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alx , a Zebrafish Homolog of Chx10 , Marks Ipsilateral Descending Excitatory Interneurons That Participate in the Regulation of Spinal Locomotor Circuits
Open accessAbstract
Recent molecular genetic studies suggest that the expression of transcription factors in the developing spinal cord helps determine the morphological and physiological properties of neurons. Using the zebrafish preparation, we have examined the properties of neurons marked by alx , a zebrafish homolog of mammalian Chx10 . We performed morphological and physiological studies using transgenic zebrafish expressing fluorescent reporter constructs in cells that had at any time point expressed alx ( alx neurons). Our data reveal that zebrafish alx neurons are all ipsilateral descending neurons that are positive for vesicular glutamate transporter 2, suggesting that they are glutamatergic excitatory interneurons. Patch recordings show that earlier-born neurons are active during stronger movements such as escapes and fast swimming (strong movement class), whereas later-born ones are involved in sustained weak swimming (weak movement class). Paired recordings between alx neurons and motoneurons show that neurons of the strong movement class make frequent monosynaptic excitatory connections onto motoneurons. Thus, neurons of this class are likely premotor interneurons that regulate motoneuron activity during escapes and fast swimming. We also show the existence of a monosynaptic connection between an alx neuron of the weak movement class and a motoneuron. Collectively, our data demonstrate that alx marks ipsilateral descending neurons that are involved in the regulation of motoneuron activity during forms of locomotion, such as escape and swimming.
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“In R7/R8, the former were found to have somata primarily within a medial glutamatergic parasagittal stripe associated with the Alx transcription factor and the latter with a more lateral GABAergic parasagittal stripe associated with the Abx1b transcription factor21,95,96.”
From Predicting modular functions and neural coding of behavior from a synaptic wiring diagram (2024) · cites this paper as [95]
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“To obtain isolated labeling in transgenic fish for morphological analysis, we used the Cre/loxP recombination system (Gu et al., 1994).”
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“To generate alx reporter constructs, we followed the method by Lee et al. (2001), which uses BAC homologous recombination system (a gift from N. Copeland, National Cancer Institute, Frederick, MD).”
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Grillner, S. E. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1137 · Cited by 839 · cited 1×
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BackgroundI-SceI meganuclease mediates highly efficient transgenesis in fish
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“The converted Kaede remains stable for several days (Hatta et al., 2006; Kimura et al., 2006).”
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“Given the striking parallels between well-characterized components of the locomotor network in zebrafish and mouse [12,48], it will be important to follow development of these Mnx1 interneurons in vivo to learn their origins.”
InfluentialZC4H2, an XLID gene, is required for the generation of a specific subset of CNS interneurons
May, M. M., Hwang, K.-S., Miles, J. H., Williams, C., Niranjan, T. S., Kahler, S. G., Chiurazzi, P., Steindl, K., van der Spek, P. J., Swagemakers, S. M. A., et al. (2015) · Human Molecular Genetics · doi:10.1093/hmg/ddv208 · Cited by 60
“However, in mutant embryos, expression of both vsx2, which labels V2a interneurons (6), and vsx1, which labels V2a/b interneuron precursors (7), was significantly decreased throughout the CNS (Figs 4E,F and 5A–D).”
BackgroundRegulation of locomotor speed and selection of active sets of neurons by V1 neurons
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Self-citationMovement, technology and discovery in the zebrafish
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“Work in the spinal cord suggests that networks differentiate in a very logical progression; those that ultimately control the fastest/ strongest movements develop first, with those controlling increasingly slower/weaker movements added with time [20,28].”
BackgroundMethodSpinal V2b neurons reveal a role for ipsilateral inhibition in speed control
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“534 Line generation 535 The Tg(gata3:gal4) and Tg(gata3:LoxP-dsRed-LoxP:GFP) lines were generated via the bacterial 536 artificial chromosome (BAC) transgenic technique [67], using BAC zK257H17.”
MethodSelf-citationThe Developing Utility of Zebrafish Models for Cognitive Enhancers Research
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Brainstem circuits encoding start, speed, and duration of swimming in adult zebrafish
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Spinal Interneurons: Diversity and Connectivity in Motor Control
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“The V2a INs constitute a phylogenetically conserved interneuronal population, and in zebrafish V2a INs provide excitatory locomotor drive to MNs (Kimura et al. 2006) and their genetically driven ablation significantly impairs the generation of rhythmic locomotion (Eklöf-Ljunggren et al. 2012).”
BackgroundCarbo-Tano, M., Lapoix, M., Jia, X., Thouvenin, O., Pascucci, M., Auclair, F., Quan, F. B., Albadri, S., Aguda, V., Farouj, Y., et al. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01418-0 · Cited by 58
Genetic dissection of rhythmic motor networks in mice
Grossmann, K. S., Giraudin, A., Britz, O., Zhang, J., & Goulding, M. (2010) · Progress in brain research · doi:10.1016/b978-0-444-53613-6.00002-2 · Cited by 55
“…the transcription factors Evx1/2, En1, Chx10, Gata2/3, and Sim1, respectively (Al-Mosawie et al., 2007; Croneet al., 2008; Karunaratne et al., 2002; Kimura et al., 2006; Lundfald et al., 2007; Moran-Rivard et al., 2001; Peng et al., 2007; Saueressig et al., 1999; Zhang et al., 2008; reviewed in…”
Mechanosensory neurons control the timing of spinal microcircuit selection during locomotion
Knafo, S., Fidelin, K., Prendergast, A. E., Tseng, P.-E. B., Parrin, A., Dickey, C. W., Böhm, U. L., Figueiredo, S. N., Thouvenin, O., Pascal‐Moussellard, H., et al. (2017) · eLife · doi:10.7554/elife.25260 · Cited by 60
Functional diversity of excitatory commissural interneurons in adult zebrafish
Björnfors, E. R., & El Manira, A. (2016) · eLife · doi:10.7554/elife.18579 · Cited by 52
“born spinal neurons in the larval zebrafish form the fast system, whereas those later born are involved in slow swimming (Liu and Westerfield, 1988; Kimura et al., 2006; McLean and Fetcho, 2009; Fetcho and McLean, 2010).”
InfluentialIn the swim of things: recent insights to neurogenetic disorders from zebrafish
Kabashi, E., Champagne, N., Brustein, E., & Drapeau, P. (2010) · Trends in Genetics · doi:10.1016/j.tig.2010.05.004 · Cited by 57
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Functional diversity of glycinergic commissural inhibitory neurons in larval zebrafish
Satou, C., Sugioka, T., Uemura, Y., Shimazaki, T., Zmarz, P., Kimura, Y., & Higashijima, S.-I. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.02.015 · Cited by 50
Self-citationTanimoto, M., Ota, Y., Horikawa, K., & Oda, Y. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5530-08.2009 · Cited by 48
“scribed previously (Kimura et al., 2006) with some modifications.”
InfluentialZebrafish as an appealing model for optogenetic studies
Simmich, J., Staykov, E., & Scott, E. K. (2012) · Progress in brain research · doi:10.1016/b978-0-444-59426-6.00008-2 · Cited by 47
Volume EM Reconstruction of Spinal Cord Reveals Wiring Specificity in Speed-Related Motor Circuits
Svara, F., Kornfeld, J. M. R., Denk, W. T., & Bollmann, J. H. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.05.023 · Cited by 46
Spinal sensory neurons project onto the hindbrain to stabilize posture and enhance locomotor speed
Wu, M., Tano, M. C., Mirat, O., Lejeune, F., Roussel, J., Quan, F. B., Fidelin, K., & Wyart, C. (2021) · Current Biology · doi:10.1016/j.cub.2021.05.042 · Cited by 56
Transgenic zebrafish expressing fluorescent proteins in central nervous system neurons
Higashijima, S. (2008) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2008.01023.x · Cited by 45
“Consistent with dual in situ hybridization data, the connections were found to be glutamatergic (Kimura et al. 2006).”
BackgroundMethodSelf-citationCapo‐Chichi, J., Boissel, S., Brustein, E., Pickles, S. R., Fallet‐Bianco, C., Nassif, C., Patry, L., Dobrzeniecka, S., Liao, M., Labuda, D., et al. (2015) · Journal of Medical Genetics · doi:10.1136/jmedgenet-2014-102952 · Cited by 45
Andrzejczuk, L., Banerjee, S., England, S. J., Voufo, C., Kamara, K. O., & Lewis, K. E. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00170 · Cited by 44
Generation of transgenic medaka using modified bacterial artificial chromosome
Nakamura, S., Saito, D., & Tanaka, M. (2008) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2008.01027.x · Cited by 43
“Numerous examples obtained from transgene expression experiments using various organisms, including zebrafish, demonstrate that bacterial artificial chromosome (BAC) vectors can be a more powerful approach to direct transgene expression (Kimura et al. 2006).”
BackgroundMethodInfluentialJuárez‐Morales, J. L., Schulte, C. J., Pezoa, S. A., Vallejo, G. K., Hilinski, W. C., England, S. J., de Jager, S., & Lewis, K. E. (2016) · Neural Development · doi:10.1186/s13064-016-0059-9 · Cited by 43
“have been identified as specifying excitatory spinal cord fates, Tlx1 and Tlx3 [4, 5, 8], work at least in part by”
BackgroundInfluentialGuner‐Ataman, B., & Karlstrom, R. O. (2007) · Gene Expression Patterns · doi:10.1016/j.modgep.2007.01.002 · Cited by 43
“2, and alx(Chx10) overlap in a few of the p2 progenitor cells (Kimura et al., 2006).”
BackgroundNkx6 proteins specify one zebrafish primary motoneuron subtype by regulating lateislet1expression
Hutchinson, S. A., Cheesman, S. E., Hale, L. A., Boone, J. Q., & Eisen, J. S. (2007) · Development · doi:10.1242/dev.02826 · Cited by 42
“In contrast to MiPs, CaPs initiate expression of islet2 while they still express islet1, and then downregulate expression of islet1 (Appel et al., 1995; Inoue et al., 1994; Korzh et al., 1993; Tokumoto et al., 1995).”
InfluentialMultifunctional and specialized spinal interneurons for turtle limb movements
Berkowitz, A. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.05428.x · Cited by 44
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Self-citationDevelopment, functional organization, and evolution of vertebrate axial motor circuits
D’Elia, K. P., & Dasen, J. S. (2018) · Neural Development · doi:10.1186/s13064-018-0108-7 · Cited by 42
“dorsal-ventral axis based on recruitment during swimming and birth order [62].”
BackgroundA functional scaffold of CNS neurons for the vertebrates: The developing Xenopus laevis spinal cord
Roberts, A., Li, W., & Soffe, S. R. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20889 · Cited by 44
“…neuron populations using the data currently available (Li et al., 2001), but what is really needed are the genetic tools based on expression of transcription factors and other markers like those already contributing so much to studies on mice (Kwan et al., 2009) and zebrafish (Kimura et al., 2006).”
BackgroundMethodKassen, S. C., Thummel, R., Burket, C. T., Campochiaro, L. A., Harding, M. J., & Hyde, D. R. (2008) · Europe PMC (PubMed Central) · Cited by 38
Knogler, L. D., Ryan, J., Saint-Amant, L., & Drapeau, P. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.1225-14.2014 · Cited by 37
Zebrafish Is a Powerful Tool for Precision Medicine Approaches to Neurological Disorders
Ochenkowska, K., Herold, A., & Samarut, É. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.944693 · Cited by 36
“…including CRISPR-CAS9 genome engineering (Hwang et al., 2013) and the development of CNS structures can be followed in vivo at a single-cell resolution thanks to an extensive repertoire of available transgenic lines (Park et al., 2000; Zerucha et al., 2000; Shin et al., 2003; Kimura et al., 2006).”
BackgroundInhibitory neuron migration and IPL formation in the developing zebrafish retina
Chow, R., Almeida, A. D., Randlett, O., Norden, C., & Harris, W. A. (2015) · Development · doi:10.1242/dev.122473 · Cited by 36
Molecular blueprints for spinal circuit modules controlling locomotor speed in zebrafish
Pallucchi, I., Bertuzzi, M., Madrid, D., Fontanel, P., Higashijima, S.-I., & El Manira, A. (2024) · Nature Neuroscience · doi:10.1038/s41593-023-01479-1 · Cited by 34
“The diversity of V2a INs was determined using scRNA-seq of Chx10 + neurons dissociated from 7-week-old zebrafish spinal cords of the vsx2 transgenic line referred to as Tg( chx10 :GFP) 42 .”
Self-citationDense Circuit Reconstruction to Understand Neuronal Computation: Focus on Zebrafish
Friedrich, R. W., & Wanner, A. A. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-110220-013050 · Cited by 33
Spinal cords: Symphonies of interneurons across species
Wilson, A. C., & Sweeney, L. B. (2023) · Frontiers in Neural Circuits · doi:10.3389/fncir.2023.1146449 · Cited by 38
“The physiological role of V2a neurons in the activation and speeddependent modulation of motor output was shown to map onto three spatially distinct microcircuits: one for driving slow, one for intermediate and one for fast motor neurons (Figure 2A; Kimura et al., 2006; Ampatzis et al., 2014).”
BackgroundInfluentialDefective glycinergic synaptic transmission in zebrafish motility mutants
Hirata, H. (2009) · Frontiers in Molecular Neuroscience · doi:10.3389/neuro.02.026.2009 · Cited by 35
Generation of highly enriched V2a interneurons from mouse embryonic stem cells
Iyer, N. R., Huettner, J. E., Butts, J. C., Brown, C. R., & Sakiyama‐Elbert, S. E. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.01.011 · Cited by 33
“They are an ipsilaterally projecting glutamatergic premotor population with conserved locomotor functions in zebrafish and mice (Crone et al., 2008; Dougherty and Kiehn, 2010b; Kimura et al., 2006).”
BackgroundLee, G., Sung, S., Chang, W.-N., Kao, T.-T., Tu, H.-C., Hsiao, T., Safo, M. K., & Fu, T.-F. (2012) · Disease Models & Mechanisms · doi:10.1242/dmm.009449 · Cited by 34
“Further examination was performed using alx:GFP transgenic fish, which express GFP specifically in excitatory interneurons under the control of the alx promoter (Kimura et al., 2006).”
MethodNeuronal labeling patterns in the spinal cord of adult transgenic Zebrafish
Stil, A., & Drapeau, P. (2015) · Developmental Neurobiology · doi:10.1002/dneu.22350 · Cited by 33
“, 2005), alx/chx10 (Kimura et al., 2006), evx1 (Suster et al.”
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Sternfeld, M. J., Hinckley, C. A., Moore, N. J., Pankratz, M. T., Hilde, K. L., Driscoll, S. P., Hayashi, M., Amin, N. D., Bonanomi, D., Gifford, W. D., et al. (2017) · eLife · doi:10.7554/elife.21540 · Cited by 31
“In addition to the cardinal marker used to label each cell type (Figure 1A), RNA-sequencing of FACS purified ES-cell-derived motor neurons and V2a interneurons revealed that each expressed a battery of genes consistent with their identity assignment (Al-Mosawie et al., 2007; Brown et al., 2014; Kimura et al., 2006; Ku…”
BackgroundBasal Protrusions Mediate Spatiotemporal Patterns of Spinal Neuron Differentiation
Hadjivasiliou, Z., Moore, R. E., McIntosh, R. L. L., Galea, G. L., Clarke, J. D. W., & Alexandre, P. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.05.035 · Cited by 30
“During the early stages of vertebrate neurogenesis, neurons of particular subtypes initially differentiate along the spinal cord withasparseperiodicpatternbut eventuallyproducemorecontinuous columns of similar neurons (Figure 1A;Dale et al., 1987; Roberts et al., 1987; Higashijima et al., 2004a, 2004b; Kimura et al.,…”
BackgroundSoans, K. G., Ramos, A. P., Sidhaye, J., Krishna, A., Solomatina, A., Hoffmann, K. B., Schlüßler, R., Guck, J. R., Sbalzarini, I. F., Modes, C. D., et al. (2022) · Current Biology · doi:10.1016/j.cub.2022.09.034 · Cited by 31
Suster, M. L., Kania, A., Liao, M., Asakawa, K., Charron, F., Kawakami, K., & Drapeau, P. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.10.004 · Cited by 33
“, 2004a) and a class of vsx2-expressing ipsilateral descending interneurons (Kimura et al., 2006).”
BackgroundRhythmogenesis in axial locomotor networks: an interspecies comparison
Ryczko, D., Dubuc, R., & Cabelguen, J. (2010) · Progress in brain research · doi:10.1016/b978-0-444-53613-6.00013-7 · Cited by 30
Spinal V1 neurons inhibit motor targets locally and sensory targets distally
Sengupta, M., Daliparthi, V., Roussel, Y., Bui, T. V., & Bagnall, M. W. (2021) · Current Biology · doi:10.1016/j.cub.2021.06.053 · Cited by 30
Distribution and neuronal circuit of spexin 1/2 neurons in the zebrafish CNS
Kim, E., Jeong, I., Chung, A.-Y., Kim, S., Kwon, S., Seong, J. Y., & Park, H. (2019) · Scientific Reports · doi:10.1038/s41598-019-41431-7 · Cited by 28
Dynamics and plasticity of spinal locomotor circuits
Manira, A. E. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.06.016 · Cited by 27
Mixed synapses reconcile violations of the size principle in zebrafish spinal cord
Menelaou, E., Kishore, S., & McLean, D. L. (2022) · eLife · doi:10.7554/elife.64063 · Cited by 32
“Mixed synapses formed by reticulospinal and propriospinal interneurons provide sources of excitation during locomotion in larval zebrafish (Bhatt et al., 2007; Kimura et al., 2006; McLean et al., 2008; Menelaou and McLean, 2019; Pujala and Koyama, 2019; Wang and McLean, 2014).”
BackgroundMethodShimazaki, T., Tanimoto, M., Oda, Y., & Higashijima, S. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.1964-18.2018 · Cited by 27
“Single-cell labeling of Ta1 and Ta2 with tetramethyl-rhodamine-dextran by electroporation was performed essentially as described previously (Bhatt et al., 2004; Kimura et al., 2006).”
MethodSelf-citationMiyazawa, H., Okumura, K., Hiyoshi, K., Maruyama, K., Kakinuma, H., Amo, R., Okamoto, H., Yamasu, K., & Tsuda, S. (2018) · Scientific Reports · doi:10.1038/s41598-018-23906-1 · Cited by 27
Kei, J. N. C., Currie, P. D., & Jusuf, P. R. (2017) · Neural Development · doi:10.1186/s13064-017-0089-y · Cited by 21
“Higashijima [40], Tg(atoh7:GFP) generated by Drs Zolessi and Poggi [41].”
BackgroundSpontaneous glycine‐induced calcium transients in spinal cord progenitors promote neurogenesis
Brustein, E., Côté, S., Ghislain, J. J., & Drapeau, P. (2012) · Developmental Neurobiology · doi:10.1002/dneu.22050 · Cited by 26
“The Alx transgenic line was used to identified glutamatergic ipsilateral descending interneurons (Kimura et al., 2006).”
MethodFormation of the spinal network in zebrafish determined by domain‐specific pax genes
Ikenaga, T., Urban, J. M., Gebhart, N., Hatta, K., Kawakami, K., & Ono, F. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22585 · Cited by 26
“In wild-type fish, nearly all CiD neurons arise from cells expressing the transcription factor alx (Kimura et al., 2006).”
BackgroundInfluentialLive Imaging of Zebrafish Development: Table 1.Preprint
Godinho, L. (2011) · Cold Spring Harbor Protocols · doi:10.1101/pdb.top119 · Cited by 26
Predicting modular functions and neural coding of behavior from a synaptic wiring diagram
Vishwanathan, A., Sood, A., Wu, J., Ramirez, A. D., Yang, R., Kemnitz, N., Ih, D., Turner, N., Lee, K., Tartavull, I., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01784-3 · Cited by 36
“…were found to have somata primarily within a medial glutamatergic parasagittal https://doi.org/10.1038/s41593-024-01784-3 stripe associated with the Alx transcription factor and the latter with a more lateral GABAergic parasagittal stripe associated with the Abx1b transcription factor 21,95,96 .”
InfluentialSite-Specific Integration of Exogenous Genes Using Genome Editing Technologies in Zebrafish
Kawahara, A., Hisano, Y., Ota, S., & Taimatsu, K. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17050727 · Cited by 25
“This makes this technique very convenient compared with the conventional BAC (bacterial artificial chromosome) method that requires complicated and tailored BAC constructs to individual target genes [42].”
MethodGerber, V., Yang, L., Takamiya, M., Ribes, V., Gourain, V., Peravali, R., Stegmaier, J., Mikut, R., Reischl, M., Ferg, M., et al. (2019) · Development · doi:10.1242/dev.172510 · Cited by 25
“Altogether, these results bring further support for the notion that V2s cells are different from the previously described V2a and V2b interneurons (Bernhardt et al., 1992; Kimura et al., 2006).”
BackgroundResultInfluentialYokoyama, T. D., Hotta, K., & Oka, K. (2014) · Developmental Dynamics · doi:10.1002/dvdy.24169 · Cited by 24
“Due to its special photoconvertible fluorescence properties, Kaede protein offers several advantages as an optical cell marker, such as the ability to visualize the precise morphology and migratory behavior of individual cells (Kimura et al., 2006; Sato et al., 2006; Ellett et al., 2011).”
BackgroundKawano, K., Kato, K., Sugioka, T., Kimura, Y., Tanimoto, M., & Higashijima, S. (2022) · Scientific Reports · doi:10.1038/s41598-022-08283-0 · Cited by 23
Self-citationLi, W., Merrison‐Hort, R., Zhang, H.-Y., & Borisyuk, R. M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4198-13.2014 · Cited by 26
“…of recent nonmammalian vertebrate studies suggest that circuit reconfiguration is needed to generate different motor responses (Ritter et al., 2001; Kimura et al., 2006; Berkowitz, 2007, 2008; Li et al., 2007; McLean et al., 2007, 2008; Liao and Fetcho, 2008; Frigon, 2009; Satou et al., 2009;…”
BackgroundTransgenic Zebrafish Recapitulating tbx16 Gene Early Developmental Expression
Wells, S., Nornes, S., & Lardelli, M. T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021559 · Cited by 22
“alx is expressed in Circumferential Descending (CiD) interneurons although it appears, perhaps, that not all CiD neurons express this gene [23].”
BackgroundFunctional Motifs Composed of Morphologically Homologous Neurons Repeated in the Hindbrain Segments
Neki, D., Nakayama, H., Fujii, T., Matsui, H., & Oda, Y. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4610-13.2014 · Cited by 21
Pedroni, A., & Ampatzis, K. (2019) · iScience · doi:10.1016/j.isci.2019.09.010 · Cited by 22
Regenerated interneurons integrate into locomotor circuitry following spinal cord injury
Vasudevan, D., Liu, Y.-C., Barrios, J. P., Wheeler, M. K., Douglass, A. D., & Dorsky, R. I. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113737 · Cited by 22
A specialized spinal circuit for command amplification and directionality during escape behavior
Guan, N. N., Xu, L., Zhang, T., Huang, C., Wang, Z., Dahlberg, E., Wang, H., Wang, F., Pallucchi, I., Hua, Y., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2106785118 · Cited by 21
“Among these are the excitatory V2a interneurons identified by their expression of the transcription factor Chx10 and distributed in the brainstem and spinal cord (34).”
BackgroundMethodInfluentialTransformation of an early-established motor circuit during maturation in zebrafish
Pallucchi, I., Bertuzzi, M., Michel, J. J. C., Miller, A. C., & Manira, A. E. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110654 · Cited by 21
“In larvae, episodic swimming movements are mainly driven by fast circuits activating fast muscles (Kimura et al., 2006; McLean et al., 2007, 2008; McLean and Fetcho, 2009; Menelaou and McLean, 2012; Myers, 1985; Pujala and Koyama, 2019; Svara et al., 2018).”
BackgroundRegulation of spinal interneuron differentiation by the paracrine action of glycine
Côté, S., & Drapeau, P. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20972 · Cited by 21
“to identify glutamatergic ipsilateral descending interneurons (Kimura et al., 2006) and the Evx line was used to visualize commissural interneurons (Suster et al.”
BackgroundMethodRosch, R. E., Burrows, D. R. W., Jones, L., Peters, C. H., Ruben, P. C., & Samarut, É. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00556 · Cited by 24
Developmental switch in the function of inhibitory commissural V0d interneurons in zebrafish
Picton, L. D., Björnfors, E. R., Fontanel, P., Pallucchi, I., Bertuzzi, M., & Manira, A. E. (2022) · Current Biology · doi:10.1016/j.cub.2022.06.059 · Cited by 19
Huang, C., Wang, Z., Cheng, J., Zhu, Z., Guan, N. N., & Song, J. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111535 · Cited by 20
Position- and quantity-dependent responses in zebrafish turning behavior
Umeda, K., Ishizuka, T., Yawo, H., & Shoji, W. (2016) · Scientific Reports · doi:10.1038/srep27888 · Cited by 19
Simple, fast, tissue‐specific bacterial artificial chromosome transgenesis in Xenopus
Fish, M. B., Nakayama, T., & Grainger, R. M. (2011) · genesis · doi:10.1002/dvg.20819 · Cited by 19
“BAC DNA has been successfully integrated in mouse and zebrafish using the Tol2 transposase-mediated method (Suster et al., 2009), and in zebrafish using the I-SceI meganuclease-mediated method (Kimura et al., 2006).”
MethodLhx3 and Lhx4 suppress Kolmer–Agduhr interneuron characteristics within zebrafish axial motoneurons
Seredick, S. D., Hutchinson, S. A., Ryswyk, L. V., Talbot, J. C., & Eisen, J. S. (2014) · Development · doi:10.1242/dev.105718 · Cited by 23
“PMNs and SMNs are Islet+ Mnx+ Lhx3+; VeLDs are Islet− Mnx+ Lhx3+; CiDs are Islet− Mnx− Lhx3+; KA′s are Islet− Mnx− Lhx3− (Batista et al., 2008; Hutchinson and Eisen, 2006; Kimura et al., 2006; Seredick et al., 2012).”
BackgroundMethodInfluentialClonally related, Notch-differentiated spinal neurons integrate into distinct circuits
Bello‐Rojas, S., & Bagnall, M. W. (2022) · eLife · doi:10.7554/elife.83680 · Cited by 20
An mnr2b/hlxb9lb enhancer trap line that labels spinal and abducens motor neurons in zebrafish
Asakawa, K., Higashijima, S., & Kawakami, K. (2011) · Developmental Dynamics · doi:10.1002/dvdy.22781 · Cited by 15
“The transgenic line Tg(vglut2a: loxPDsRed-GFP) was constructed using a bacterial artificial chromosome (DKEY-145P24) by a previously described method (Kimura et al., 2006).”
BackgroundMethodSelf-citationAlternative forms of axial startle behaviors in fishes
Liu, Y.-C., & Hale, M. E. (2013) · Zoology · doi:10.1016/j.zool.2013.10.008 · Cited by 17
Lmx1b is required for the glutamatergic fates of a subset of spinal cord neurons
Hilinski, W. C., Bostrom, J. R., England, S. J., Juárez‐Morales, J. L., de Jager, S., Armant, O., Legradi, J., Strähle, U., Link, B. A., & Lewis, K. E. (2016) · Neural Development · doi:10.1186/s13064-016-0070-1 · Cited by 17
“In contrast, double in situ hybridization with lmx1bb and slc32a1, which labels all spinal cord inhibitory neurons [33, 68], revealed that only 10 % of lmx1bb neurons are inhibitory (Fig.”
BackgroundMethodResultInfluentialOkamoto, H., Sato, T., & Aizawa, H. (2008) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2008.01003.x · Cited by 17
“This procedure stochastically induced the expression of Gal4VP16 under the control of the brn3a-hsp70 promoter after the DsRed sequence was excised by Cre recombinase, and resulted in the induction of GFP expression (Dong & Stuart 2004; Kimura et al. 2006).”
Notch-mediated re-specification of neuronal identity during central nervous system development
Engerer, P., Petridou, E., Williams, P. R., Suzuki, S. C., Yoshimatsu, T., Portugues, R., Misgeld, T., & Godinho, L. (2021) · Current Biology · doi:10.1016/j.cub.2021.08.049 · Cited by 16
Chx10+V2a interneurons in spinal motor regulation and spinal cord injury
Li, Z., Wang, Y., Li, W., Deng, L., Zhai, F., & Wang, X. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.355746 · Cited by 16
Tanimoto, Y., Kakinuma, H., Aoki, R., Shiraki, T., Higashijima, S.-I., & Okamoto, H. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113916 · Cited by 16
Self-citationRNA profiling of FAC‐sorted neurons from the developing zebrafish spinal cord
Cerda, G. A., Hargrave, M. R., & Lewis, K. E. (2008) · Developmental Dynamics · doi:10.1002/dvdy.21818 · Cited by 16
Reinoß, P., Ciglieri, E., Minère, M., Bremser, S., Klein, A., Löhr, H., Fuller, P. M., Büschges, A., Kloppenburg, P., Fenselau, H., et al. (2020) · Current Biology · doi:10.1016/j.cub.2020.08.103 · Cited by 16
“TgBAC(vsx2:EGFP)nns1Tg [64], Tg(vsx2:Gal4FF)nns18Tg [33] and Tg(14xUAS:GCaMP6s)mpn101Tg [65] lines were obtained from RIKEN Center for Brain Science (Japan) and National Institute for Genetics (Japan).”
MethodTranscriptional autoregulation of zebrafish tbx6 is required for somite segmentation
Ban, H., Yokota, D., Otosaka, S., Kikuchi, M., Kinoshita, H., Fujino, Y., Yabe, T., Ovara, H., Izuka, A., Akama, K., et al. (2019) · Development · doi:10.1242/dev.177063 · Cited by 14
“An EGFP reporter and a kanamycin-resistant gene were amplified by PCR with the following primers (5′-TTCATTTAATATTCGATAAACAGAAACGTGAAGAAAGAGCAGACCGAGACATGGTGAGCAAGGGCGAGGA-3′ and 5′-CTGTAATAGCAGTCGCTCAATCTCTGAGGTCCCAGAGCCAAACCAGGGTACAGTTGGTGATTTTGAACTT-3′) as described previously (Kawamura et al., 2016; Kimura et al.,…”
MethodDefects of the Glycinergic Synapse in Zebrafish
Ogino, K., & Hirata, H. (2016) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2016.00050 · Cited by 14
“…of hindbrain, spinal neuron Hirata et al., 2005 Frontiers in Molecular Neuroscience | www.frontiersin.org 5 June 2016 | Volume 9 | Article 50 Saint-Amant and Drapeau, 2001; Sidi et al., 2003; Higashijima et al., 2004; Kimura et al., 2006; Fetcho, 2007; McLean et al., 2007; Tanimoto et al., 2009).”
BackgroundPredicting modular functions and neural coding of behavior from a synaptic wiring diagramPreprint
Vishwanathan, A., Ramirez, A. D., Wu, J., Sood, A., Yang, R., Kemnitz, N., Ih, D., Turner, N. L., Lee, K., Tartavull, I., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.28.359620 · Cited by 14
“S9C, ZBB-alx-gal4 ) where most neurons are glutamatergic (Kimura et al., 2006).”
BackgroundSingle-cell RNAseq analysis of spinal locomotor circuitry in larval zebrafish
Kelly, J. J., Wen, H., & Brehm, P. (2023) · eLife · doi:10.7554/elife.89338 · Cited by 14
“One molecular feature differentiating the two types is the higher expression level of both the vsx2 and shox2 marker genes in type I compared to type II v2a ( Kimura et al., 2006 ; Menelaou et al., 2014 ; Hayashi et al., 2018 ; Mene-laou and McLean, 2019 ).”
BackgroundResultInfluentialConnexin 35b expression in the spinal cord of Danio rerio embryos and larvae
Carlisle, T. C., & Ribera, A. B. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23449 · Cited by 12
“In the Tg(vsx2:Kaede)nns2 line, CiDs express Kaede (Kimura et al., 2006).”
BackgroundMethodResultInfluentialCell-Specific Actions of a Human LHX3 Gene Enhancer During Pituitary and Spinal Cord Development
Park, S., Mullen, R. D., & Rhodes, S. J. (2013) · Molecular Endocrinology · doi:10.1210/me.2013-1161 · Cited by 12
Spinal Basis of Direction Control during Locomotion in Larval Zebrafish
Jay, M., MacIver, M. A., & McLean, D. L. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0703-22.2023 · Cited by 11
Li, W., & Soffe, S. R. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00047 · Cited by 12
“Transcription factor expression has also been studied in developing zebrafish where CHX10-expressing glutamatergic V2a interneurons (CiD) extend from the spinal cord into the hindbrain (Kimura et al., 2006, 2013).”
BackgroundInfluentialubtor Mutation Causes Motor Hyperactivity by Activating mTOR Signaling in Zebrafish
Wang, T., Zhou, M.-S., Zhang, Q., Zhang, C.-Z., & Peng, G. (2021) · Neuroscience Bulletin · doi:10.1007/s12264-021-00755-z · Cited by 8
The Temporal Mechanisms Guiding Interneuron Differentiation in the Spinal Cord
Deska‐Gauthier, D., & Zhang, Y. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22158025 · Cited by 11
“Early maturation of swimming behaviours is underscored by sequential waves of neurogenesis (C), early-born and fast swimming recruitment; (D), late-born and slow swimming recruitment; motor neurons (MNs), [49]; V0, [48,49,55]; V2a INs, [52]; V1 INs, [53]; dI6 INs, [62].”
BackgroundChapouton, P., & Godinho, L. (2010) · Methods in cell biology · doi:10.1016/b978-0-12-384892-5.00004-9 · Cited by 11
Switching gears in the spinal cord
Manira, A. E., & Grillner, S. E. (2008) · Nature Neuroscience · doi:10.1038/nn1208-1367 · Cited by 11
Metadata
- Authors
- Kimura, Y., Okamura, Y., & Higashijima, S.-I.
- Affiliations
- National Institutes of Natural Sciences (JP)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-05-24
- Volume
- 26
- Issue
- 21
- Pages
- 5684-5697
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6675258
- OpenAlex
- W2030150624
- Cited by
- 302
- References
- 54
- Citations by year
- 2026: 6 · 2025: 10 · 2024: 9 · 2023: 17 · 2022: 16 · 2021: 18 · 2020: 15 · 2019: 18 · 2018: 11 · 2017: 12 · 2016: 17 · 2015: 13 · 2014: 19 · 2013: 13 · 2012: 13
- FWCI
- 6.77
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- spinal interneurons, vesicular glutamate transporter 2, spinal locomotor circuits, premotor interneurons, swimming behavior, escape behavior, zebrafish
- MeSH terms
- Animals, Efferent Pathways, Eye Proteins, Feedback, Interneurons, Locomotion, Nerve Net, Spinal Cord, Tissue Distribution, Zebrafish, Homeodomain Proteins, Excitatory Postsynaptic Potentials, Zebrafish Proteins
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