Functional role of a specialized class of spinal commissural inhibitory neurons during fast escapes in zebrafish

Journal of Neuroscience

Volumn 29, Issue 21, 2009, Pages 6780-6793

  Satou, Chie ^a,b   Kimura, Yukiko ^a   Kohashi, Tsunehiko ^c   Horikawa, Kazuki ^d,e   Takeda, Hiroyuki ^d   Oda, Yoichi ^c   Higashijima, Shin Ichi ^a,b  

^a OKAZAKI INSTITUTE FOR INTEGRATIVE BIOSCIENCE   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; CELL ACTIVATION; CELL FUNCTION; CELL POPULATION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EMBRYO; GOLDFISH; LARVA; MOTONEURON; MOVEMENT (PHYSIOLOGY); NONHUMAN; PRIORITY JOURNAL; SPINAL CORD NERVE CELL; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; VIBRATION; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BEHAVIOR, ANIMAL; BIOTIN; CALCIUM; DEXTRANS; ELECTRIC STIMULATION; ESCAPE REACTION; GAP JUNCTIONS; GREEN FLUORESCENT PROTEINS; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; LARVA; LASER THERAPY; MEMBRANE POTENTIALS; NEURAL INHIBITION; NEURAL PATHWAYS; PATCH-CLAMP TECHNIQUES; RHODAMINES; SPINAL CORD; SWIMMING; ZEBRAFISH;

EID: 66149190564     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0801-09.2009     Document Type: Article

References (40)

1. Baba SA, Mogami Y (1985) An approach to digital image analysis of bending shapes of eukaryotic flagella and cilia. Cell Motil 5:475-489.
2. Bhatt DH, Otto SJ, Depoister B, Fetcho JR (2004) Cyclic AMP-induced repair of zebrafish spinal circuits. Science 305:254-258. (Pubitemid 38886741)
3. Burgess HA, Granato M (2007) Sensorimotor gating in larval zebrafish. J Neurosci 27:4984-4994. (Pubitemid 46699065)
4. Casagrand JL, Guzik AL, Eaton RC (1999) Mauthner and reticulospinal responses to the onset of acoustic pressure and acceleration stimuli. J Neurophysiol 82:1422-1437. (Pubitemid 29439707)
5. Day JW, Hall DH, Hall LM, Bennett MV (1983) α-Bungarotoxin labeling and acetylcholinesterase localization at the Mauthner fiber giant synapse in the hatchetfish. J Neurosci 3:272-279.
6. Diamond J (1971) The Mauthner cell. In: Fish physiology, Vol V (Hoar WS, Randall DJ, eds), pp 265-346. New York: Academic.
7. Eaton RC (1984) Neural mechanisms of startle behavior. New York: Plenum.
8. Eaton RC, Lavender WA, Wieland CM (1981) Identification of Mauthner-initiated response patterns in goldfish: evidence from simultaneous cinematography and electrophysiology. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 144:521-531.
9. Eaton RC, DiDomenico R, Nissanov J (1988) Flexible body dynamics of the goldfish C-start: implications for reticulospinal command mechanisms. J Neurosci 8:2758-2768. (Pubitemid 18219065)
10. Eaton RC, Hofve JC, Fetcho JR (1995) Beating the competition: the reliability hypothesis for Mauthner axon size. Brain Behav Evol 45:183-194.
11. Eaton RC, Lee RK, Foreman MB (2001) The Mauthner cell and other identified neurons of the brainstem escape network of fish. Prog Neurobiol 63:467-485. (Pubitemid 32332880)
12. Fetcho JR (1990) Morphological variability, segmental relationships, and functional role of a class of commissural interneurons in the spinal cord of goldfish. J Comp Neurol 299:283-298. (Pubitemid 20319168)
13. Fetcho JR (1991) Spinal network of the Mauthner cell. Brain Behav Evol 37:298-316.
14. Fetcho JR, Faber DS (1988) Identification of motoneurons and interneurons in the spinal network for escapes initiated by the Mauthner cell in goldfish. J Neurosci 8:4192-4213. (Pubitemid 19017403)
15. Halloran MC, Sato-Maeda M, Warren JT, Su F, Lele Z, Krone PH, Kuwada JY, Shoji W (2000) Laser-induced gene expression in specific cells of transgenic zebrafish. Development 127:1953-1960. (Pubitemid 30311798)
16. Hatta K, Korn H (1999) Tonic inhibition alternates in paired neurons that set direction of fish escape reaction. Proc Natl Acad Sci U S A 96:12090-12095. (Pubitemid 29502863)
17. Higashijima S, Mandel G, Fetcho JR (2004a) Distribution of prospective glutamatergic, glycinergic, and GABAergic neurons in embryonic and larval zebrafish. J Comp Neurol 480:1-18. (Pubitemid 39453134)
18. Higashijima S, Schaefer M, Fetcho JR (2004b) Neurotransmitter properties of spinal interneurons in embryonic and larval zebrafish. J Comp Neurol 480:19-37. (Pubitemid 39453135)
19. Higashijima S, Masino MA, Mandel G, Fetcho JR (2004c) Engrailed-1 expression marks a primitive class of inhibitory spinal interneuron. J Neurosci 24:5827-5839. (Pubitemid 38857237)
20. Jayne BC, Lauder GV (1993) Red and white muscle activity and kinematics of the escape response of the bluegill sunfish during swimming. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 173:495-508.
21. Kawakami K (2005) Transposon tools and methods in zebrafish. Dev Dyn 234:244-254. (Pubitemid 41369134)
22. Kimura Y, Okamura Y, Higashijima S (2006) alx, a zebrafish homolog of Chx10, marks ipsilateral descending excitatory interneurons that participate in the regulation of spinal locomotor circuits. J Neurosci 26:5684-5697. (Pubitemid 44315260)
23. Kohashi T, Oda Y (2008) Initiation of Mauthner- or non-Mauthner-mediated fast escape evoked by different modes of sensory input. J Neurosci 28:10641-10653.
24. Korn H, Faber DS (2005) The Mauthner cell half a century later: a neurobiological model for decision-making? Neuron 47:13-28.
25. Liao JC, Fetcho JR (2008) Shared versus specialized glycinergic spinal interneurons in axial motor circuits of larval zebrafish. J Neurosci 28:12982-12992.
26. Nagayoshi S, Hayashi E, Abe G, Osato N, Asakawa K, Urasaki A, Horikawa K, Ikeo K, Takeda H, Kawakami K (2008) Insertional mutagenesis by the Tol2 transposon-mediated enhancer trap approach generated mutations in two developmental genes: tcf7 and synembryn-like. Development 135:159-169.
27. Nissanov J, Eaton RC, DiDomenico R (1990) The motor output of the Mauthner cell, a reticulospinal command neuron. Brain Res 517:88-98. (Pubitemid 20207224)
28. O'Brien J, Bruzzone R, White TW, Al-Ubaidi MR, Ripps H (1998) Cloning and expression of two related connexins from the perch retina define a distinct subgroup of the connexin family. J Neurosci 18:7625-7637. (Pubitemid 28441005)
29. O'Malley DM, Kao YH, Fetcho JR (1996) Imaging the functional organization of zebrafish hindbrain segments during escape behaviors. Neuron 17:1145-1155. (Pubitemid 27021100)
30. Pereda A, O'Brien J, Nagy JI, Bukauskas F, Davidson KG, Kamasawa N, Yasumura T, Rash JE (2003) Connexin35 mediates electrical transmission at mixed synapses on Mauthner cells. J Neurosci 23:7489-7503. (Pubitemid 37034065)
31. Rash JE, Yasumura T, Dudek FE, Nagy JI (2001) Cell-specific expression of connexins and evidence of restricted gap junctional coupling between glial cells and between neurons. J Neurosci 21:1983-2000. (Pubitemid 32221382)
32. Roberts A, Clarke JDW (1982) The neuroanatomy of an amphibian embryo spinal cord. Philos Trans R Soc Lond B Biol Sci 296:195-212.
33. Shiba K, Ohmuro J, Mogami Y, Nishigaki T, Wood CD, Darszon A, Tatsu Y, Yumoto N, Baba SA (2005) Sperm-activating peptide induces asymmetric flagellar bending in sea urchin sperm. Zoolog Sci 22:293-299. (Pubitemid 40607694)
34. Svoboda KR, Fetcho JR (1996) Interactions between the neural networks for escape and swimming in goldfish. J Neurosci 16:843-852. (Pubitemid 26028840)
35. Takahashi M, Narushima M, Oda Y (2002) In vivo imaging of functional inhibitory networks on the Mauthner cell of larval zebrafish. J Neurosci 22:3929-3938.
36. 2+ in flagellar movement and motility in single sea urchin sperm. J Cell Biol 169:725-731.
37. Yasargil GM, Diamond J (1968) Startle-response in teleost fish: an elementary circuit for neural discrimination. Nature 220:241-243.
38. Yasargil GM, Sandri C (1987) Morphology of the Mauthner axon inhibitory system in tench (Tinca tinca L.) spinal cord. Neurosci Lett 81:63-68.
39. Yasargil GM, Sandri C (1990) Topography and ultrastructure of commissural interneurons that may establish reciprocal inhibitory connections of the Mauthner axons in the spinal cord of the tench, Tinca tinca L. J Neurocytol 19:111-126. (Pubitemid 20056735)
40. Zottoli SJ (1977) Correlation of the startle reflex and Mauthner cell auditory responses in unrestrained goldfish. J Exp Biol 66:243-254.