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.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In R7/R8, the former VPNI cells 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 factor.
“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]
Cites
A monomeric red fluorescent protein
Campbell, R. E., Tour, O., Palmer, A. E., Steinbach, P. A., Baird, G. S., Zacharias, D. A., & Tsien, R. Y. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.082243699 · Cited by 2,346 · see citing works
The action of calcium on the electrical properties of squid axons
FRANKENHAEUSER, B., & Hodgkin, A. L. (1957) · The Journal of Physiology · doi:10.1113/jphysiol.1957.sp005808 · Cited by 1,839 · see citing works
Deletion of a DNA Polymerase β Gene Segment in T Cells Using Cell Type-Specific Gene Targeting
Gu, H., Marth, J. D., Orban, P. C., Mossmann, H., & Rajewsky, K. (1994) · Science · doi:10.1126/science.8016642 · Cited by 1,397 · see citing works
Lee, E.-C., Yu, D., de Velasco, J. M., Tessarollo, L., Swing, D. A., Court, D. L., Jenkins, N. A., & Copeland, N. G. (2001) · Genomics · doi:10.1006/geno.2000.6451 · Cited by 1,179 · see citing works
Briscoe, J., Pierani, A., Jessell, T. M., & Ericson, J. (2000) · Cell · doi:10.1016/s0092-8674(00)80853-3 · Cited by 1,111 · see citing works
Pax6 Controls Progenitor Cell Identity and Neuronal Fate in Response to Graded Shh Signaling
Ericson, J., Rashbass, P., Schedl, A., Brenner‐Morton, S., Kawakami, A., van Heyningen, V., Jessell, T. M., & Briscoe, J. (1997) · Cell · doi:10.1016/s0092-8674(00)80323-2 · Cited by 1,044 · see citing works
An optical marker based on the UV-induced green-to-red photoconversion of a fluorescent protein
Ando, R., Hama, H., Yamamoto‐Hino, M., Mizuno, H., & Miyawaki, A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.202320599 · Cited by 1,028 · see citing works
Interneuronal relay in spinal pathways from proprioceptors
Jankowska, E. (1992) · Progress in Neurobiology · doi:10.1016/0301-0082(92)90024-9 · Cited by 931 · see citing works
The motor infrastructure: from ion channels to neuronal networks
Grillner, S. E. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1137 · Cited by 839 · see citing works
I-SceI meganuclease mediates highly efficient transgenesis in fish
Thermes, V., Grabher, C., Ristoratore, F., Bourrat, F., Choulika, A., Wittbrodt, J., & Joly, J. (2002) · Mechanisms of Development · doi:10.1016/s0925-4773(02)00218-6 · Cited by 522 · see citing works
LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons.
Sharma, K., Sheng, H. Z., Lettieri, K., Li, H., Karavanov, A., Potter, S., Westphal, H., & Pfaff, S. (1998) · Cell · doi:10.1016/s0092-8674(00)81704-3 · Cited by 461 · see citing works
Higashijima, S., Okamoto, H., Ueno, N., Hotta, Y., & Eguchi, G. (1997) · Developmental Biology · doi:10.1006/dbio.1997.8779 · Cited by 417 · see citing works
Self-citationV1 spinal neurons regulate the speed of vertebrate locomotor outputs
Gosgnach, S., Lanuza, G. M., Butt, S. J. B., Saueressig, H., Zhang, Y., Velasquez, T., Riethmacher, D., Callaway, E. M., Kiehn, O., & Goulding, M. (2006) · Nature · doi:10.1038/nature04545 · Cited by 405 · see citing works
Role of EphA4 and EphrinB3 in Local Neuronal Circuits That Control Walking
Kullander, K., Butt, S., Lebret, J. M., Lundfald, L., Restrepo, C. E., Rydström, A., Klein, R., & Kiehn, O. (2003) · Science · doi:10.1126/science.1079641 · Cited by 365 · see citing works
Thaler, J., Harrison, K., Sharma, K., Lettieri, K., Kehrl, J., & Pfaff, S. L. (1999) · Neuron · doi:10.1016/s0896-6273(01)80027-1 · Cited by 354 · see citing works
Identification of spinal neurons in the embryonic and larval zebrafish
Bernhardt, R. R., Chitnis, A. B., Lindamer, L., & Kuwada, J. Y. (1990) · Journal of Comparative Neurology · doi:10.1002/cne.903020315 · Cited by 329 · see citing works
Dale, N., & Roberts, A. (1985) · The Journal of Physiology · doi:10.1113/jphysiol.1985.sp015694 · Cited by 326 · see citing works
Cloning of a functional vesicular GABA and glycine transporter by screening of genome databases
Sagné, C., Mestikawy, S. E., Isambert, M., Hamon, M., Henry, J., Bruno Giros, A., & Gasnier, B. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)01279-9 · Cited by 311 · see citing works
Newly identified ‘glutamate interneurons’ and their role in locomotion in the lamprey spinal cord
Buchanan, J. T., & Grillner, S. (1987) · Science · doi:10.1126/science.3563512 · Cited by 304 · see citing works
Correlation of the startle reflex and Mauthner cell auditory responses in unrestrained goldfish
Zottoli, S. J. (1977) · Journal of Experimental Biology · doi:10.1242/jeb.66.1.243 · Cited by 285 · see citing works
Sander, M., Paydar, S., Ericson, J., Briscoe, J., Berber, E., German, M., Jessell, T. M., & Rubenstein, J. L. R. (2000) · Genes & Development · doi:10.1101/gad.820400 · Cited by 270 · see citing works
Postnatal phenotype and localization of spinal cord V1 derived interneurons
Alvarez, F. J., Jonas, P. C., Sapir, T., Hartley, R., Berrocal, M. C., Geiman, E. J., Todd, A. J., & Goulding, M. (2005) · Journal of Comparative Neurology · doi:10.1002/cne.20711 · Cited by 243 · see citing works
Higashijima, S., Mandel, G., & Fetcho, J. R. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20278 · Cited by 234 · see citing works
Self-citationKiehn, O., & Butt, S. J. B. (2003) · Progress in Neurobiology · doi:10.1016/s0301-0082(03)00091-1 · Cited by 219 · see citing works
Electrotonic Junctions between Teleost Spinal Neurons: Electrophysiology and Ultrastructure
Bennett, M. V. L., Aljure, E. F., Nakajima, Y., & Pappas, G. D. (1963) · Science · doi:10.1126/science.141.3577.262 · Cited by 213 · see citing works
Central Circuits Controlling Locomotion in Young Frog Tadpoles
Roberts, A., Soffe, S. R., Wolf, E., YOSHIDA, M., & Zhao, F.-Y. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb09036.x · Cited by 205 · see citing works
A confocal study of spinal interneurons in living larval zebrafish
Hale, M. E., Ritter, D. A., & Fetcho, J. R. (2001) · Journal of Comparative Neurology · doi:10.1002/cne.1266 · Cited by 203 · see citing works
Pax6 and Engrailed 1 Regulate Two Distinct Aspects of Renshaw Cell Development
Sapir, T., Geiman, E. J., Wang, Z., Velasquez, T., Mitsui, S., Yoshihara, Y., Frank, E., Álvarez, F. J., & Goulding, M. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3187-03.2004 · Cited by 189 · see citing works
Saueressig, H., Burrill, J. D., & Goulding, M. (1999) · Development · doi:10.1242/dev.126.19.4201 · Cited by 188 · see citing works
Engrailed-1 Expression Marks a Primitive Class of Inhibitory Spinal Interneuron
Higashijima, S., Masino, M. A., Mandel, G., & Fetcho, J. R. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5342-03.2004 · Cited by 187 · see citing works
Self-citationCyclic AMP-Induced Repair of Zebrafish Spinal Circuits
Bhatt, D. H., Otto, S. J., Depoister, B., & Fetcho, J. R. (2004) · Science · doi:10.1126/science.1098439 · Cited by 184 · see citing works
Visualization of active neural circuitry in the spinal cord of intact zebrafish
Fetcho, J. R., & O'Malley, D. M. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.73.1.399 · Cited by 171 · see citing works
Saint-Amant, L., & Drapeau, P. (2001) · Neuron · doi:10.1016/s0896-6273(01)00416-0 · 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
Ritter, D. A., Bhatt, D. H., & Fetcho, J. R. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-22-08956.2001 · Cited by 159 · see citing works
Spinal Network of the Mauthner Cell (Part 1 of 2)
Fetcho, J. R. (2008) · Brain Behavior and Evolution · doi:10.1159/000114367 · Cited by 150 · see citing works
Neurotransmitter properties of spinal interneurons in embryonic and larval zebrafish
Higashijima, S., Schaefer, M., & Fetcho, J. R. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20279 · Cited by 141 · see citing works
Self-citationIn vivo recording from identifiable neurons of the locomotor network in the developing zebrafish
Drapeau, P., Ali, D. W., Buss, R. R., & Saint‐Amant, L. (1999) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(99)00008-4 · Cited by 141 · see citing works
Contributions of identifiable neurons and neuron classes to lamprey vertebrate neurobiology
Buchanan, J. T. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00050-2 · Cited by 138 · see citing works
Cracking the Transcriptional Code for Cell Specification in the Neural Tube
Marquardt, T., & Pfaff, S. L. (2001) · Cell · doi:10.1016/s0092-8674(01)00499-8 · Cited by 138 · see citing works
The formation of sensorimotor circuits.
Goulding, M. D., Lanuza, G. M., Sapir, T., & Narayan, S. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00371-9 · Cited by 125 · see citing works
Soffe, S. R. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-10-04456.1993 · Cited by 125 · see citing works
Development of spinal neurons and tracts in the zebrafish embryo
Kuwada, J. Y., Bernhardt, R. R., & Nguyen, N. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.903020316 · Cited by 125 · see citing works
Development of circuits that generate simple rhythmic behaviors in vertebrates
Goulding, M., & Pfaff, S. L. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.01.017 · Cited by 124 · see citing works
Primitive Roles for Inhibitory Interneurons in Developing Frog Spinal Cord
Li, W., Higashijima, S., Parry, D. M., Roberts, A., & Soffe, S. R. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1633-04.2004 · Cited by 117 · see citing works
Self-citationGATA Proteins Identify a Novel Ventral Interneuron Subclass in the Developing Chick Spinal Cord
Karunaratne, A., Hargrave, M. R., Poh, A. M., & Yamada, T. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0754 · Cited by 107 · see citing works
Neave, B., Rodaway, A., Wilson, S. W., Patient, R. K., & Holder, N. (1995) · Mechanisms of Development · doi:10.1016/0925-4773(95)00351-7 · Cited by 93 · see citing works
Wenner, P., O'Donovan, M. J., & Matise, M. P. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.5.2651 · Cited by 70 · see citing works
EphA4 defines a class of excitatory locomotor-related interneurons
Butt, S. J. B., Lundfald, L., & Kiehn, O. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503317102 · Cited by 68 · see citing works
Barabino, S. M. L., Spada, F., Cotelli, F., & Boncinelli, E. (1997) · Mechanisms of Development · doi:10.1016/s0925-4773(97)00036-1 · Cited by 68 · see citing works
Localization and electrical characteristics of a giant synapse in the spinal cord of the lamprey.
Ringham, G. L. (1975) · The Journal of Physiology · doi:10.1113/jphysiol.1975.sp011100 · Cited by 58 · see citing works
A novel family of ancient vertebrate odorant receptors
Berghard, A., & Dryer, L. (1998) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(19981115)37:3 · Cited by 50 · see citing works
Fetcho, J. R. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.6.1574 · Cited by 49 · see citing works
Flagged first, then by citations
1 of the 54 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Decoding the organization of spinal circuits that control locomotion
Kiehn, O. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.9 · Cited by 742 · see citing works
Circuits controlling vertebrate locomotion: moving in a new direction
Goulding, M. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2608 · Cited by 777 · see citing works
Current principles of motor control, with special reference to vertebrate locomotion
Grillner, S., & El Manira, A. (2020) · Physiological Reviews · doi:10.1152/physrev.00015.2019 · Cited by 560 · see citing works
Highly efficient CRISPR/Cas9-mediated knock-in in zebrafish by homology-independent DNA repair
Auer, T. O., Duroure, K., De Cian, A., Concordet, J.-P., & Del Bene, F. (2014) · Genome Research · doi:10.1101/gr.161638.113 · Cited by 631 · see citing works
Asakawa, K., Suster, M. L., Mizusawa, K., Nagayoshi, S., Kotani, T., Urasaki, A., Kishimoto, Y., Hibi, M., & Kawakami, K. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704963105 · Cited by 554 · see citing works
A 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 · see citing works
Self-citationMeasured motion: searching for simplicity in spinal locomotor networks
Grillner, S. E., & Jessell, T. M. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.10.011 · Cited by 380 · see citing works
Crone, S. A., Quinlan, K. A., Zagoraiou, L., Droho, S., Restrepo, C. E., Lundfald, L., Endo, T., Setlak, J., Jessell, T. M., Kiehn, O., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.08.009 · Cited by 358 · see citing works
V3 Spinal Neurons Establish a Robust and Balanced Locomotor Rhythm during Walking
Zhang, Y., Narayan, S., Geiman, E. J., Lanuza, G. M., Velasquez, T., Shanks, B., Akay, T., Dyck, J. R. B., Pearson, K. G., Gosgnach, S., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.027 · Cited by 350 · see citing works
Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena
Takehana, Y., Matsuda, M., Myosho, T., Suster, M. L., Kawakami, K., Shin‐I, T., Kohara, Y., Kuroki, Y., Toyoda, A., Fujiyama, A., et al. (2014) · Nature Communications · doi:10.1038/ncomms5157 · Cited by 342 · see citing works
Kimura, Y., Hisano, Y., Kawahara, A., & Higashijima, S. (2014) · Scientific Reports · doi:10.1038/srep06545 · Cited by 322 · see citing works
Self-citationAnatomy of zebrafish cerebellum and screen for mutations affecting its development
Bae, Y.-K., Kani, S., Shimizu, T., Tanabe, K., Nojima, H., Kimura, Y., Higashijima, S.-I., & Hibi, M. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.04.013 · Cited by 293 · see citing works
Self-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 · see citing works
In 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 · see citing works
Control 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 · see citing works
Development and functional organization of spinal locomotor circuits
Kiehn, O. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.09.004 · Cited by 250 · see citing works
Retinoic acid and Cyp26b1 are critical regulators of osteogenesis in the axial skeleton
Spoorendonk, K. M., Peterson-Maduro, J., Renn, J., Trowe, T., Kranenbarg, S., Winkler, C., & Schulte‐Merker, S. (2008) · Development · doi:10.1242/dev.024034 · Cited by 247 · see citing works
Transgenic 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 · see citing works
Self-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 · see citing works
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 · see citing works
Self-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 · see citing works
Self-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 · see citing works
Ampatzis, K., Song, J., Ausborn, J., & El Manira, A. (2014) · Neuron · doi:10.1016/j.neuron.2014.07.018 · Cited by 186 · see citing works
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 · see citing works
Hindbrain 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 · see citing works
Self-citationKimura, Y., Satou, C., & Higashijima, S. (2008) · Development · doi:10.1242/dev.024802 · Cited by 182 · see citing works
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 · see citing works
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 · see citing works
Rapid BAC selection fortol2-mediated transgenesis in zebrafish
Bussmann, J., & Schulte‐Merker, S. (2011) · Development · doi:10.1242/dev.068080 · Cited by 172 · see citing works
McLean, D. L., & Fetcho, J. R. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3277-09.2009 · Cited by 157 · see citing works
Satou, 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 · see citing works
Self-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 · see citing works
Proneural gene-linked neurogenesis in zebrafish cerebellum
Kani, S., Bae, Y., Shimizu, T., Tanabe, K., Satou, C., Parsons, M. J., Scott, E. K., Higashijima, S., & Hibi, M. (2010) · Developmental Biology · doi:10.1016/j.ydbio.2010.03.024 · Cited by 151 · see citing works
Self-citationSatou, C., Kimura, Y., & Higashijima, S. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.5500-11.2012 · Cited by 150 · see citing works
Self-citationVaz, R., Hofmeister, W., & Lindstrand, A. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20061296 · Cited by 143 · see citing works
Firing and Cellular Properties of V2a Interneurons in the Rodent Spinal Cord
Dougherty, K. J., & Kiehn, O. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4821-09.2010 · Cited by 138 · see citing works
Motor neurons control locomotor circuit function retrogradely via gap junctions
Song, J., Ampatzis, K., Björnfors, E. R., & Manira, A. E. (2016) · Nature · doi:10.1038/nature16497 · Cited by 146 · see citing works
Two populations of endochondral osteoblasts with differential sensitivity to Hedgehog signalling
Hammond, C. L., & Schulte‐Merker, S. (2009) · Development · doi:10.1242/dev.042150 · Cited by 142 · see citing works
Zebrafish and motor control over the last decade
Fetcho, J. R., Higashijima, S., & McLean, D. L. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.06.018 · Cited by 135 · see citing works
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 · see citing works
Heterogeneity of V2‐derived interneurons in the adult mouse spinal cord
Al‐Mosawie, A., Wilson, J. M. M., & Brownstone, R. M. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05907.x · Cited by 136 · see citing works
Fetcho, J. R., & McLean, D. L. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2010.05539.x · Cited by 132 · see citing works
Menelaou, E., & McLean, D. L. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.1809-12.2012 · Cited by 116 · see citing works
Concentric zones, cell migration and neuronal circuits in the Drosophila visual center
Hasegawa, E., Kitada, Y., Kaido, M., Takayama, R., Awasaki, T., Tabata, T., & Sato, M. (2011) · Development · doi:10.1242/dev.058370 · Cited by 128 · see citing works
Visually guided gradation of prey capture movements in larval zebrafish
Patterson, B. W., Abraham, A. O., MacIver, M. A., & McLean, D. L. (2013) · Journal of Experimental Biology · doi:10.1242/jeb.087742 · Cited by 122 · see citing works
Barrio, 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 · see citing works
Vsx2 in the zebrafish retina: restricted lineages through derepression
Vitorino, M., Jusuf, P. R., Maurus, D., Kimura, Y., Higashijima, S., & Harris, W. A. (2009) · Neural Development · doi:10.1186/1749-8104-4-14 · Cited by 121 · see citing works
Self-citationModular Organization of Axial Microcircuits in Zebrafish
Bagnall, M. W., & McLean, D. L. (2014) · Science · doi:10.1126/science.1245629 · Cited by 120 · see citing works
Büschges, A., Scholz, H., & Manira, A. E. (2011) · Current Biology · doi:10.1016/j.cub.2011.05.029 · Cited by 117 · see citing works
Zebrafish models for the functional genomics of neurogenetic disorders
Kabashi, E., Brustein, E., Champagne, N., & Drapeau, P. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2010.09.011 · Cited by 117 · see citing works
Sato, T., Hamaoka, T., Aizawa, H., Hosoya, T., & Okamoto, H. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0883-07.2007 · Cited by 109 · see citing works
Sidhaye, J., & Norden, C. (2017) · eLife · doi:10.7554/elife.22689 · Cited by 105 · see citing works
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 · see citing works
Self-citationBerkowitz, A. (2010) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2010.00036 · Cited by 102 · see citing works
Control of orienting movements and locomotion by projection-defined subsets of brainstem V2a neurons
Usseglio, G., Gatier, E., Heuzé, A., Hérent, C., & Bouvier, J. (2020) · Current Biology · doi:10.1016/j.cub.2020.09.014 · Cited by 87 · see citing works
Grading movement strength by changes in firing intensity versus recruitment of spinal interneurons
Bhatt, D. H., McLean, D. L., Hale, M. E., & Fetcho, J. R. (2007) · Neuron · doi:10.1016/j.neuron.2006.11.011 · Cited by 103 · see citing works
Delineating the Diversity of Spinal Interneurons in Locomotor Circuits
Gosgnach, S., Bikoff, J. B., Dougherty, K. J., Manira, A. E., Lanuza, G. M., & Zhang, Y. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1829-17.2017 · Cited by 100 · 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
Transgenic 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 96 · see citing works
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 · see citing works
Zhong, G., Sharma, K., & Harris‐Warrick, R. M. (2011) · Nature Communications · doi:10.1038/ncomms1276 · Cited by 95 · see citing works
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 98 · see citing works
Pujala, A., & Koyama, M. (2019) · eLife · doi:10.7554/elife.42135 · Cited by 80 · see citing works
Benito‐Gonzalez, A., & Álvarez, F. J. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3630-12.2012 · Cited by 91 · see citing works
Nakamura, 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 · see citing works
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 89 · see citing works
Song, 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 · see citing works
Batista, M. F., Jacobstein, J., & Lewis, K. E. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.07.015 · Cited by 82 · see citing works
Wiggin, 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 · see citing works
Cerebellospinal 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 83 · see citing works
Li, W., Sautois, B., Roberts, A., & Soffe, S. R. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3694-07.2007 · Cited by 82 · see citing works
Soffe, S. R., Roberts, A., & Li, W. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.175208 · Cited by 80 · see citing works
Peeling 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 · see citing works
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 · see citing works
Using 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 80 · see citing works
Ausborn, J., Mahmood, R. Z., & Manira, A. E. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1216256110 · Cited by 78 · see citing works
Song, M., Sun, Y., Bryson, A., Gill, G. N., Evans, S. Μ., & Pfaff, S. L. (2009) · Development · doi:10.1242/dev.037986 · Cited by 76 · see citing works
Hierarchical 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 · see citing works
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 · see citing works
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 75 · see citing works
Neuronal subtype specification in the spinal cord of a protovertebrate
Stolfi, A., & Levine, M. (2011) · Development · doi:10.1242/dev.061507 · Cited by 74 · see citing works
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 · see citing works
Menelaou, E., VanDunk, C., & McLean, D. L. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23465 · Cited by 73 · see citing works
Selective 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 74 · see citing works
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 · see citing works
Berkowitz, A. (2008) · Journal of Neurophysiology · doi:10.1152/jn.90235.2008 · Cited by 71 · see citing works
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 67 · see citing works
From 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 69 · see citing works
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 68 · see citing works
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 · see citing works
Technologies 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 · see citing works
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 · see citing works
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 63 · see citing works
Kishore, S., Bagnall, M. W., & McLean, D. L. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0514-14.2014 · Cited by 64 · see citing works
Hale, M. E., Katz, H. R., Peek, M. Y., & Fremont, R. (2016) · Journal of Neurogenetics · doi:10.1080/01677063.2016.1182526 · Cited by 65 · see citing works
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 · see citing works
Song, J., Dahlberg, E., & El Manira, A. (2018) · Nature Communications · doi:10.1038/s41467-018-05827-9 · Cited by 64 · see citing works
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 · see citing works
Self-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 · see citing works
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 60 · see citing works
- 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review