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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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“2008), Tg(vsx2:eGFP) (Kimura et al. 2006), Tg(pou4f3:mGFP) (Xiao et al.”
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“The activities of these neurons during swimming have been studied by electrophysiological analysis of transgenic fish expressing GFP under the control of the En-1 and the alx promoter (26, 27).”
BackgroundA topographic map of recruitment in spinal cord
McLean, D. L., Fan, J., Higashijima, S.-I., Hale, M. E., & Fetcho, J. R. (2007) · Nature · doi:10.1038/nature05588 · Cited by 384
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Self-citationAnatomy of zebrafish cerebellum and screen for mutations affecting its development
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“The Tg(vglut2a:EGFP) line was constructed using the BAC DKEY-145P24 by a previously described method (Kimura et al., 2006).”
MethodSelf-citationContinuous shifts in the active set of spinal interneurons during changes in locomotor speed
McLean, D. L., Masino, M. A., Koh, I. Y. Y., Lindquist, W. B., & Fetcho, J. R. (2008) · Nature Neuroscience · doi:10.1038/nn.2225 · Cited by 270
“Prior work has revealed the distribution of the CiD interneurons and their direct connections with motoneuron”
BackgroundIn mice lacking V2a interneurons, gait depends on speed of locomotion
Crone, S. A., Zhong, G., Harris-Warrick, R., & Sharma, K. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1206-09.2009 · Cited by 263
“The speed dependence of V2a neuron function is consistent with the role of the CiD interneurons, which express the Chx10 homolog alx in the zebrafish; a subset of these interneurons is selectively activated only at high swim speeds (Kimura et al., 2006).”
BackgroundInfluentialControl of visually guided behavior by distinct populations of spinal projection neurons
Orger, M. B., Kampff, A. R., Severi, K. E., Bollmann, J. H., & Engert, F. (2008) · Nature Neuroscience · doi:10.1038/nn2048 · Cited by 274
“Interestingly, the spinal interneurons involved in slow swimming behavior also appear a few hours later than those involved in escape”
BackgroundDevelopment and functional organization of spinal locomotor circuits
Kiehn, O. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.09.004 · Cited by 260
Retinoic acid and Cyp26b1 are critical regulators of osteogenesis in the axial skeleton
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“YFP was recombined directly after the ATG site of the gene of interest on a BAC clone, containing the genomic information of the gene of interest (Kimura et al., 2006).”
MethodTransgenic tools to characterize neuronal properties of discrete populations of zebrafish neurons
Satou, C., Kimura, Y., Hirata, H., Suster, M. L., Kawakami, K., & Higashijima, S. (2013) · Development · doi:10.1242/dev.099531 · Cited by 224
“All the transgenic fish (Table 1) were generated using the BAC (bacterial artificial chromosome) homologous recombination technique with either the I-SceI-mediated method (Kimura et al., 2006) or the Tol2-mediated method (Suster et al., 2009).”
MethodSelf-citationSocial conflict resolution regulated by two dorsal habenular subregions in zebrafish
Chou, M.-Y., Amo, R., Kinoshita, M., Cherng, B.-W., Shimazaki, H., Agetsuma, M., Shiraki, T., Aoki, T., Takahoko, M., Yamazaki, M., et al. (2016) · Science · doi:10.1126/science.aac9508 · Cited by 193
Self-citationA structural and functional ground plan for neurons in the hindbrain of zebrafish
Kinkhabwala, A., Riley, M., Koyama, M., Monen, J., Satou, C., Kimura, Y., Higashijima, S.-I., & Fetcho, J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012185108 · Cited by 203
“Huc:Kaede and alx:Kaede transgenic embryos (38, 40) were illuminated with UV light from a mercury bulb source for 10– 40 s within their chorion.”
MethodSelf-citationMapping a sensory-motor network onto a structural and functional ground plan in the hindbrain
Koyama, M., Kinkhabwala, A., Satou, C., Higashijima, S.-I., & Fetcho, J. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012189108 · Cited by 190
“The transgenic lines Tg(vglut2a: loxPDsRed-GFP) and Tg(dbx1b:Cre) were constructed using bacterial artificial chromosomes (DKEY-145P24 and zK17G17, respectively) (31).”
MethodSelf-citationHayashi, M., Hinckley, C. A., Driscoll, S. P., Moore, N. J., Levine, A. J., Hilde, K. L., Sharma, K., & Pfaff, S. L. (2018) · Neuron · doi:10.1016/j.neuron.2018.01.023 · Cited by 188
“These interneurons can be identified by their expression of the transcription factor Chx10/Vsx2 (Ericson et al., 1997; Kimura et al., 2006).”
InfluentialAmpatzis, K., Song, J., Ausborn, J., & El Manira, A. (2014) · Neuron · doi:10.1016/j.neuron.2014.07.018 · Cited by 186
Molecular and cellular development of spinal cord locomotor circuitry
Lu, D. C.-T., Niu, T., & Alaynick, W. A. (2015) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2015.00025 · Cited by 193
“In zebrafish, alx, a zebrafish homolog of Chx10, is expressed in an ipsilateral descending excitatory interneuron population named CiD (circumferential descending) neurons that monosynaptically contact motor neurons (Kimura et al., 2006; McLean et al., 2008).”
BackgroundHindbrain V2a neurons in the excitation of spinal locomotor circuits during zebrafish swimming
Kimura, Y., Satou, C., Fujioka, S., Shoji, W., Umeda, K., Ishizuka, T., Yawo, H., & Higashijima, S.-I. (2013) · Current Biology · doi:10.1016/j.cub.2013.03.066 · Cited by 186
Self-citationKimura, Y., Satou, C., & Higashijima, S. (2008) · Development · doi:10.1242/dev.024802 · Cited by 182
“A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA.”
Self-citationNotch and MAML Signaling Drives Scl-Dependent Interneuron Diversity in the Spinal Cord
Peng, C., Yajima, H., Burns, C. E., Zon, L. I., Sisodia, S. S., Pfaff, S. L., & Sharma, K. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.019 · Cited by 178
Lundfald, L., Restrepo, C. E., Butt, S. J. B., Peng, C., Droho, S., Endo, T., Zeilhofer, H. U., Sharma, K., & Kiehn, O. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05906.x · Cited by 172
“The distribution is also similar to the distribution of the Alx population in zebrafish embryos (Kimura et al., 2006) although, due to the difference in size and shape of the spinal cord in these two species, a direct comparison is more difficult.”
BackgroundInfluentialRapid BAC selection fortol2-mediated transgenesis in zebrafish
Bussmann, J., & Schulte‐Merker, S. (2011) · Development · doi:10.1242/dev.068080 · Cited by 172
“In previous experiments (Spoorendonk et al., 2008; Hogan et al., 2009), we have used I-SceI-mediated transgenesis (Grabher et al., 2004; Kimura et al., 2006) to perform BAC integration.”
MethodMcLean, D. L., & Fetcho, J. R. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3277-09.2009 · Cited by 162
“In vivo imaging of CiD differentiation using the photoconvertible protein Kaede In the prior study examining the development and activity of CiDs mentioned above, the cells were divided into two groups, a dorsally located strong-movement class and a ventrally located weakmovement class (Kimura et al., 2006).”
BackgroundMethodInfluentialSatou, C., Kimura, Y., Kohashi, T., Horikawa, K., Takeda, H., Oda, Y., & Higashijima, S. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0801-09.2009 · Cited by 155
“This has worked well in zebrafish for functional analyses of several classes of neurons (Kimura et al., 2006).”
BackgroundMethodInfluentialSelf-citationBrainstem neurons that command mammalian locomotor asymmetries
Cregg, J. M., Leiras, R., Montalant, A., Wanken, P., Wickersham, I. R., & Kiehn, O. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0633-7 · Cited by 154
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“Tg(atoh1a:EGFP), Tg (atoh1a:dTomato), and Tg(vglut2a:DsRed2) were constructed using the BAC CHORI211-247L22 and DEKY-145P2, by a previously described method (Kimura et al., 2006).”
BackgroundMethodSelf-citationSatou, C., Kimura, Y., & Higashijima, S. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5500-11.2012 · Cited by 150
“Microinjection of BAC DNA for the generation of transgenic fish was performed as described previously (Kimura et al., 2006).”
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“Moreover, the Chx10 homologues in zebrafish, called Alx neurons, have been shown to contact motor neurons through both chemical and electrical synapses (Kimura et al., 2006).”
BackgroundInfluentialMotor neurons control locomotor circuit function retrogradely via gap junctions
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“mCherry was recombined directly after the ATG site of the Collagen 2a1 on a bacterial artificial chromosome (BAC) clone, using similar principles to those previously (Kimura et al., 2006).”
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Self-citationInitiation of Locomotion in Adult Zebrafish
Kyriakatos, A., Mahmood, R. Z., Ausborn, J., Porres, C. P., Büschges, A., & Manira, A. E. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.1012-11.2011 · Cited by 134
“In this regard, the zebrafish at early developmental stages has emerged as an attractive system that already enabled some of the neuronal components for swimming and escape behavior (Drapeau et al., 2002; Kimura et al., 2006; McLean et al., 2007; Fetcho et al., 2008; Liao and Fetcho, 2008; McLean et al., 2008; Satou e…”
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“Journal Compilation ª Federation of European Neuroscience Societies and Blackwell Publishing Ltd European Journal of Neuroscience, 26, 3003–3015 neurons are last-order glutamatergic interneurons with ipsilateral descending axons (Kimura et al., 2006).”
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“In zebrafish, neural networks exhibit topographic patterns of functional organization due to their order of development (Kimura et al., 2006; McLean and Fetcho, 2009; Kinkhabwala et al., 2011; Koyama et al., 2011; Miri et al., 2011; Liao and Haehnel, 2012; Pujol-Martí et al., 2012; Satou et al.,…”
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BackgroundBarrio, M. G. D., Taveira‐Marques, R., Muroyama, Y., Yuk, D., Li, S., Wines-Samuelson, M., Shen, J., Smith, H. K., Xiang, M., Rowitch, D. H., et al. (2007) · Development · doi:10.1242/dev.005868 · Cited by 123
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“To investigate the in vivo role of Vsx2 in the zebrafish retina, we used Tg(vsx2:GFP) and Tg(vsx2:dsRed) transgenic zebrafish [26].”
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Origin of excitation underlying locomotion in the spinal circuit of zebrafish
Eklöf-Ljunggren, E., Haupt, S., Ausborn, J., Dehnisch, I., Uhlén, P., Higashijima, S.-I., & El Manira, A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1115377109 · Cited by 95
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BackgroundTransgenic fluorescent zebrafish lines that have revolutionized biomedical research
Choe, C. P., Choi, S., Kee, Y., Kim, J. M., Kim, S.-H., Lee, Y., Park, H., & Ro, H. (2021) · Laboratory Animal Research · doi:10.1186/s42826-021-00103-2 · Cited by 104
Ljunggren, E. E., Haupt, S., Ausborn, J., Ampatzis, K., & El Manira, A. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.4087-13.2014 · Cited by 93
“In lamprey, Xenopus tadpoles, and larval zebrafish, ipsilateral excitatory interneurons have been shown to activate motoneurons monosynaptically (Grillner, 2003; Kimura et al., 2006; Roberts et al., 2008, 2010).”
InfluentialZhong, G., Sharma, K., & Harris‐Warrick, R. M. (2011) · Nature Communications · doi:10.1038/ncomms1276 · Cited by 95
Principles Governing Locomotion in Vertebrates: Lessons From Zebrafish
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 112
“…2 September 2018 | Volume 12 | Article 73 glycinergic CiAs belong to the V1 population and express the transcription factor En1, while the CiDs correspond to the V2a population defined by the expression of the transcription factor Chx10 (Higashijima et al., 2004a; Kimura et al., 2006).”
InfluentialPujala, A., & Koyama, M. (2019) · eLife · doi:10.7554/elife.42135 · Cited by 80
Benito‐Gonzalez, A., & Álvarez, F. J. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3630-12.2012 · Cited by 93
“Early born V2a/CiDs are large, dorsally located, and active during stronger movements such as escape or fast swimming, while later born neurons are smaller, more ventrally located, and recruited during slower and weaker sustained swimming (Kimura et al., 2006; McLean and Fetcho, 2009).”
BackgroundNakamura, S., Aoki, Y., Saito, D., Kuroki, Y., Fujiyama, A., Naruse, K., & Tanaka, M. (2007) · Molecular Reproduction and Development · doi:10.1002/mrd.20764 · Cited by 89
Generation of Rab‐based transgenic lines for in vivo studies of endosome biology in zebrafish
Clark, B. S., Winter, M. R., Cohen, A. R., & Link, B. A. (2011) · Developmental Dynamics · doi:10.1002/dvdy.22758 · Cited by 90
“In order to direct tissue-specific expression of the Rab mutants to the retina and developing nervous system (Liu et al., 1994; Rowan and Cepko, 2005; Kimura et al., 2006), a portion of the promoter of the zebrafish ortholog of Chx10, vsx2, was cloned to generate a 50 entry clone to assemble the Tol2 – vsx2:Gal4vp16 c…”
BackgroundMethodInfluentialSong, J., Pallucchi, I., Ausborn, J., Ampatzis, K., Bertuzzi, M., Fontanel, P., Picton, L. D., & El Manira, A. (2020) · Neuron · doi:10.1016/j.neuron.2019.12.030 · Cited by 84
Batista, M. F., Jacobstein, J., & Lewis, K. E. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.07.015 · Cited by 82
“Until very recently, the only known functional characteristics of vertebrate V2 cells, were those described for V2a cells in zebrafish (Kimura et al., 2006).”
BackgroundResultInfluentialWiggin, T. D., Anderson, T. M., Eian, J., Peck, J. H., & Masino, M. A. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00233.2012 · Cited by 74
“…al., 2009; Koyama et al., 2011) and early touch 57 response (Downes and Granato, 2006; Pietri et al., 2009) have been characterized, the 58 CPG circuits that control swimming in larval zebrafish are less well characterized 59 (Kimura et al., 2006; McLean et al., 2008; Eklöf-Ljunggren et al., 2012).”
BackgroundCerebellospinal Neurons Regulate Motor Performance and Motor Learning
Sathyamurthy, A., Barik, A., Dobrott, C. I., Matson, K. J. E., Stoica, S., Pursley, R. H., Chesler, A. T., & Levine, A. J. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107595 · Cited by 87
“In contrast, excitatory Chx10-expressing V2a neurons, which have also been implicated in regulating the speed of locomotor rhythm (Ampatzis et al., 2014; Crone et al., 2009; Kimura et al., 2006), were only infrequently targeted by CeS cer-contra neurons (Figure S5I).”
Li, W., Sautois, B., Roberts, A., & Soffe, S. R. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3694-07.2007 · Cited by 82
“In addition to shared elements, selective recruitment of neurons between patterns also occurs in larval zebrafish and turtles (Ritter et al., 2001; Kimura et al., 2006; Berkowitz, 2007).”
BackgroundSoffe, S. R., Roberts, A., & Li, W. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.175208 · Cited by 80
“…like the tadpole and the zebrafish, the available evidence, from the expression patterns of transcription factors (Cepeda-Nieto et al. 2005; Kimura et al. 2006, 2008; A. Roberts, unpublished observations) and inhibitory neurotransmitters (Roberts et al. 1987, 1988), indicates that columns…”
BackgroundPeeling back the layers of locomotor control in the spinal cord
McLean, D. L., & Dougherty, K. J. (2015) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2015.03.001 · Cited by 78
LMO4 Controls the Balance between Excitatory and Inhibitory Spinal V2 Interneurons
Joshi, K., Lee, S., Lee, J. W., Lee, S., & Lee, S. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.011 · Cited by 80
“Considering the dramatic downregulation of Gata3 in LMO4 / ;SCL embryos (Figure 2A) and the presence of multiple types of GABAergic interneurons in the ventral spinal cord in addition to V2b-INs (Lanuza et al., 2004; Alvarez et al., 2005; Kimura et al., 2006), it is likely that the majority of remaining GABAergic inte…”
InfluentialUsing imaging and genetics in zebrafish to study developing spinal circuits in vivo
McLean, D. L., & Fetcho, J. R. (2008) · Developmental Neurobiology · doi:10.1002/dneu.20617 · Cited by 81
“-PA Author M anuscript N IH -PA Author M anuscript N IH -PA Author M anuscript (Gleason et al., 2003; Higashijima et al., 2003; Hale et al., 2004; Li et al., 2005; Kimura et al., 2006; Smear et al., 2007).”
BackgroundInfluentialAusborn, J., Mahmood, R. Z., & Manira, A. E. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1216256110 · Cited by 78
“We used a transgenic zebrafish line in which GFP expression is driven by the promoter of the transcription factor Chx10, which characterizes V2a interneurons (Fig.”
BackgroundMethodInfluentialSong, M., Sun, Y., Bryson, A., Gill, G. N., Evans, S. Μ., & Pfaff, S. L. (2009) · Development · doi:10.1242/dev.037986 · Cited by 76
“V2a INs arise from p2 progenitors and extend axons ipsilaterally over multiple segments to control proper locomotion (Kimura et al., 2006; Lundfald et al., 2007).”
BackgroundHierarchical control of locomotion by distinct types of spinal V2a interneurons in zebrafish
Menelaou, E., & McLean, D. L. (2019) · Nature Communications · doi:10.1038/s41467-019-12240-3 · Cited by 73
Functional organization of V2a‐related locomotor circuits in the rodent spinal cord
Dougherty, K. J., & Kiehn, O. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05502.x · Cited by 75
Zebrafish pigment cells develop directly from persistent highly multipotent progenitors
Subkhankulova, T., Sosa, K. C., Урошлев, Л. А., Nikaido, M., Shriever, N. P., Kasianov, A. S., Yang, X., Rodrigues, F. S. L. M., Carney, T. J., Bavister, G., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-36876-4 · Cited by 105
Neuronal subtype specification in the spinal cord of a protovertebrate
Stolfi, A., & Levine, M. (2011) · Development · doi:10.1242/dev.061507 · Cited by 74
“By contrast, Vsx orthologs are more broadly associated with interneurons arising in different nervous tissues and expressing different neurotransmitters (Kimura et al., 2006; Svendsen and McGhee, 1995).”
Electron Microscopic Reconstruction of Functionally Identified Cells in a Neural Integrator
Vishwanathan, A., Daie, K., Ramirez, A. D., Lichtman, J. W., Aksay, E. R. F., & Seung, H. S. (2017) · Current Biology · doi:10.1016/j.cub.2017.06.028 · Cited by 74
Menelaou, E., VanDunk, C., & McLean, D. L. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23465 · Cited by 73
“Chx10 is a transcription factor that selectively labels V2a neurons and was formerly known as Alx (Kimura et al., 2006, 2013).”
BackgroundSelective Responses to Tonic Descending Commands by Temporal Summation in a Spinal Motor Pool
Wang, W., & McLean, D. L. (2014) · Neuron · doi:10.1016/j.neuron.2014.06.021 · Cited by 77
“16), which is more consistent with a chemical connection (Kimura et al., 2006; McLean et al., 2008).”
Excitatory components of the mammalian locomotor CPG
Kiehn, O., Quinlan, K. A., Restrepo, C. E., Lundfald, L., Borgius, L., Talpalar, A. E., & Endo, T. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.07.002 · Cited by 73
Berkowitz, A. (2008) · Journal of Neurophysiology · doi:10.1152/jn.90235.2008 · Cited by 71
Sternberg, J. R., Severi, K. E., Fidelin, K., Gómez, J., Ihara, H., Alcheikh, Y., Hubbard, J. M., Kawakami, K., Suster, M. L., & Wyart, C. (2016) · Current Biology · doi:10.1016/j.cub.2016.06.037 · Cited by 69
“Coiling persisted when embryos expressed BoTxBLC-GFP in chx10 interneurons (V2as) or in GABAergic pkd2l1 cerebrospinal-fluidcontacting neurons (CSF-cNs) (Figures 1E and 1F) [14, 26].”
BackgroundFrom circuits to behaviour: motor networks in vertebrates
García‐Campmany, L., Stam, F. J., & Goulding, M. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.01.002 · Cited by 74
Voltage imaging identifies spinal circuits that modulate locomotor adaptation in zebrafish
Böhm, U. L., Kimura, Y., Kawashima, T., Ahrens, M. B., Higashijima, S., Engert, F., & Cohen, A. E. (2022) · Neuron · doi:10.1016/j.neuron.2022.01.001 · Cited by 70
Self-citationOrigin and Determination of Inhibitory Cell Lineages in the Vertebrate Retina
Jusuf, P. R., Almeida, A. D., Randlett, O., Joubin, K., Poggi, L., & Harris, W. A. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4713-10.2011 · Cited by 68
“Zebrafish transgenic lines Tg (vsx1:GFP), Tg(vsx2:GFP) and Tg(vsx2:dsRed) were kind gifts from Shin-ichi Higashijima’s laboratory (Kimura et al., 2006, 2008) (National Institutes of Natural Sciences, Okazaki Institute for Integrative Bioscience, Okazaki, Japan).”
MethodTechnologies for micromanipulating, imaging, and phenotyping small invertebrates and vertebrates.
Yanik, M., Rohde, C., & Pardo-Martín, C. (2011) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-071910-124703 · Cited by 74
Development of vestibular behaviors in zebrafish
Bagnall, M. W., & Schoppik, D. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.06.004 · Cited by 66
“Additionally, the elements of spinal circuitry that produce fast swimming are largely in place by 2 days old, whereas the motor and premotor components of slower muscle control, which are thought to underlie most postural movements [28], develop around 2–4 days old [29,30].”
Spectrum of Fates: a new approach to the study of the developing zebrafish retina
Almeida, A. D., Boije, H., Chow, R., He, J., Tham, J., Suzuki, S. C., & Harris, W. A. (2014) · Development · doi:10.1242/dev.104760 · Cited by 65
Kishore, S., Bagnall, M. W., & McLean, D. L. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0514-14.2014 · Cited by 64
Hale, M. E., Katz, H. R., Peek, M. Y., & Fremont, R. (2016) · Journal of Neurogenetics · doi:10.1080/01677063.2016.1182526 · Cited by 65
A spinal organ of proprioception for integrated motor action feedback
Picton, L. D., Bertuzzi, M., Pallucchi, I., Fontanel, P., Dahlberg, E., Björnfors, E. R., Iacoviello, F., Shearing, P. R., & El Manira, A. (2021) · Neuron · doi:10.1016/j.neuron.2021.01.018 · Cited by 59
“, 2012, 2020); V2a interneurons were labeled in Tg(Chx10:GFP) zebrafish (Ampatzis et al., 2014; Ausborn et al., 2012; Kimura et al., 2006; Song et al., 2018, 2020); and motor neurons were back-labeled by injecting dextran dye into the muscles (Ampatzis et al.”
Song, J., Dahlberg, E., & El Manira, A. (2018) · Nature Communications · doi:10.1038/s41467-018-05827-9 · Cited by 64
Wada, H., Ghysen, A., Satou, C., Higashijima, S., Kawakami, K., Hamaguchi, S., & Sakaizumi, M. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.02.017 · Cited by 63
“The atoh1a:dtomato line was constructed from zC247L22 BAC and dTomato (Shaner et al., 2004; Kimura et al., 2006).”
MethodSelf-citationLocomotor Pattern in the Adult Zebrafish Spinal Cord In Vitro
Gabriel, J. P., Mahmood, R. Z., Walter, A. M., Kyriakatos, A., Hauptmann, G., Calabrese, R. L., & Manira, A. E. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00785.2007 · Cited by 63
The SoLute Carrier (SLC) Family Series in Teleost Fish
Verri, T., Terova, G., Romano, A., Barca, A., Pisani, P., Storelli, C., & Saroglia, M. G. (2012) · Wiley eBooks · doi:10.1002/9781118350041.ch10 · Cited by 61
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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