Optical stimulation of zebrafish hair cells expressing channelrhodopsin-2

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Monesson Olson, Bryan D ^a   Browning Kamins, Jenna ^a   Aziz Bose, Razina ^a   Kreines, Fabiana ^a   Trapani, Josef G ^a  

^a AMHERST COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHANNELRHODOPSIN 2; SENSORY RHODOPSIN; UNCLASSIFIED DRUG; CHANNELRHODOPSIN-2, ZEBRAFISH; RHODOPSIN; ZEBRAFISH PROTEIN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL MEMBRANE POTENTIAL; CELLULAR DISTRIBUTION; CELLULAR PARAMETERS; CHR2 GENE; CONTROLLED STUDY; ESCAPE BEHAVIOR; FREQUENCY MODULATION; GENE; GENE ACTIVATION; GENE EXPRESSION; GENE FUNCTION; GENE INTERACTION; HAIR CELL; IN VIVO STUDY; LARVAL STAGE; LIGHT INTENSITY; LIGHT RELATED PHENOMENA; MAUTHNER CELL ACTIVITY; MECHANOTRANSDUCTION; MYO6B GENE; NERVE CELL STIMULATION; NONHUMAN; OPTICAL STIMULATION; OPTOGENETICS; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RESPONSE TIME; SENSORY NERVE; SENSORY STIMULATION; SPIKE WAVE; STIMULUS RESPONSE; TRANSGENIC ZEBRAFISH; ANIMAL; CELL LINE; ELECTROPHYSIOLOGY; GENE EXPRESSION REGULATION; GENETICS; LIGHT; METABOLISM; PHOTOSTIMULATION; PHYSIOLOGY; TRANSGENE; TRANSGENIC ANIMAL; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL LINE; ELECTROPHYSIOLOGY; ESCAPE REACTION; GENE EXPRESSION REGULATION; HAIR CELLS, AUDITORY; LIGHT; MECHANOTRANSDUCTION, CELLULAR; PHOTIC STIMULATION; PROMOTER REGIONS, GENETIC; RHODOPSIN; TRANSGENES; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84900390232     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096641     Document Type: Article

References (50)

1. Hudspeth AJ (1985) The Cellular Basis of Hearing: The Biophysics of Hair Cells. Science 230: 745-752.
2. Stommel EW, Stephens RE, Alkon DL (1980) Motile statocyst cilia transmit rather than directly transduce mechanical stimuli. J Cell Biol 87: 652-662.
3. Fettiplace R (2009) Defining features of the hair cell mechanoelectrical transducer channel. Pflugers Arch 458: 1115-1123. doi:10.1007/s00424-009-0683-x.
4. Nicolson T (2005) The genetics of hearing and balance in zebrafish. Annu Rev Genet 39: 9-22.
5. Safieddine S, El-Amraoui A, Petit C (2012) The Auditory Hair Cell Ribbon Synapse: From Assembly to Function. Annu Rev Neurosci 35: 509-528. doi:10.1146/annurev-neuro-061010-113705.
6. Beurg M, Fettiplace R, Nam J-H, Ricci AJ (2009) Localization of inner hair cell mechanotransducer channels using high-speed calcium imaging. Nat Neurosci 12: 553-558. doi:10.1038/nn.2295.
7. Fuchs PA (2005) Time and intensity coding at the hair cell's ribbon synapse. J Physiol 566: 7-12. doi:10.1113/jphysiol.2004.082214.
8. Ricci AJ, Kennedy HJ, Crawford AC, Fettiplace R (2005) The Transduction Channel Filter in Auditory Hair Cells. J Neurosci 25: 7831-7839. doi:10.1523/JNEUROSCI.1127-05.2005. (Pubitemid 41208655)
9. Ricci AJ, Crawford AC, Fettiplace R (2003) Tonotopic variation in the conductance of the hair cell mechanotransducer channel. Neuron 40: 983-990. (Pubitemid 37522055)
10. Goutman JD, Glowatzki E (2007) Time course and calcium dependence of transmitter release at a single ribbon synapse. Proc Natl Acad Sci U S A 104: 16341-16346. doi:10.1073/pnas.0705756104. (Pubitemid 350099406)
11. Moser T, Beutner D (2000) Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proc Natl Acad Sci U S A 97: 883-888. (Pubitemid 30070404)
12. Schnee ME, Santos-Sacchi J, Castellano-Muñoz M, Kong J-H, Ricci AJ (2011) Calcium-dependent synaptic vesicle trafficking underlies indefatigable release at the hair cell afferent fiber synapse. Neuron 70: 326-338. doi:10.1016/ j.neuron.2011.01.031.
13. Zampini V, Johnson SL, Franz C, Lawrence ND, Münkner S, et al. (2010) Elementary properties of CaV1.3 Ca(2 +) channels expressed in mouse cochlear inner hair cells. J Physiol 588: 187-199. doi:10.1113/jphysiol.2009. 181917.
14. Obholzer N, Wolfson S, Trapani JG, Mo W, Nechiporuk A, et al. (2008) Vesicular glutamate transporter 3 is required for synaptic transmission in zebrafish hair cells. J Neurosci 28: 2110-2118. doi:10.1523/JNEUROSCI.5230-07. 2008. (Pubitemid 351317615)
15. Nagel G, Ollig D, Fuhrmann M, Kateriya S, Musti AM, et al. (2002) Channelrhodopsin-1: A Light-Gated Proton Channel in Green Algae. Science 296: 2395-2398. doi:10.1126/science.1072068. (Pubitemid 34734214)
16. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, et al. (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci 100: 13940-13945. (Pubitemid 37499170)
17. Boyden ES, Deisseroth K, Wang L-P, Zhang F (2006) Channelrhodopsin-2 and optical control of excitable cells. Nat Methods 3: 785+.
18. Douglass AD, Kraves S, Deisseroth K, Schier AF, Engert F (2008) Escape behavior elicited by single, channelrhodopsin-2-evoked spikes in zebrafish somatosensory neurons. Curr Biol CB 18: 1133-1137. doi:10.1016/j.cub.2008.06. 077.
19. Schoonheim PJ, Arrenberg AB, Bene FD, Baier H (2010) Optogenetic Localization and Genetic Perturbation of Saccade-Generating Neurons in Zebrafish. J Neurosci 30: 7111-7120. doi:10.1523/JNEUROSCI.5193-09.2010.
20. Umeda K, Shoji W, Sakai S, Muto A, Kawakami K, et al. (2013) Targeted expression of a chimeric channelrhodopsin in zebrafish under regulation of Gal4-UAS system. Neurosci Res 75: 69-75. doi:10.1016/j.neures.2012.08.010.
21. Eaton RC, Farley RD, Kimmel CB, Schabtach E (1977) Functional development in the Mauthner cell system of embryos and larvae of the zebra fish. J Neurobiol 8: 151-172. doi:10.1002/neu.480080207. (Pubitemid 8070900)
22. Eaton RC, Lee RKK, Foreman MB (2001) The Mauthner cell and other identified neurons of the brainstem escape network of fish. Prog Neurobiol 63: 467-485. doi:10.1016/S0301-0082(00)00047-2. (Pubitemid 32332880)
23. Liu KS, Fetcho JR (1999) Laser Ablations Reveal Functional Relationships of Segmental Hindbrain Neurons in Zebrafish. Neuron 23: 325-335. doi:10.1016/S0896-6273(00)80783-7. (Pubitemid 29315727)
24. Pujol-Martí J, Baudoin J-P, Faucherre A, Kawakami K, López-Schier H (2010) Progressive neurogenesis defines lateralis somatotopy. Dev Dyn 239: 1919-1930. doi:10.1002/dvdy.22320.
25. Korn H, Faber DS (1975) Inputs from the posterior lateral line nerves upon the goldfish Mauthner cell. I. Properties and synaptic localization of the excitatory component. Brain Res 96: 342-348.
26. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310. doi:10.1002/aja.1002030302.
27. Soroldoni D, Hogan BM, Oates AC (2009) Simple and efficient transgenesis with meganuclease constructs in zebrafish. Methods Mol Biol 546: 117-130. doi:10.1007/978-1-60327-977-2-8.
28. Trapani JG, Nicolson T (2010) Physiological recordings from zebrafish lateral-line hair cells and afferent neurons. Methods Cell Biol 100: 219-231. doi:10.1016/B978-0-12-384892-5.00008-6.
29. Issa FA, O'Brien G, Kettunen P, Sagasti A, Glanzman DL, et al. (2011) Neural circuit activity in freely behaving zebrafish (Danio rerio). J Exp Biol 214: 1028-1038. doi:10.1242/jeb.048876.
30. Prugh JI, Kimmel CB, Metcalfe WK (1982) Noninvasive recording of the Mauthner neurone action potential in larval zebrafish. J Exp Biol 101: 83-92.
31. Goldberg JM, Brown PB (1969) Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J Neurophysiol 32: 613-636.
32. Heil P (2004) First-spike latency of auditory neurons revisited. Curr Opin Neurobiol 14: 461-467. doi:10.1016/j.conb.2004.07.002.
33. Furukawa S, Middlebrooks JC (2002) Cortical Representation of Auditory Space: Information-Bearing Features of Spike Patterns. J Neurophysiol 87: 1749-1762. doi:10.1152/jn.00491.2001. (Pubitemid 34670741)
34. Tan X, Wang X, Yang W, Xiao Z (2008) First spike latency and spike count as functions of tone amplitude and frequency in the inferior colliculus of mice. Hear Res 235: 90-104. doi:10.1016/j.heares.2007.10.002. (Pubitemid 350297669)
35. Eggermont JJ (1998) Azimuth Coding in Primary Auditory Cortex of the Cat. II. Relative Latency and Interspike Interval Representation. J Neurophysiol 80: 2151-2161.
36. Heil P (1997) Auditory Cortical Onset Responses Revisited. I. First-Spike Timing. J Neurophysiol 77: 2616-2641.
37. VanRullen R, Guyonneau R, Thorpe SJ (2005) Spike times make sense. Trends Neurosci 28: 1-4. doi:10.1016/j.tins.2004.10.010. (Pubitemid 40038795)
38. Fenno L, Yizhar O, Deisseroth K (2011) The Development and Application of Optogenetics. Annu Rev Neurosci 34: 389-412. doi:10.1146/annurev-neuro-061010- 113817.
39. Karavitaki KD, Corey DP (2010) Sliding adhesion confers coherent motion to hair cell stereocilia and parallel gating to transduction channels. J Neurosci 30: 9051-9063. doi:10.1523/JNEUROSCI.4864-09.2010.
40. Kozlov AS, Risler T, Hudspeth AJ (2007) Coherent motion of stereocilia assures the concerted gating of hair-cell transduction channels. Nat Neurosci 10: 87-92. doi:10.1038/nn1818. (Pubitemid 46026531)
41. Trapani JG, Obholzer N, Mo W, Brockerhoff SE, Nicolson T (2009) Synaptojanin1 is required for temporal fidelity of synaptic transmission in hair cells. PLoS Genet 5: e1000480. doi:10.1371/journal.pgen.1000480.
42. Farris HE, LeBlanc CL, Goswami J, Ricci AJ (2004) Probing the pore of the auditory hair cell mechanotransducer channel in turtle. J Physiol 558: 769-792. doi:10.1113/jphysiol.2004.061267. (Pubitemid 39199104)
43. Jaramillo F, Hudspeth AJ (1991) Localization of the hair cell's transduction channels at the hair bundle's top by iontophoretic application of a channel blocker. Neuron 7: 409-420.
44. Gunaydin LA, Yizhar O, Berndt A, Sohal VS, Deisseroth K, et al. (2010) Ultrafast optogenetic control. Nat Neurosci 13: 387-392. doi:10.1038/nn.2495.
45. Eatock RA, Corey DP, Hudspeth AJ (1987) Adaptation of mechanoelectrical transduction in hair cells of the bullfrog's sacculus. J Neurosci 7: 2821-2836.
46. Smedemark-Margulies N, Trapani JG (2013) Tools, methods, and applications for optophysiology in neuroscience. Front Mol Neurosci 6: 18. doi:10.3389/fnmol.2013.00018.
47. Faber DS, Korn H (1975) Inputs from the posterior lateral line nerves upon the goldfish Mauthner cells. II. Evidence that the inhibitory components are mediated by interneurons of the recurrent collateral network. Brain Res 96: 349-356.
48. Korn H, Faber DS, Mariani J (1974) [Existence of projections of posterior nerves from the lateral line on the Mauthner cell; their antagonistic effect on the activation of this neuron by vestibular afferences]. Comptes Rendus Hebd Séances Académie Sci Sér Sci Nat 279: 413-416.
49. Korn H, Faber DS (2005) The Mauthner Cell Half a Century Later: A Neurobiological Model for Decision-Making? Neuron 47: 13-28. doi:10.1016/j.neuron.2005.05.019. (Pubitemid 40922847)
50. Liao JC, Haehnel M (2012) Physiology of afferent neurons in larval zebrafish provides a functional framework for lateral line somatotopy. J Neurophysiol 107: 2615-2623. doi:10.1152/jn.01108.2011.