology of Disease · doi:10.1016/j.nbd.2011.05.016 · Cited by 66 · see citing works
Molecular cloning and developmental expression of foxP2 in zebrafish
Bonkowsky, J. L., & Chien, C.-B. (2005) · Developmental Dynamics · doi:10.1002/dvdy.20504 · Cited by 62 · see citing works
Self-citationDomain-specific regulation of foxP2 CNS expression by lef1
Bonkowsky, J. L., Wang, X., Fujimoto, E., Lee, J. E., Chien, C.-B., & Dorsky, R. I. (2008) · BMC Developmental Biology · doi:10.1186/1471-213x-8-103 · Cited by 59 · see citing works
Self-citationDopamine Release in the Prefrontal Cortex and Striatum: Temporal and Behavioural Aspects
Hauber, W. (2010) · Pharmacopsychiatry · doi:10.1055/s-0030-1248300 · Cited by 56 · see citing works
l-DOPA-induced air-stepping in developing rats
Hartesveldt, C. V., Sickles, A. E., Porter, J. D., & Stehouwer, D. J. (1991) · Developmental Brain Research · doi:10.1016/0165-3806(91)90012-8 · Cited by 53 · see citing works
L-DOPA and quipazine elicit air-stepping in neonatal rats with spinal cord transections.
McEwen, M. L., Hartesveldt, C. V., & Stehouwer, D. J. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.4.825 · Cited by 52 · see citing works
Fujimoto, E., Stevenson, T. J., Chien, C.-B., & Bonkowsky, J. L. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.01.023 · Cited by 37 · see citing works
Self-citationDopamine D1 and D2 antagonists block l-DOPA-elicited air-stepping in neonatal rats
Sickles, A. E., Stehouwer, D. J., & Hartesveldt, C. V. (1992) · Developmental Brain Research · doi:10.1016/0165-3806(92)90243-p · Cited by 21 · see citing works
Dopamine D1 and D2 antagonists block l-DOPA-induced air-stepping in decerebrate neonatal rats
McCrea, A. E., Stehouwer, D. J., & Hartesveldt, C. V. (1997) · Developmental Brain Research · doi:10.1016/s0165-3806(97)00027-8 · Cited by 19 · see citing works
Imaging to Differentiate Between Ischemic and Nonischemic Cardiomyopathy
Bax, J. J., Poldermans, D., Schuijf, J. D., Scholte, A. J. H. A., Elhendy, A., & van der Wall, E. E. (2006) · Heart Failure Clinics · doi:10.1016/j.hfc.2006.01.003 · Cited by 8 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Reiner A Medina L Veenman CL Structural and functional evolution of the basal ganglia in vertebrates Brain Res Brain Res Rev 1998 28 235 285 9858740
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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 · see citing works
Dopamine: a parallel pathway for the modulation of spinal locomotor networks
Sharples, S. A., Koblinger, K., Humphreys, J. M., & Whelan, P. J. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00055 · Cited by 155 · see citing works
ZebraZoom: an automated program for high-throughput behavioral analysis and categorization
Mirat, O., Sternberg, J. R., Severi, K. E., & Wyart, C. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00107 · Cited by 143 · see citing works
Reimer, M. M., Norris, A., Ohnmacht, J., Patani, R., Zhong, Z., Dias, T. B., Kuscha, V., Scott, A. L. M., Chen, Y., Rozov, S. V., et al. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.04.012 · Cited by 141 · see citing works
Norepinephrine is required to promote wakefulness and for hypocretin-induced arousal in zebrafish
Singh, C., Oikonomou, G., & Prober, D. A. (2015) · eLife · doi:10.7554/elife.07000 · Cited by 133 · see citing works
Characterization of A11 neurons projecting to the spinal cord of mice
Koblinger, K., Füzesi, T., Ejdrygiewicz, J., Krajacic, A., Bains, J. S., & Whelan, P. J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0109636 · Cited by 114 · see citing works
Multiple convergent hypothalamus–brainstem circuits drive defensive behavior
Lovett-Barron, M., Chen, R., Bradbury, S., Andalman, A. S., Wagle, M. D., Guo, S., & Deisseroth, K. A. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0655-1 · Cited by 110 · see citing works
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Tosches, M. A., & Arendt, D. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.09.005 · Cited by 106 · see citing works
Spulber, S., Kilian, P., Wan Ibrahim, W. N., Onishchenko, N., Ulhaq, M., Norrgren, L., Negri, S., Di Tuccio, M., & Ceccatelli, S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094227 · Cited by 98 · see citing works
Ingebretson, J. J., & Masino, M. A. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00109 · Cited by 97 · see citing works
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Becker, C. G., & Becker, T. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.01.001 · Cited by 97 · see citing works
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Pantoja, C., Hoagland, A., Carroll, E. C., Karalis, V., Conner, A. F., & Isacoff, E. Y. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.016 · Cited by 100 · see citing works
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Berg, E. M., Björnfors, E. R., Pallucchi, I., Picton, L. D., & Manira, A. E. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00073 · Cited by 98 · see citing works
Pujala, A., & Koyama, M. (2019) · eLife · doi:10.7554/elife.42135 · Cited by 80 · see citing works
Shams, S., Amlani, S., Buske, C., Chatterjee, D., & Gerlai, R. T. (2017) · Developmental Psychobiology · doi:10.1002/dev.21581 · Cited by 91 · see citing works
Olfactory projectome in the zebrafish forebrain revealed by genetic single-neuron labelling
Miyasaka, N., Arganda‐Carreras, I., Wakisaka, N., Masuda, M., Sümbül, U., Seung, H. S., & Yoshihara, Y. (2014) · Nature Communications · doi:10.1038/ncomms4639 · Cited by 84 · see citing works
Jay, M., De Faveri, F., & McDearmid, J. R. (2015) · Current Biology · doi:10.1016/j.cub.2014.12.033 · Cited by 82 · see citing works
Shams, S., Séguin, D., Facciol, A., Chatterjee, D., & Gerlai, R. T. (2017) · Behavioral Neuroscience · doi:10.1037/bne0000220 · Cited by 81 · see citing works
Wasel, O., & Freeman, J. L. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21175981 · Cited by 80 · see citing works
Silva, M. H. (2020) · Birth Defects Research · doi:10.1002/bdr2.1661 · Cited by 78 · see citing works
Mathias, J. R., Zhang, Z., Saxena, M. T., & Mumm, J. S. (2014) · Zebrafish · doi:10.1089/zeb.2013.0937 · Cited by 70 · see citing works
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Kim, L. H., Sharma, S., Sharples, S. A., Mayr, K. A., Kwok, C. H. T., & Whelan, P. J. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00581 · Cited by 70 · see citing works
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Horstick, E. J., Bayleyen, Y., Sinclair, J. L., & Burgess, H. A. (2017) · BMC Biology · doi:10.1186/s12915-016-0346-2 · Cited by 61 · see citing works
Godoy, R. S., Noble, S., Yoon, K., Anisman, H., & Ekker, M. (2015) · Journal of Neurochemistry · doi:10.1111/jnc.13214 · Cited by 59 · see citing works
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Sharples, S. A., Burma, N. E., Borowska-Fielding, J., Kwok, C. H. T., Eaton, S. E. A., Baker, G. B., Jean-Xavier, C., Zhang, Y., Trang, T., & Whelan, P. J. (2020) · Scientific Reports · doi:10.1038/s41598-020-73230-w · Cited by 58 · see citing works
McPherson, A. D., Barrios, J. P., Luks-Morgan, S. J., Manfredi, J. P., Bonkowsky, J. L., Douglass, A. D., & Dorsky, R. I. (2016) · Current Biology · doi:10.1016/j.cub.2015.11.064 · Cited by 57 · see citing works
Self-citationLaar, V. S. V., Chen, J., Zharikov, A., Bai, Q., Maio, R. D., Dukes, A. A., Hastings, T. G., Watkins, S. C., Greenamyre, J. T., Croix, C. M. S., et al. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101695 · Cited by 56 · see citing works
Onaolapo, A. Y., Onaolapo, O. J., & Nwoha, P. U. (2016) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2016.08.006 · Cited by 56 · see citing works
Onaolapo, O. J., Adekola, M. A., Azeez, T. O., Salami, K., & Onaolapo, A. Y. (2016) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2016.11.033 · Cited by 56 · see citing works
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Bergemann, D., Massoz, L., Bourdouxhe, J., Pardo, C. C., Voz, M. L., Peers, B., & Manfroid, I. (2018) · Wound Repair and Regeneration · doi:10.1111/wrr.12633 · Cited by 52 · see citing works
Chen, S., Qin, Y., Ye, X., Liu, J., Yan, X., Zhou, L., Wang, X., Martyniuk, C. J., & Yan, B. (2023) · Environmental Science & Technology · doi:10.1021/acs.est.3c06284 · Cited by 51 · see citing works
Dukes, A. A., Bai, Q., Laar, V. S. V., Zhou, Y., Ильин, В. Н., David, C. N., Ağım, Z. S., Bonkowsky, J. L., Cannon, J. R., Watkins, S. C., et al. (2016) · Neurobiology of Disease · doi:10.1016/j.nbd.2016.07.020 · Cited by 50 · see citing works
Self-citationCaldwell, L. J., Davies, N. O., Cavone, L., Mysiak, K. S., Semenova, S. A., Panula, P., Armstrong, J. D., Becker, C. G., & Becker, T. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.2706-18.2019 · Cited by 49 · see citing works
Strachan, L. R., Stevenson, T. J., Freshner, B., Keefe, M. D., Miranda Bowles, D., & Bonkowsky, J. L. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx249 · Cited by 46 · see citing works
Self-citationLange, M., Froc, C., Grunwald, H. A., Norton, W., & Bally‐Cuif, L. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.02.010 · Cited by 46 · see citing works
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Koblinger, K., Jean-Xavier, C., Sharma, S., Füzesi, T., Young, L., Eaton, S. E. A., Kwok, C. H. T., Bains, J. S., & Whelan, P. J. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00086 · Cited by 46 · see citing works
Decker-Farrell, A. R., McNeill, M., Lambert, A. M., Overton, J. D., Chen, Y.-C., Lorca, R. A., Johnson, N. A., Brockerhoff, S. E., Mohapatra, D. P., Macarthur, H., et al. (2013) · Developmental Biology · doi:10.1016/j.ydbio.2013.11.015 · Cited by 44 · see citing works
Self-citationChakravarthy, V. S., Balasubramani, P. P., Mandali, A., Jahanshahi, M., & Moustafa, A. A. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.06.032 · Cited by 43 · see citing works
Intraspinal serotonergic signaling suppresses locomotor activity in larval zebrafish
Montgomery, J. E., Wahlstrom‐Helgren, S., Wiggin, T. D., Corwin, B. M., Lillesaar, C., & Masino, M. A. (2018) · Developmental Neurobiology · doi:10.1002/dneu.22606 · Cited by 40 · see citing works
Self-citationHypoxia and connectivity in the developing vertebrate nervous system
Bonkowsky, J. L., & Son, J. (2018) · Disease Models & Mechanisms · doi:10.1242/dmm.037127 · Cited by 40 · see citing works
Self-citationModeling spinal locomotor circuits for movements in developing zebrafish
Roussel, Y., Gaudreau, S. F., Kacer, E. R., Sengupta, M., & Bui, T. V. (2021) · eLife · doi:10.7554/elife.67453 · Cited by 39 · see citing works
Bakthavatsalam, S., Sharma, S. D., Sonawane, M. S., Thirumalai, V., & Datta, A. (2014) · Disease Models & Mechanisms · doi:10.1242/dmm.016683 · Cited by 39 · see citing works
Haehnel, M., Fernandes, A. M., Böhler, M., Schmitt, I., Tittel, L., & Driever, W. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00020 · Cited by 36 · see citing works
Neurotoxicity and gene expression alterations in zebrafish larvae in response to manganese exposure
Xu, Y., Peng, T., Xiang, Y., Liao, G., Zou, F., & Meng, X. (2022) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2022.153778 · Cited by 36 · see citing works
Montgomery, J. E., Wiggin, T. D., Rivera-Pérez, L. M., Lillesaar, C., & Masino, M. A. (2015) · Developmental Neurobiology · doi:10.1002/dneu.22352 · Cited by 36 · see citing works
Self-citationDopamine system, cerebellum, and nucleus ruber in fish and mammals
Matsui, H. (2017) · Development Growth & Differentiation · doi:10.1111/dgd.12357 · Cited by 34 · see citing works
Naderi, M., Ferrari, M. C. O., Chivers, D. P., & Niyogi, S. (2018) · Environmental Science & Technology · doi:10.1021/acs.est.8b04768 · Cited by 32 · see citing works
Onaolapo, A. Y., Abdusalam, S. Z., & Onaolapo, O. J. (2017) · Pathophysiology · doi:10.1016/j.pathophys.2017.01.002 · Cited by 31 · see citing works
Jha, U., & Thirumalai, V. (2020) · Current Biology · doi:10.1016/j.cub.2019.12.064 · Cited by 32 · see citing works
Godoy, R. S., Hua, K., Kalyn, M., Cusson, V.-M., Anisman, H., & Ekker, M. (2020) · Scientific Reports · doi:10.1038/s41598-020-69734-0 · Cited by 30 · see citing works
Neuromodulation and Behavioral Flexibility in Larval Zebrafish: From Neurotransmitters to Circuits
Corradi, L., & Filosa, A. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.718951 · Cited by 28 · see citing works
Xing, L., Son, J., Stevenson, T. J., Lillesaar, C., Bally‐Cuif, L., Dahl, T. M., & Bonkowsky, J. L. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1295-15.2015 · Cited by 29 · see citing works
Self-citationDopamine D1 and D2 receptor antagonism during development alters later behavior in zebrafish
Oliveri, A. N., & Levin, E. D. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.08.028 · Cited by 27 · see citing works
Luchtenburg, F. J., Schaaf, M. J. M., & Richardson, M. K. (2019) · Psychopharmacology · doi:10.1007/s00213-019-05193-4 · Cited by 31 · see citing works
Exposure to D2-like dopamine receptor agonists inhibits swimming in Daphnia magna
Barrozo, E. R., Fowler, D. A., & Beckman, M. L. (2015) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2015.08.010 · Cited by 27 · see citing works
Forlano, P. M., Licorish, R. R., Ghahramani, Z. N., Timothy, M., Ferrari, M., Palmer, W. C., & Sisneros, J. A. (2017) · Integrative and Comparative Biology · doi:10.1093/icb/icx053 · Cited by 25 · see citing works
Pierre, C., Pradère, N., Froc, C., Ornelas‐García, C. P., Callebert, J., & Rétaux, S. (2020) · Journal of Experimental Biology · doi:10.1242/jeb.226092 · Cited by 25 · see citing works
Vanishing white matter disease expression of truncated EIF2B5 activates induced stress response
Keefe, M. D., Soderholm, H. E., Shih, H., Stevenson, T. J., Glaittli, K. A., Bowles, D. M., Scholl, E. A., Colby, S., Merchant, S. S., Hsu, E. W., et al. (2020) · eLife · doi:10.7554/elife.56319 · Cited by 25 · see citing works
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Hageter, J., Waalkes, M., Starkey, J., Copeland, H., Price, H., Bays, L. D., Showman, C., Laverty, S. M., Bergeron, S. A., & Horstick, E. J. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.777778 · Cited by 23 · see citing works
Developmental changes in head movement kinematics during swimming inXenopus laevistadpoles
Hänzi, S., & Straka, H. (2016) · Journal of Experimental Biology · doi:10.1242/jeb.146449 · Cited by 24 · see citing works
Hachoumi, L., & Sillar, K. T. (2019) · Developmental Neurobiology · doi:10.1002/dneu.22725 · Cited by 24 · see citing works
Nabinger, D. D., Altenhofen, S., Peixoto, J. V., da Silva, J. M. K., Gerlai, R. T., & Bonan, C. D. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110179 · Cited by 24 · see citing works
Currie, S. P., Combes, D., Scott, N. W., Simmers, J., & Sillar, K. T. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00283.2015 · Cited by 23 · see citing works
A robust and tunable system for targeted cell ablation in developing embryos
Labbaf, Z., Petratou, K., Ermlich, L., Backer, W., Tarbashevich, K., Reichman‐Fried, M., Luschnig, S., Schulte‐Merker, S., & Raz, E. (2022) · Developmental Cell · doi:10.1016/j.devcel.2022.07.008 · Cited by 22 · see citing works
Athira, A., Dondorp, D. C., Rudolf, J., Peytral, O., & Chatzigeorgiou, M. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001744 · Cited by 21 · see citing works
Optimizing assays of zebrafish larvae swimming performance for drug discovery
Widrick, J. J., Lambert, M. R., Kunkel, L. M., & Beggs, A. H. (2023) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2023.2211802 · Cited by 21 · see citing works
Neuromodulation in developing motor microcircuits
Sillar, K. T., Combes, D., & Simmers, J. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.05.009 · Cited by 21 · see citing works
Full Anatomical Recovery of the Dopaminergic System after a Complete Spinal Cord Injury in Lampreys
Fernández‐López, B., Romaus‐Sanjurjo, D., Cornide‐Petronio, M. E., Gómez-Fernández, S., Barreiro‐Iglesias, A., & Rodicio, M. C. (2015) · Neural Plasticity · doi:10.1155/2015/350750 · Cited by 20 · see citing works
Wiggin, T. D., Peck, J. H., & Masino, M. A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0109117 · Cited by 20 · see citing works
Self-citationGutierrez-Triana, J. A., Herget, U., Lichtner, P., Castillo-Ramírez, L. A., & Ryu, S. (2014) · BMC Developmental Biology · doi:10.1186/preaccept-1743418341322888 · Cited by 18 · see citing works
A zebrafish model of hyperammonemia
Feldman, B., Tuchman, M., & Caldovic, L. (2014) · Molecular Genetics and Metabolism · doi:10.1016/j.ymgme.2014.07.001 · Cited by 20 · see citing works
Somatostatin 1.1 contributes to the innate exploration of zebrafish larva
Quan, F. B., Desban, L., Mirat, O., Kermarquer, M., Roussel, J., Koëth, F., Marnas, H., Djenoune, L., Lejeune, F., Tostivint, H., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-72039-x · Cited by 19 · see citing works
Learning steers the ontogeny of an efficient hunting sequence in zebrafish larvae
Lagogiannis, K., Diana, G., & Meyer, M. P. (2020) · eLife · doi:10.7554/elife.55119 · Cited by 18 · see citing works
Picton, L. D., & Sillar, K. T. (2016) · Scientific Reports · doi:10.1038/srep35749 · Cited by 18 · see citing works
Nabinger, D. D., Altenhofen, S., Buatois, A., Facciol, A., Peixoto, J. V., da Silva, J. M. K., Chatterjee, D., Rübensam, G., Gerlai, R. T., & Bonan, C. D. (2023) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2023.110753 · Cited by 15 · see citing works
Kim, S. S., Lee, S., Eghan, K., Yoo, D., Chun, H., & Kim, W. (2024) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2024.117350 · Cited by 15 · see citing works
Yamamoto, N., Nakayama, T., & Hagio, H. (2017) · Development Growth & Differentiation · doi:10.1111/dgd.12355 · Cited by 15 · see citing works
Social Status-Related Differences in Motor Activity Between Wild-Type and Mutant Zebrafish
Clements, K. N., Miller, T. H., Keever, J. M., Hall, A. M., & Issa, F. A. (2018) · Biological Bulletin · doi:10.1086/699514 · Cited by 15 · see citing works
Wahlstrom-Helgren, S., Montgomery, J. E., Vanpelt, K. T., Biltz, S. L., Peck, J. H., & Masino, M. A. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00337.2019 · Cited by 14 · see citing works
Self-citationRoussel, Y., Paradis, M., Gaudreau, S. F., Lindsey, B. W., & Bui, T. V. (2020) · eneuro · doi:10.1523/eneuro.0508-18.2020 · Cited by 14 · see citing works
Cuprizone-induced dopaminergic hyperactivity and locomotor deficit in zebrafish larvae
Liu, M., Zheng, P., Zheng, M., Zhang, W., Yang, F., Hong, L., Yu, X., & Xu, H. (2022) · Brain Research · doi:10.1016/j.brainres.2022.147802 · Cited by 14 · see citing works
Qi, Z., Zhai, Y., Han, Y., Li, K., Wang, T., Li, P., Li, J., Zhou, X., Zhao, X., & Song, W. (2024) · Environmental Science & Technology · doi:10.1021/acs.est.4c06892 · Cited by 14 · see citing works
Bhat, S. K., & Ganesh, C. B. (2017) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2017.05.004 · Cited by 14 · see citing works
Licitra, R., Martinelli, M., Jasinski, L. P., Marchese, M., Kiferle, C., & Fronte, B. (2021) · Pharmaceuticals · doi:10.3390/ph14121224 · Cited by 14 · see citing works
Long-lasting behavioral effects of quinpirole exposure on zebrafish
Nabinger, D. D., Altenhofen, S., Peixoto, J. V., da Silva, J. M. K., & Bonan, C. D. (2021) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2021.107034 · Cited by 14 · see citing works
Fasano, G., Godoy, R. S., Angiulli, E., Consalvo, A., Franco, C., Mancini, M., Santucci, D., Alleva, E., Ciavardelli, D., Toni, M., et al. (2021) · Environmental Pollution · doi:10.1016/j.envpol.2021.117151 · Cited by 13 · see citing works
Zebrafish as a Model for Revealing the Neuronal Basis of Behavior
McArthur, K. L., Chow, D. M., & Fetcho, J. R. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-812431-4.00046-4 · Cited by 13 · see citing works
Pagiazitis, J. G., Delestrée, N., Sowoidnich, L., Sivakumar, N., Simon, C. M., Chatzisotiriou, A., Albani, M., & Mentis, G. Z. (2025) · Cell Reports · doi:10.1016/j.celrep.2024.115147 · Cited by 11 · see citing works
Wasser‐Bennett, G., Brown, A. R., Maynard, S. K., Owen, S. F., & Tyler, C. R. (2025) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.70031 · Cited by 11 · see citing works
Son, J., Stevenson, T. J., Bowles, M. D., Scholl, E. A., & Bonkowsky, J. L. (2020) · eNeuro · doi:10.1523/eneuro.0355-19.2020 · Cited by 11 · see citing works
Self-citationChen, S., Wang, X., Ye, X., Qin, Y., Wang, H., Liang, Z., Zhu, L., Zhou, L., Martyniuk, C. J., & Yan, B. (2023) · Chemosphere · doi:10.1016/j.chemosphere.2023.139861 · Cited by 10 · see citing works
Koleilat, A., Dugdale, J. A., Christenson, T. A., Bellah, J. L., Lambert, A. M., Masino, M. A., Ekker, S. C., & Schimmenti, L. A. (2020) · Disease Models & Mechanisms · doi:10.1242/dmm.043885 · Cited by 10 · see citing works
Self-citationDolutegravir and Folic Acid Interaction during Neural System Development in Zebrafish Embryos
Zizioli, D., Quirós-Roldán, E., Ferretti, S., Mignani, L., Tiecco, G., Monti, E., Castelli, F., & Zanella, I. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25094640 · Cited by 9 · see citing works
Derksen, A., Shih, H., Forget, D., Darbelli, L., Tran, L. T., Poitras, C., Guerrero, K., Tharun, S., Alkuraya, F. S., Kurdi, W., et al. (2021) · Human Genetics and Genomics Advances · doi:10.1016/j.xhgg.2021.100034 · Cited by 9 · see citing works
Self-citationLi, S., Shi, W., Ma, D.-D., Zhang, J., Lu, Z., Long, X.-B., Liu, X., Huang, C.-S., & Ying, G. (2024) · Bulletin of Environmental Contamination and Toxicology · doi:10.1007/s00128-024-03883-0 · Cited by 9 · see citing works
Sharples, S. A., Parker, J. R., Vargas, A., Milla-Cruz, J. J., Lognon, A. P., Cheng, N., Young, L., Shonak, A., Cymbalyuk, G., & Whelan, P. J. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.715427 · Cited by 9 · see citing works
Kandeil, M. A., Mohammed, E. T., Radi, R. A., Khalıl, F., Abdel‐Razik, A. H., Abdel‐Daim, M. M., & Safwat, G. M. (2021) · Journal of Toxicology · doi:10.1155/2021/4411316 · Cited by 9 · see citing works
Blecharz‐Klin, K., Pyrzanowska, J., Piechal, A., Joniec‐Maciejak, I., Wawer, A., Jawna, K., Mirowska-Guzel, D. M., & Widy‐Tyszkiewicz, E. (2024) · Journal of Pre-Clinical and Clinical Research · doi:10.26444/jpccr/178182 · Cited by 8 · see citing works
- 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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