Optogenetic Localization and Genetic Perturbation of Saccade-Generating Neurons in Zebrafish
Open accessAbstract
The optokinetic response (OKR) to a visual stimulus moving at constant velocity consists of a series of two alternating components, a slow phase, during which the eyes follow the stimulus, and a quick phase, which resets the eyes to begin a new response cycle. The quick phases of the OKR resemble the saccades observed during free viewing. It is unclear to what extent the premotor circuitry underlying these two types of jerky, conjugate eye movements is conserved among vertebrates. Zebrafish (Danio rerio) larvae, broadly expressing halorhodopsin (NpHR) or channelrhodopsin-2 (ChR2) in most neurons, were used to map the location of neurons involved in this behavior. By blocking activity in localized groups of NpHR-expressing neurons with an optic fiber positioned above the head of the fish and by systematically varying the site of photostimulation, we discovered that activity in a small hindbrain area in rhombomere 5 was necessary for saccades to occur. Unilateral block of activity at this site affected behavior in a direction-specific manner. Inhibition of the right side suppressed rightward saccades of both eyes, while leaving leftward saccades unaffected, and vice versa. Photostimulation of this area in ChR2-transgenic fish was sufficient to trigger saccades that were precisely locked to the light pulses. These extra saccades could be induced both during free viewing and during the OKR, and were distinct in their kinetics from eye movements elicited by stimulating the abducens motor neurons. Zebrafish double indemnity(didy) mutants were identified in a chemical mutagenesis screen based on a defect in sustaining saccades during OKR. Positional cloning, molecular analysis, and electrophysiology revealed that the didy mutation disrupts the voltage-gated sodium channel Scn1lab (Nav1.lb). ChR2 photostimulation of the putative hindbrain saccade generator was able to fully reconstitute saccades in the didy mutant. Our studies demonstrate that an optogenetic approach is useful for targeted loss-of-function and gain-of-function manipulations of neural circuitry underlying eye movements in zebrafish and that the saccade-generating circuit in this species shares many of its properties with that in mammals.
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?
The imaged volume includes neurons involved in eye movements.
“The imaged volume includes neurons involved in eye movements16,21,22,28.”
From Predicting modular functions and neural coding of behavior from a synaptic wiring diagram (2024) · cites this paper as [28]
Cites
Brainard, D. H. (1997) · Spatial Vision · doi:10.1163/156856897x00357 · Cited by 19,308 · see citing works
The VideoToolbox software for visual psychophysics: transforming numbers into movies
Pelli, D. G. (1997) · Spatial Vision · doi:10.1163/156856897x00366 · Cited by 11,110 · see citing works
Ogiwara, I., Miyamoto, H., Morita, N., Atapour, N., Mazaki, E., Inoue, I., Takeuchi, T., Itohara, S., Yanagawa, Y., Obata, K., et al. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.5270-06.2007 · Cited by 879 · see citing works
Genes controlling and mediating locomotion behavior of the zebrafish embryo and larva
Granato, M., van Eeden, F. J. M., Schach, U., Trowe, T., Brand, M., Furutani-Seiki, M., Haffter, P., Hammerschmidt, M., Heisenberg, C., Jiang, Y., et al. (1996) · Development · doi:10.1242/dev.123.1.399 · Cited by 634 · see citing works
The Development of Vision in the Zebrafish (Danio rerio)
Easter, S. S., & Nicola, G. N. (1996) · Developmental Biology · doi:10.1006/dbio.1996.0335 · Cited by 536 · see citing works
The brainstem burst generator for saccadic eye movements
Scudder, C. A., Kaneko, C. R. S., & Fuchs, A. F. (2002) · Experimental Brain Research · doi:10.1007/s00221-001-0912-9 · Cited by 487 · see citing works
A behavioral screen for isolating zebrafish mutants with visual system defects.
Brockerhoff, S. E., Hurley, J. B., Janssen‐Bienhold, U., Neuhauss, S. C. F., Driever, W., & Dowling, J. E. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.23.10545 · Cited by 485 · see citing works
Genetic disorders of vision revealed by a behavioral screen of 400 essential loci in zebrafish
Neuhauss, S. C. F., Biehlmaier, O., Seeliger, M. W., Das, T., Kohler, K., Harris, W. A., & Baier, H. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-19-08603.1999 · Cited by 414 · see citing works
Self-citationOptogenetic dissection of a behavioural module in the vertebrate spinal cord
Wyart, C., Bene, F. D., Warp, E., Scott, E. K., Trauner, D., Baier, H., & Isacoff, E. Y. (2009) · Nature · doi:10.1038/nature08323 · Cited by 409 · see citing works
Self-citationStrassman, A. M., Highstein, S. M., & McCREA, R. A. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902490303 · Cited by 397 · see citing works
Targeting neural circuitry in zebrafish using GAL4 enhancer trapping
Scott, E. K., Mason, L., Arrenberg, A. B., Ziv, L., Gosse, N. J., Xiao, T., Chi, N. C., Asakawa, K., Kawakami, K., & Baier, H. (2007) · Nature Methods · doi:10.1038/nmeth1033 · Cited by 394 · see citing works
Self-citationNeuronal activity in prepositus nucleus correlated with eye movement in the alert cat
López‐Barneo, J., Darlot, C., Berthoz, A., & Baker, R. (1982) · Journal of Neurophysiology · doi:10.1152/jn.1982.47.2.329 · Cited by 357 · see citing works
Zebrafish Genetic Map with 2000 Microsatellite Markers
Shimoda, N., Knapik, E. W., Ziniti, J. P., Sim, C. U., Yamada, E., Kaplan, S., Jackson, D. G., de Sauvage, F. J., Jacob, H. J., & Fishman, M. C. (1999) · Genomics · doi:10.1006/geno.1999.5824 · Cited by 350 · see citing works
Forward genetic analysis of visual behavior in zebrafish
Muto, A., Orger, M. B., Wehman, A. M., Smear, M. C., Kay, J. N., Page-McCaw, P. S., Gahtan, E., Xiao, T., Nevin, L. M., Gosse, N. J., et al. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0010066 · Cited by 321 · see citing works
Self-citationSignals in vestibular nucleus mediating vertical eye movements in the monkey
Tomlinson, R. D., & Robinson, D. A. (1984) · Journal of Neurophysiology · doi:10.1152/jn.1984.51.6.1121 · Cited by 308 · see citing works
T HE N EUROBIOLOGY OF V ISUAL -S ACCADIC D ECISION M AKING
Glimcher, P. W. (2003) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.010302.081134 · Cited by 291 · see citing works
Slow inactivation of the sodium conductance in squid giant axons. Pronase resistance.
Rudy, B. (1978) · The Journal of Physiology · doi:10.1113/jphysiol.1978.sp012485 · Cited by 267 · see citing works
Mechanisms of sodium channel inactivation
Goldin, A. L. (2003) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(03)00065-5 · Cited by 247 · see citing works
Optical control of zebrafish behavior with halorhodopsin
Arrenberg, A. B., Bene, F. D., & Baier, H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0906252106 · Cited by 244 · see citing works
Self-citationJung, H.-Y., Mickus, T. J., & Spruston, N. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-17-06639.1997 · Cited by 243 · see citing works
Kearney, J. A., Plummer, N. W., Smith, M. R., Kapur, J., Cummins, T., Waxman, S. G., Goldin, A. L., & Meisler, M. H. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00479-6 · Cited by 242 · see citing works
Yoshida, K., McCREA, R. A., Berthoz, A., & Vidal, P. P. (1982) · Journal of Neurophysiology · doi:10.1152/jn.1982.48.3.761 · Cited by 236 · see citing works
In vivo intracellular recording and perturbation of persistent activity in a neural integrator
Aksay, E., Gamkrelidze, G., Seung, H. S., Baker, R., & Tank, D. W. (2001) · Nature Neuroscience · doi:10.1038/84023 · Cited by 201 · see citing works
Strassman, A. M., Highstein, S. M., & McCREA, R. A. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902490304 · Cited by 176 · see citing works
Carr, D. B., Day, M., Cantrell, A. R., Held, J. E., Scheuer, T., Catterall, W. A., & Surmeier, D. J. (2003) · Neuron · doi:10.1016/s0896-6273(03)00531-2 · Cited by 169 · see citing works
Beck, J. C., Gilland, E., Tank, D. W., & Baker, R. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00311.2004 · Cited by 167 · see citing works
Toib, A., Lyakhov, V., & Marom, S. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-05-01893.1998 · Cited by 165 · see citing works
The cellular architecture of the larval zebrafish tectum, as revealed by Gal4 enhancer trap lines
Scott, E. K. (2009) · Frontiers in Neural Circuits · doi:10.3389/neuro.04.013.2009 · Cited by 161 · see citing works
Functional dissection of circuitry in a neural integrator
Aksay, E., Olasagasti, I., Mensh, B. D., Baker, R., Goldman, M. S., & Tank, D. W. (2007) · Nature Neuroscience · doi:10.1038/nn1877 · Cited by 134 · see citing works
Aksay, E., Baker, R., Seung, H. S., & Tank, D. W. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.2.1035 · Cited by 119 · see citing works
Smear, M. C., Tao, H. W., Staub, W., Orger, M. B., Gosse, N. J., Liu, Y., Takahashi, K., Poo, M., & Baier, H. (2007) · Neuron · doi:10.1016/j.neuron.2006.12.013 · Cited by 101 · see citing works
Self-citationEye position and eye velocity integrators reside in separate brainstem nuclei.
Pastor, Á. M., de la Cruz, R. R., & Baker, R. G. V. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.2.807 · Cited by 100 · see citing works
Embryonic and larval expression of zebrafish voltage‐gated sodium channel α‐subunit genes
Novak, A. E., Taylor, A. D., Pineda, R., Lasda, E. L., Wright, M. A., & Ribera, A. B. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20811 · Cited by 100 · see citing works
Comparative Neurobiology of the Optokinetic Reflex
Masseck, O. A., & Hoffmann, K. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.03854.x · Cited by 92 · see citing works
How do mutant Nav1.1 sodium channels cause epilepsy?
Ragsdale, D. S. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.01.003 · Cited by 90 · see citing works
Chapter 25 Expression of Ion Channels by Injection of mRNA into Xenopus Oocytes
Goldin, A. L. (1991) · Methods in cell biology · doi:10.1016/s0091-679x(08)60293-9 · Cited by 85 · see citing works
Olig2+ Precursors Produce Abducens Motor Neurons and Oligodendrocytes in the Zebrafish Hindbrain
Zannino, D., & Appel, B. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3755-08.2009 · Cited by 77 · see citing works
Ilg, U. J., & Hoffmann, K. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01170.x · Cited by 64 · see citing works
Catterall, W. A. (2001) · Nature · doi:10.1038/35059188 · Cited by 60 · see citing works
Modification of slow inactivation of single sodium channels by phenytoin in neuroblastoma cells.
Quandt, F. N. (1988) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)09773-1 · Cited by 57 · see citing works
Plasticity and tuning by visual feedback of the stability of a neural integrator
Major, G., Baker, R., Aksay, E. R. F., Mensh, B. D., Seung, H. S., & Tank, D. W. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401970101 · Cited by 56 · see citing works
Normal and Adapted Visuooculomotor Reflexes in Goldfish
Marsh, E. D., & Baker, R. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.3.1099 · Cited by 48 · see citing works
Straka, H., Beck, J. C., Pastor, Á. M., & Baker, R. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00334.2006 · Cited by 42 · see citing works
Beck, J. C., Rothnie, P., Straka, H., Wearne, S. L., & Baker, R. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00335.2006 · Cited by 32 · see citing works
Responses of monkey nucleus of the optic tract neurons during pursuit and fixation
Ilg, U. J., & Hoffmann, K. ‐. (1991) · Neuroscience Research · doi:10.1016/0168-0102(91)90103-6 · Cited by 30 · see citing works
A brain stem generator for saccadic eye movements
Fuchs, A. F., & Kaneko, C. R. S. (1981) · Trends in Neurosciences · doi:10.1016/0166-2236(81)90089-8 · Cited by 28 · see citing works
Inhibitory input to pause neurons from pontine burst neuron area in the cat
Kamogawa, H., Ohki, Y., Shimazu, H., Suzuki, I., & Yamashita, M. (1996) · Neuroscience Letters · doi:10.1016/0304-3940(95)12285-0 · Cited by 27 · see citing works
Slow Sodium Channel Inactivation in CA1 Pyramidal Cells
Mickus, T. J., Jung, H.-Y., & Spruston, N. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb11280.x · Cited by 18 · see citing works
Glycinergic inputs cause the pause of pontine omnipause neurons during saccades
Kanda, T., Iwamoto, Y., Yoshida, K., & Shimazu, H. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.11.024 · Cited by 17 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The development and application of optogenetics
Fenno, L., Yizhar, O., & Deisseroth, K. (2011) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113817 · Cited by 1,822 · see citing works
Baraban, S. C., Dinday, M. T., & Hortopan, G. A. (2013) · Nature Communications · doi:10.1038/ncomms3410 · Cited by 432 · see citing works
Remote Control of Neuronal Signaling
Rogan, S. C., & Roth, B. L. (2011) · Pharmacological Reviews · doi:10.1124/pr.110.003020 · Cited by 339 · see citing works
Prey capture behavior evoked by simple visual stimuli in larval zebrafish
Bianco, I. H., Kampff, A. R., & Engert, F. (2011) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2011.00101 · Cited by 332 · see citing works
Clemizole and modulators of serotonin signalling suppress seizures in Dravet syndrome
Griffin, A., Hamling, K. R., Knupp, K. G., Hong, S., Lee, L. P., & Baraban, S. C. (2016) · Brain · doi:10.1093/brain/aww342 · Cited by 228 · see citing works
Descending Control of Swim Posture by a Midbrain Nucleus in Zebrafish
Thiele, T. R., Donovan, J. C., & Baier, H. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.018 · Cited by 191 · see citing works
Self-citationKubo, F., Hablitzel, B., Dal Maschio, M., Driever, W., Baier, H., & Arrenberg, A. B. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.043 · Cited by 182 · see citing works
Self-citationdal Maschio, M., Donovan, J. C., Helmbrecht, T. O., & Baier, H. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.034 · Cited by 169 · see citing works
Self-citationZebrafish Models of Neurodevelopmental Disorders: Past, Present, and Future
Sakai, C., Ijaz, S., & Hoffman, E. J. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00294 · Cited by 164 · see citing works
Optogenetic Control of Cells and Circuits
Miesenböck, G. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100109-104051 · Cited by 158 · see citing works
Balestrini, S., & Sisodiya, S. M. (2017) · Neuroscience Letters · doi:10.1016/j.neulet.2017.01.014 · Cited by 158 · see citing works
Large-Scale Phenotype-Based Antiepileptic Drug Screening in a Zebrafish Model of Dravet Syndrome
Dinday, M. T., & Baraban, S. C. (2015) · eNeuro · doi:10.1523/eneuro.0068-15.2015 · Cited by 150 · 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
Glia-neuron interactions underlie state transitions to generalized seizures
Verdugo, C. D., Myren‐Svelstad, S., Aydin, E., Hoeymissen, E. V., Deneubourg, C., Vanderhaeghe, S., Vancraeynest, J., Pelgrims, R., Coşacak, M. İ., Muto, A., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11739-z · Cited by 141 · see citing works
Pharmacological Analysis of the Anti-epileptic Mechanisms of Fenfluramine in scn1a Mutant Zebrafish
Sourbron, J., Smolders, I. J., de Witte, P. A. M., & Lagae, L. G. (2017) · Frontiers in Pharmacology · doi:10.3389/fphar.2017.00191 · Cited by 139 · see citing works
Spatial gradients and multidimensional dynamics in a neural integrator circuit
Miri, A., Daie, K., Arrenberg, A. B., Baier, H., Aksay, E., & Tank, D. W. (2011) · Nature Neuroscience · doi:10.1038/nn.2888 · Cited by 138 · see citing works
Self-citationFocusing on optic tectum circuitry through the lens of genetics
Nevin, L. M., Robles, E., Baier, H., & Scott, E. K. (2010) · BMC Biology · doi:10.1186/1741-7007-8-126 · Cited by 135 · see citing works
Self-citationThe tangential nucleus controls a gravito-inertial vestibulo-ocular reflex
Bianco, I. H., Ma, L.-H., Schoppik, D., Robson, D. N., Orger, M. B., Beck, J. C., Li, J. M., Schier, A. F., Engert, F., & Baker, R. (2012) · Current Biology · doi:10.1016/j.cub.2012.05.026 · Cited by 134 · see citing works
Sensorimotor computation underlying phototaxis in zebrafish
Wolf, S., Dubreuil, A. M., Bertoni, T., Böhm, U. L., Bormuth, V., Candelier, R., Karpenko, S., Hildebrand, D. G. C., Bianco, I. H., Monasson, R., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00310-3 · Cited by 134 · see citing works
Parker, M. O., Brock, A. J., Walton, R. T., & Brennan, C. H. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00063 · Cited by 130 · see citing works
Zhu, P., Fajardo, O., Shum, J. W. H., Zhang, Y., & Friedrich, R. W. (2012) · Nature Protocols · doi:10.1038/nprot.2012.072 · Cited by 128 · see citing works
Left Habenula Mediates Light-Preference Behavior in Zebrafish via an Asymmetrical Visual Pathway
Zhang, B.-B., Yao, Y.-Y., Zhang, H.-F., Kawakami, K., & Du, J.-L. (2017) · Neuron · doi:10.1016/j.neuron.2017.01.011 · Cited by 115 · see citing works
Optogenetic investigation of neural circuits in vivo
Carter, M. E., & de Lecea, L. (2011) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2010.12.005 · Cited by 115 · see citing works
Characterization of genetically targeted neuron types in the zebrafish optic tectum
Robles, E., Smith, S. J., & Baier, H. (2011) · Frontiers in Neural Circuits · doi:10.3389/fncir.2011.00001 · Cited by 113 · see citing works
Self-citationTopography of a Visuomotor Transformation
Helmbrecht, T. O., dal Maschio, M., Donovan, J. C., Koutsouli, S., & Baier, H. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.021 · Cited by 113 · see citing works
Self-citationZebrafish: An integrative system for neurogenomics and neurosciences
Rinkwitz, S., Mourrain, P., & Becker, T. S. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.11.003 · Cited by 112 · see citing works
Zhang, Y., Kecskés, A., Copmans, D., Langlois, M., Crawford, A. D., Ceulemans, B., Lagae, L. G., de Witte, P. A. M., & Esguerra, C. V. (2015) · PLoS ONE · doi:10.1371/journal.pone.0125898 · Cited by 112 · see citing works
Optogenetics in a transparent animal: circuit function in the larval zebrafish
Portugues, R., Severi, K. E., Wyart, C., & Ahrens, M. B. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.11.001 · Cited by 110 · see citing works
State-Dependent Modulation of Locomotion by GABAergic Spinal Sensory Neurons
Fidelin, K., Djenoune, L., Stokes, C. C. A., Prendergast, A. E., Gómez, J., Baradel, A., Bene, F. D., & Wyart, C. (2015) · Current Biology · doi:10.1016/j.cub.2015.09.070 · Cited by 108 · see citing works
Serotonergic Modulation as Effective Treatment for Dravet Syndrome in a Zebrafish Mutant Model
Sourbron, J., Schneider, H., Kecskés, A., Liu, Y., Buening, E., Lagae, L. G., Smolders, I. J., & de Witte, P. A. M. (2016) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.5b00342 · Cited by 108 · see citing works
Seizing the moment: Zebrafish epilepsy models
Gaweł, K., Langlois, M., Martins, T., van der Ent, W., Tiraboschi, E., Jacmin, M., Crawford, A. D., & Esguerra, C. V. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.06.010 · Cited by 107 · see citing works
Preclinical Animal Models for Dravet Syndrome: Seizure Phenotypes, Comorbidities and Drug Screening
Griffin, A., Hamling, K. R., Hong, S., Anvar, M., Lee, L. P., & Baraban, S. C. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00573 · Cited by 103 · see citing works
Functional regionalization of the teleost cerebellum analyzed in vivo
Matsui, H., Namikawa, K., Babaryka, A., & Köster, R. W. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1403105111 · Cited by 98 · see citing works
Grone, B. P., Marchese, M., Hamling, K. R., Kumar, M. G., Krasniak, C. S., Sicca, F., Santorelli, F. M., Patel, M., & Baraban, S. C. (2016) · PLoS ONE · doi:10.1371/journal.pone.0151148 · Cited by 97 · 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
Optogenetic Control of Fly Optomotor Responses
Haikala, V., Joesch, M., Borst, A., & Mauss, A. S. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0340-13.2013 · Cited by 93 · see citing works
Optogenetics: A new enlightenment age for zebrafish neurobiology
Bene, F. D., & Wyart, C. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20914 · Cited by 87 · see citing works
Mendes, H. W., Neelakantan, U., Liu, Y., Fitzpatrick, S. E., Chen, T., Wu, W., Pruitt, A., Jin, D. S., Jamadagni, P., Carlson, M., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112243 · Cited by 82 · see citing works
Rein, M. L., & Deussing, J. M. (2011) · Molecular Genetics and Genomics · doi:10.1007/s00438-011-0663-7 · Cited by 81 · see citing works
Fisher, D., Olasagasti, I., Tank, D. W., Aksay, E. R. F., & Goldman, M. S. (2013) · Neuron · doi:10.1016/j.neuron.2013.06.041 · Cited by 75 · see citing works
Rea, V., & Raay, T. J. V. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.575575 · Cited by 75 · see citing works
New insights into the early mechanisms of epileptogenesis in a zebrafish model of Dravet syndrome
Tiraboschi, E., Martina, S., van der Ent, W., Grzyb, K., Gaweł, K., Cordero-Maldonado, M. L., Poovathingal, S. K., Heintz, S., Satheesh, S. V., Brattespe, J., et al. (2020) · Epilepsia · doi:10.1111/epi.16456 · Cited by 74 · see citing works
Inada, K., Kohsaka, H., Takasu, E., Matsunaga, T., & Nose, A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0029019 · Cited by 73 · see citing works
Analysis of the Retina in the Zebrafish Model
Avanesov, A. S., & Malicki, J. J. (2010) · Methods in cell biology · doi:10.1016/b978-0-12-384892-5.00006-2 · Cited by 68 · see citing works
Navigational strategies underlying phototaxis in larval zebrafish
Chen, X., & Engert, F. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00039 · Cited by 67 · see citing works
Eimon, P. M., Ghannad‐Rezaie, M., Rienzo, G. D., Allalou, A., Wu, Y., Gao, M., Roy, A., Skolnick, J., & Yanik, M. F. (2018) · Nature Communications · doi:10.1038/s41467-017-02404-4 · Cited by 65 · see citing works
Genetic Control of Collective Behavior in Zebrafish
Tang, W., Davidson, J. D., Zhang, G., Conen, K. E., Fang, J., Serluca, F. C., Li, J., Xiong, X., Coble, M., Tsai, T., et al. (2020) · iScience · doi:10.1016/j.isci.2020.100942 · Cited by 62 · see citing works
Hwang, H., & Lu, H. (2012) · Biotechnology Journal · doi:10.1002/biot.201200129 · Cited by 62 · see citing works
Stirman, J. N., Crane, M. M., Husson, S. J., GOTTSCHALK, A. R., & Lu, H. (2012) · Nature Protocols · doi:10.1038/nprot.2011.433 · Cited by 61 · see citing works
Movement, technology and discovery in the zebrafish
McLean, D. L., & Fetcho, J. R. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.09.011 · Cited by 60 · see citing works
d’Amora, M., Galgani, A., Marchese, M., Tantussi, F., Faraguna, U., Angelis, F. D., & Giorgi, F. S. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24097702 · Cited by 57 · see citing works
Advancing epilepsy treatment through personalized genetic zebrafish models
Griffin, A., Krasniak, C. S., & Baraban, S. C. (2016) · Progress in brain research · doi:10.1016/bs.pbr.2016.03.012 · Cited by 57 · see citing works
Optogenetic manipulation of neural and non‐neural functions
Yawo, H., Asano, T., Sakai, S., & Ishizuka, T. (2013) · Development Growth & Differentiation · doi:10.1111/dgd.12053 · Cited by 55 · see citing works
Imaging epilepsy in larval zebrafish
Burrows, D. R. W., Samarut, É., Liu, J., Baraban, S. C., Richardson, M. P., Meyer, M. P., & Rosch, R. E. (2020) · European Journal of Paediatric Neurology · doi:10.1016/j.ejpn.2020.01.006 · Cited by 55 · see citing works
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 54 · see citing works
Channelrhodopsin-2 Localised to the Axon Initial Segment
Grubb, M. S., & Burrone, J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013761 · Cited by 54 · see citing works
Feierstein, C. E., Portugues, R., & Orger, M. B. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.11.046 · Cited by 52 · see citing works
Gaze-Stabilizing Central Vestibular Neurons Project Asymmetrically to Extraocular Motoneuron Pools
Schoppik, D., Bianco, I. H., Prober, D. A., Douglass, A. D., Robson, D. N., Li, J., Greenwood, J. S. F., Soucy, E. R., Engert, F., & Schier, A. F. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1711-17.2017 · Cited by 52 · see citing works
Use of Zebrafish Models to Boost Research in Rare Genetic Diseases
Crouzier, L., Richard, É. M., Sourbron, J., Lagae, L. G., Maurice, T., & Delprat, B. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222413356 · Cited by 51 · see citing works
Let there be light: zebrafish neurobiology and the optogenetic revolution
Wyart, C., & Bene, F. D. (2011) · Reviews in the Neurosciences · doi:10.1515/rns.2011.013 · Cited by 48 · see citing works
Challenges in understanding psychiatric disorders and developing therapeutics: a role for zebrafish
McCammon, J. M., & Sive, H. L. (2015) · Disease Models & Mechanisms · doi:10.1242/dmm.019620 · Cited by 48 · see citing works
Control of a specific motor program by a small brain area in zebrafish
Fajardo, O., Zhu, P., & Friedrich, R. W. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00067 · Cited by 47 · see citing works
Zebrafish 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 · see citing works
Hsieh, J.-Y., Ulrich, B. N., Issa, F. A., Wan, J., & Papazian, D. M. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00147 · Cited by 46 · see citing works
Fish in a dish: drug discovery for hearing habilitation
Esterberg, R., Coffin, A. B., Ou, H. C., Simon, J. A., Raible, D. W., & Rubel, E. W. (2012) · Drug Discovery Today Disease Models · doi:10.1016/j.ddmod.2012.02.001 · Cited by 44 · see citing works
Behavioral Comorbidities and Drug Treatments in a Zebrafishscn1labModel of Dravet Syndrome
Grone, B. P., Qu, T., & Baraban, S. C. (2017) · eNeuro · doi:10.1523/eneuro.0066-17.2017 · Cited by 44 · see citing works
Cannabis constituents reduce seizure behavior in chemically-induced and scn1a-mutant zebrafish
Thornton, C., Dickson, K., Carty, D. R., Ashpole, N. M., & Willett, K. L. (2020) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2020.107152 · Cited by 44 · see citing works
A zebrafish-centric approach to antiepileptic drug development
Baraban, S. C. (2021) · Disease Models & Mechanisms · doi:10.1242/dmm.049080 · Cited by 43 · see citing works
Optogenetic excitation of neurons with channelrhodopsins
Lin, J. Y. (2012) · Progress in brain research · doi:10.1016/b978-0-444-59426-6.00002-1 · Cited by 43 · see citing works
Extraocular motoneuron pools develop along a dorsoventral axis in zebrafish, Danio rerio
Greaney, M. R., Privorotskiy, A., D’Elia, K. P., & Schoppik, D. (2016) · The Journal of Comparative Neurology · doi:10.1002/cne.24042 · Cited by 41 · see citing works
Addressing the Genetics of Human Mental Health Disorders in Model Organisms
McCammon, J. M., & Sive, H. L. (2015) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-090314-050048 · Cited by 40 · see citing works
Model systems for studying cellular mechanisms of SCN1A -related epilepsy
Schutte, S. S., Schutte, R. J., Barragan, E. V., & O’Dowd, D. K. (2016) · Journal of Neurophysiology · doi:10.1152/jn.00824.2015 · Cited by 39 · see citing works
Cassar, S. C., Dunn, C., & Ramos, M. F. (2020) · Toxicologic Pathology · doi:10.1177/0192623320964748 · Cited by 34 · see citing works
Zebrafish: unraveling genetic complexity through duplicated genes
Tasnim, M., Wahlquist, P., & Hill, J. T. (2024) · Development Genes and Evolution · doi:10.1007/s00427-024-00720-6 · Cited by 32 · see citing works
Current Treatment Strategies and Future Treatment Options for Dravet Syndrome
Ziobro, J. M., Eschbach, K. L., Sullivan, J. E., & Knupp, K. G. (2018) · Current Treatment Options in Neurology · doi:10.1007/s11940-018-0537-y · Cited by 32 · see citing works
Precise Spatiotemporal Control of Optogenetic Activation Using an Acousto-Optic Device
Wang, K., Liu, Y., Li, Y., Guo, Y., Song, P., Zhang, X., Zeng, S., & Wang, Z. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028468 · Cited by 32 · see citing works
Phenotype-Based Screening of Synthetic Cannabinoids in a Dravet Syndrome Zebrafish Model
Griffin, A., Anvar, M., Hamling, K. R., & Baraban, S. C. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.00464 · Cited by 31 · see citing works
Yi, A., Mamaeva, N. V., Li, H., Spudich, J. L., & Rothschild, K. J. (2016) · Biochemistry · doi:10.1021/acs.biochem.6b00104 · Cited by 31 · see citing works
Illusory patterns are fishy for fish, too
Agrillo, C., Petrazzini, M. E. M., & Dadda, M. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00137 · Cited by 30 · see citing works
Evoking and tracking zebrafish eye movement in multiple larvae with ZebEyeTrack
Dehmelt, F. A., von Daranyi, A., Leyden, C., & Arrenberg, A. B. (2018) · Nature Protocols · doi:10.1038/s41596-018-0002-0 · Cited by 30 · see citing works
Self-citationSustained Rhythmic Brain Activity Underlies Visual Motion Perception in Zebrafish
Pérez-Schuster, V., Kulkarni, A., Nouvian, M., Romano, S. A., Lygdas, K., Jouary, A., Dipoppa, M., Pietri, T., Haudrechy, M., Candat, V., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.09.065 · Cited by 30 · see citing works
Analysis of the retina in the zebrafish model
Malicki, J. J., Pooranachandran, N., Nikolaev, A., Fang, X., & Avanesov, A. S. (2016) · Methods in cell biology · doi:10.1016/bs.mcb.2016.04.017 · Cited by 30 · see citing works
Banerji, R., Huynh, C. Q., Figueroa, F., Dinday, M. T., Baraban, S. C., & Patel, M. (2021) · Brain Communications · doi:10.1093/braincomms/fcab004 · Cited by 29 · see citing works
Brain selective transgene expression in zebrafish using an NRSE derived motif
Bergeron, S. A., Hannan, M. C., Codore, H., Fero, K. C., Li, G. H., Moak, Z. B., Yokogawa, T., & Burgess, H. A. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00110 · Cited by 29 · see citing works
Optogenetic perturbations reveal the dynamics of an oculomotor integrator
Gonçalves, P. J., Arrenberg, A. B., Hablitzel, B., Baier, H., & Machens, C. K. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00010 · Cited by 28 · see citing works
Self-citationCelsr3 Is Required for Normal Development of GABA Circuits in the Inner Retina
Lewis, A. A., Wilson, N. M., Stearns, G., Johnson, N. A., Nelson, R., & Brockerhoff, S. E. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002239 · Cited by 28 · see citing works
Investigating the genetics of visual processing, function and behaviour in zebrafish
Renninger, S. L., Schönthaler, H. B., Neuhauss, S. C. F., & Dahm, R. (2011) · Neurogenetics · doi:10.1007/s10048-011-0273-x · Cited by 27 · see citing works
An Overview towards Zebrafish Larvae as a Model for Ocular Diseases
da Rosa, J. G. S., Lopes‐Ferreira, M., & Lima, C. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24065387 · Cited by 26 · see citing works
Anatomy and Connectivity of the Torus Longitudinalis of the Adult Zebrafish
Folgueira, M., Riva-Mendoza, S., Ferreño-Galmán, N., Castro, A., Bianco, I. H., Anadón, R., & Yáñez, J. (2020) · Frontiers in Neural Circuits · doi:10.3389/fncir.2020.00008 · Cited by 26 · see citing works
Brysch, C., Leyden, C., & Arrenberg, A. B. (2019) · BMC Biology · doi:10.1186/s12915-019-0720-y · Cited by 26 · see citing works
Self-citationPredicting 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 25 · see citing works
“The imaged volume includes neurons involved in eye movements 16,21,22,28 .”
Channelrhodopsins: visual regeneration and neural activation by a light switch
Natasha, G., Tan, A., Farhatnia, Y., Rajadas, J., Hamblin, M. R., Khaw, P. T., & Seifalian, A. M. (2013) · New Biotechnology · doi:10.1016/j.nbt.2013.04.007 · Cited by 25 · see citing works
Kaneda, K., Kasahara, H., Matsui, R., Katoh, T., Mizukami, H., Ozawa, K., Watanabe, D., & Isa, T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018452 · Cited by 25 · see citing works
Optogenetic control of neural activity: The biophysics of microbial rhodopsins in neuroscience
Piatkevich, K. D., & Boyden, E. S. (2023) · Quarterly Reviews of Biophysics · doi:10.1017/s0033583523000033 · Cited by 24 · see citing works
Development of oculomotor circuitry independent of hox3 genes
Ma, L.-H., Grove, C. L., & Baker, R. (2014) · Nature Communications · doi:10.1038/ncomms5221 · Cited by 23 · see citing works
Screening Platforms for Genetic Epilepsies—Zebrafish, iPSC-Derived Neurons, and Organoids
Shcheglovitov, A., & Peterson, R. T. (2021) · Neurotherapeutics · doi:10.1007/s13311-021-01115-5 · Cited by 23 · see citing works
Engineering brain activity patterns by neuromodulator polytherapy for treatment of disorders
Ghannad‐Rezaie, M., Eimon, P. M., Wu, Y., & Yanik, M. F. (2019) · Nature Communications · doi:10.1038/s41467-019-10541-1 · Cited by 23 · see citing works
Carrella, S., D’Agostino, Y., Barbato, S., Huber‐Reggi, S. P., Salierno, F. G., Manfredi, A., Neuhauss, S. C. F., Banfi, S., & Conte, I. (2015) · Developmental Neurobiology · doi:10.1002/dneu.22282 · Cited by 22 · see citing works
Toward molecular genetic dissection of neural circuits for emotional and motivational behaviors
Guo, S., Wagle, M. D., & Mathur, P. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20927 · Cited by 20 · see citing works
Zebrafishdscaml1Deficiency Impairs Retinal Patterning and Oculomotor Function
Ma, M., Ramirez, A. D., Wang, T., Roberts, R. L., Harmon, K. E., Schoppik, D., Sharma, A., Kuang, C., Goei, S. L., Gagnon, J. A., et al. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1783-19.2019 · Cited by 20 · see citing works
- Authors
- Schoonheim, P. J., Arrenberg, A. B., Del Bene, F., & Baier, H.
- Affiliations
- University of California, San Francisco (US)
- Corresponding author
- Baier, Herwig
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-05-19
- Volume
- 30
- Issue
- 20
- Pages
- 7111-7120
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3842466
- OpenAlex
- W2084811348
- Cited by
- 185
- References
- 49
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 9 · 2023: 11 · 2022: 6 · 2021: 8 · 2020: 18 · 2019: 9 · 2018: 9 · 2017: 10 · 2016: 16 · 2015: 12 · 2014: 13 · 2013: 13 · 2012: 11
- FWCI
- 10.08
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Boehringer Ingelheim Stiftung
- National Institutes of Health
- National Eye Institute (R01EY012406)
- National Institute of Neurological Disorders and Stroke (R01NS053358)
- Topics
- Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Keywords
- saccades, optokinetic response, zebrafish, halorhodopsin, channelrhodopsin-2, optogenetics, voltage-gated sodium channels, eye movements, conjugate eye movements, photostimulation
- MeSH terms
- Animals, Bacterial Proteins, Carrier Proteins, Kinetics, Larva, Luminescent Proteins, Microinjections, Mutation, Neurons, Oocytes, Photic Stimulation, Reaction Time, Rhombencephalon, Saccades, Xenopus, Zebrafish, Sodium Channels, Mutagenesis, Site-Directed, Nystagmus, Optokinetic, Halorhodopsins, Zebrafish Proteins, Animals, Genetically Modified
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