Neural circuits that drive startle behavior, with a focus on the Mauthner cells and spiral fiber neurons of fishes

Journal of Neurogenetics

Volumn 30, Issue 2, 2016, Pages 89-100

  Hale, Melina E ^a,b   Katz, Hilary R ^a,b   Peek, Martin Y ^c   Fremont, Rachel T ^a,b,d  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Escape; giant neurons; hindbrain; startle; zebrafish

Indexed keywords

ADULT ANIMAL; ANIMAL BEHAVIOR; ANIMAL CELL; CONNECTOME; CRAYFISH; DROSOPHILA; EMBRYO; INTERNEURON; MAUTHNER CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; RHOMBENCEPHALON; SPINAL CORD; SPIRAL FIBER NEURON; STARTLE REFLEX; STIMULUS; TELEOST; VERTEBRATE; ANIMAL; FISH; NERVE CELL; NERVE TRACT; PHYSIOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; FISHES; NEURAL PATHWAYS; NEURONS; REFLEX, STARTLE;

EID: 84976322331     PISSN: 01677063     EISSN: 15635260     Source Type: Journal    
DOI: 10.1080/01677063.2016.1182526     Document Type: Review

References (90)

1. M.B.Ahrens,, M.B.Orger,, D.N.Robson,, J.M.Li,, & P.J.Keller, (2013). Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nature Methods, 10, 413–420.
2. M.J.Allan,, T.A.Godenschwege,, M.A.Tanouye,, & P.Phelan, (2006). Making an escape: development and function of the Drosophila giant fiber system. Seminars in cell and Developmental Biology, 17, 31–41.
3. J.P.Bacon,, & N.J.Strausfeld, (1986). The dipteran ‘Giant fibre’ pathway: neurons and signals. Journal of Comparative Physiology A, 158, 529–548.
4. R.A.Baines,, J.P.Uhler,, A.Thompson,, S.T.Sweeney,, & M.Bate, (2001). Altered electrical properties in drosophila neurons. The Journal of Neuroscience, 21, 1523–1531.
5. R.R.Bernhardt,, A.B.Chitnis,, L.Lindamer,, & J.Y.Kuwada, (1915). Mauthner’s cell and the nucleus motorius tegmenti. Journal of Comparative Neurology, 25, 87–128.
6. R.R.Bernhardt,, A.B.Chitnis,, L.Lindamer,, & J.Y.Kuwada, (1990). Identification of spinal neurons in the embryonic and larval zebrafish. Journal of Comparative Neurology, 302, 603–616.
7. H.S.Bierman,, S.J.Zottoli,, & M.E.Hale, (2009). Evolution of the Mauthner axon cap. Brain Behavior and Evolution, 73, 174–187.
8. D.Bodian, (1937). The structure of the vertebrate synapse. A study of the axon endings on Mauthner’s cell and neighboring centers in the goldfish. Journal of Comparative Neurology, 68, 117–159.
9. A.Borst, (2014). Neural circuits for elementary motion detection. Journal of Neurogenetics, 2014, 361–373.
10. G.M.Card, (2012). Escape behaviors in insects. Current Opinion in Neurobiology, 22, 180–186.
11. G.Card,, & M.Dickinson, (2008a). Performance trade-offs in the flight initiation of Drosophila. Journal of Experimental Biology, 211, 341–353.
12. G.Card,, & M.Dickinson, (2008b). Visually mediated motor planning in the escape response of Drosophila. Current Biology, 18, 1300–1307.
13. W.Cho,, U.Heberlein,, & F.W.Wolf, (2004). Habituation of an odorant-induced startle response in Drosophila. Genes, Brain and Behavior, 3, 127–137.
14. S.Currie,, & R.C.Carlsen, (1985). A rapid startle response in larval lampreys. Brain Research, 358, 367–371.
15. M.I.Davis,, D.S.Gendelman,, M.D.Tischler,, & P.M.Gendelman, (1982). A primary acoustic startle circuit: lesion and stimulation studies. The Journal of Neuroscience, 2, 791–805.
16. S.E.J.De Vries,, & T.R.Clandinin, (2012). Loom sensitive neurons link computation to action in the Drosophila visual system. Current Biology, 22, 353–362.
17. J.Diamond, 1971. The Mauthner cell. In: W.S.Hoar,, D.J.Randall, eds. Fish Physiology vol. V., New York: Academic Press, 265–346.
18. L.M.Dill, (1974). The escape response of the zebra danio (Brachdanio rerio). I. The stimulus for escape. Animal Behaviour, 22, 710–721.
19. P.Domenici,, & R.Blake, (1997). The kinematics and performance of fish fast-start swimming. Journal of Experimental Biology, 200, 1165–1178.
20. J.A.Doudna,, & E.Charpentier, (2014). The new frontier of genome engineering with CRISPR-Cas9. Science, 346, 1077–1087.
21. T.W.Dunn,, C.Gebhardt,, E.A.Naumann,, C.Riegler,, M.B.Ahrens,, F.Engert,, & F.Del Bene, (2016). Neural circuits underlying visually evoked escapes in larval zebrafish. Neuron, 89, 613–628.
22. R.C.Eaton,, & S.D.Emberley, (1991). How stimulus direction determines the trajectory of the Mauthner-initiated escape response in a teleost fish. Journal of Experimental Biology, 161, 469–487.
23. R.C.Eaton,, R.K.K.Lee,, & M.B.Foreman, (2001). The Mauthner cell and other identified neurons of the brainstem escape network of fish. Progress in Neurobiology, 63, 467–485.
24. D.H.Edwards,, W.J.Heitler, and F.B.Krasne, (1999). Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish. Trends in Neurosciences, 22, 153–161.
25. D.S.Faber,, & H.Korn, 1978. Neurobiology of the Mauthner Cell. New York: Raven Press.
26. L.Facchin,, H.A.Burgess,, M.Siddiqi,, M.Granato,, & M.E.Halpern, (2009). Determining the function of zebrafish epithalamic asymmetry. Philosophical Transactions of the Royal Society B, 364, 1021–1032.
27. J.R.Fetcho,, & S.D.Faber, (1988). Identification of motoneurons and interneurons in the spinal network for escapes initiated by the Mauthner cell in goldfish. The Journal of Neuroscience, 8, 4192–4213.
28. J.R.Fetcho,, & D.M.O'Malley, (1995). Visualization of active neural circuitry in the spinal cord of intact zebrafish. Journal of Neurophysiology, 73, 399–406.
29. M.B.Foreman,, & C.R.Eaton, (1993). The direction change concept for reticulospinal control of goldfish escape. The Journal of Neuroscience, 13, 4101–4113.
30. R.Gómez-Nieto,, C.José de Anchieta,, O.Castellano,, L.Millian-Morell,, M.E.Rubio,, & D.E.López, (2014). Origin and function of short-latency inputs to the neural substrates underlying the acoustic startle reflex. Frontiers in Neuroscience, 8, 216. doi:10.3389/fnins.2014.00216.
31. M.Granato,, F.J.M.van Eeden,, U.Schach,, T.Trowe,, M.Brand,, M.Furutani-Seiki,, …. C.Nusslein-Volhard, (1996). Genes controlling and mediating locomotion behaviour of the zebrafish embryo and larva. Development, 123,399–413.
32. M.E.Hale, (2002). S- and C-start escape responses of the muskellunge (Esox masquinongy) require alternative neuromotor mechanisms. Journal of Experimental Biology, 205, 2005–2016.
33. M.E.Hale,, D.A.Ritter, and R.J.Fetcho, (2001). A confocal study of spinal interneurons in living larval zebrafish. Journal of Comparative Neurology, 437, 1–16.
34. M.E.Hale,, M.A.Kheirbek,, J.E.Schriefer,, & V.E.Prince, (2004). Hox gene misexpression and cell-specific lesions reveal functionality of homeotically transformed neurons. The Journal of Neuroscience, 24, 3070–3076.
35. S.Hammond,, & O.M’Shea, (2007). Escape flight initation in the fly. Journal of Comparative Physiology A, 193, 471–476.
36. M.Heidenreich,, & F.Zhang, (2016). Application of CRISPR-Cas systems in neuroscience. Nature Reviews Neuroscience, 17, 36–44.
37. J.R.Ison,, D.W.McAdam,, & R.G.Hammond, (1973). Latency and amplitude changes in the acoustic startle reflex of the rat produced by variation in auditory prestimulation. Physiology & Behavior, 10, 1035–1039.
38. A.Kamikouchi,, H.K.Inagaki,, T.Effertz,, O.Hendrich,, A.Fiala,, M.C.Göpfert,, & K.Ito, (2009). The neural basis of Drosophila gravity-sensing and hearing. Nature, 458, 165–71.
39. A.Y.Katsov,, & T.R.Clandinin, (2008). Motion processing streams in Drosophila are behaviorally specialized. Neuron, 59, 322–35.
40. Y.Kimura,, Y.Okamura,, & S.-I.Higashijima, (2006). alx, a zebrafish homolog of chx10, marks ipsilateral descending excitatory interneurons that participate in the regulation of spinal locomotor circuits. The Journal of Neuroscience, 26, 5684–5697.
41. D.G.King,, & R.J.Wyman, (1980). Anatomy of the giant fibre pathway in Drosophila. I. Three thoracic components of the pathway. Journal of Neurocytology, 9, 753–770.
42. N.C.Klapoetke,, Y.Murata,, S.S.Kim,, S.R.Pulver,, A.Birdsey-Benson,, Y.K.Cho,, … E.S.Boyden, (2014). Independent optical excitation of distinct neural populations. Nature Methods, 11, 338–346.
43. M.Koch, (1999). The neurobiology of startle. Progress in Neurobiology, 59, 107–128.
44. M.Koch,, & H.U.Schnitzler, (1997). The acoustic startle response in rats—circuits mediating evocation, inhibition and potentiation. Behavioural Brain Research, 89, 35–49.
45. H.Korn,, & S.D.Faber, (1975). An electrically mediated inhibition in goldfish medulla. Journal of Neurophysiology, 38, 452–471.
46. H.Korn,, & S.D.Faber, (2005). The Mauthner cell half a century later: a neurobiological model for decision-making? Neuron, 47, 13–28.
47. M.Koyama,, A.Kinkhabwala,, C.Satou,, S.-I.Higashijima,, & J.R.Fetcho, (2011). Mapping a sensory-motor network onto a structural and functional ground plan in the hindbrain. Proceedings of the National Academy of Sciences of the United States of America, 108, 1170–1175.
48. F.B.Krasne,, W.J.Heitler,, & D.H.Edwards, (2014). The escape behavior of crayfish. Nervous Systems and Control of Behavior, 3, 396–427.
49. A.M.Lacoste,, D.Schoppik,, D.N.Robson,, M.Haesemeyer,, R.Portugues,, J.M.Li,, … A.F.Schier, (2015). A convergent and essential interneuron pathway for Mauthner-cell-mediated escapes. Current Biology, 25,1526–1534.
50. R.K.Lee,, R.C.Eaton,, & S.J.Zottoli, (1993). Segmental arrangement of reticulospinal neurons in the goldfish hindbrain. Journal of Comparative Neurology, 329, 539–556.
51. R.K.K.Lee,, & C.,.R.Eaton, (1991). Identifiable reticulospinal neurons of the adult zebrafish, Brachydanio Rerio. Journal of Comparative Neurology, 304, 34–52.
52. Y.Lee,, D.E.López,, E.G.Meloni,, & M.Davis, (1996). A primary acoustic startle pathway: obligatory role of cochlear root neurons and the nucleus reticularis pontis caudalis. The Journal of Neuroscience, 16, 3775–3789.
53. B.P.Lehnert,, A.E.Baker,, Q.Gaudry,, A.Chiang,, & R.I.Wilson, (2013). Distinct roles of TRP channels in auditory transduction and amplification in drosophila. Neuron, 77, 115–128.
54. L.Li,, & E.,.J.Dowling, (1997). A dominant form of inherited retinal degeneration caused by a non-photoreceptor cell-specific mutation. Proceedings of the National Academy of Sciences of the United States of America, 94, 11640–11650.
55. J.C.Liao,, & J.R.Fetcho, (2008). Shared versus specialized glycinergic spinal interneurons in axial motor circuits of larval zebrafish. The Journal of Neuroscience, 28, 12982–12992.
56. K.Lingenhöhl,, & E.Friauf, (1992). Giant neurons in the caudal pontine reticular formation receive short latency acoustic input: an intracellular recording and HRP‐study in the rat. Journal of Comparative Neurology, 325, 473–492.
57. K.Lingenhöhl,, & E.Friauf, (1994). Giant neurons in the rat reticular formation: a sensorimotor interface in the elementary acoustic startle circuit. The Journal of Neuroscience, 14, 1176–1194.
58. K.S.Liu,, M.Gray,, S.J.Otto,, J.R.Fetcho,, & C.E.Beattie, (2003). Mutations in deadly seven/notch1a reveal developmental plasticity in the escape response circuit. The Journal of Neuroscience, 23, 8159–8166.
59. K.S.Liu,, & J.R.Fetcho, (1999). Laser ablations reveal functional relationships of segmental hindbrain neurons in zebrafish. Neuron, 23, 325–335.
60. Y.C.Liu,, I.Bailey,, & M.E.Hale, (2012). Alternative startle motor patterns and behaviors in the larval zebrafish (Danio rerio). Journal of Comparative Physiology A 198, 11–24.
61. Y.C.Liu,, & M.E.Hale, (2014). Alternative forms of axial startle behaviors in fishes. Zoology, 117, 36–47.
62. K.Lorent,, K.S.Liu,, J.R.Fetcho,, & M.Granato, (2001). The zebrafish space cadet gene controls axonal pathfinding of neurons that modulate fast turning movements. Development, 128, b2131–2142.
63. L.Mauthner, (1859). Untersuchungen uuml;ber den Bau des Ruuml;ckenmarks der Fische. Eine vorlauml;ufige Mittheilung. Sitzgsber Kaiserl Akad Wiss Wien Math-Naturw Classe, 34, 31–6.
64. J.M.McClintock,, M.A.Kheirbek,, & V.E.Prince, (2002). Knockdown of duplicated zebrafish hoxb1b genes reveals distinct roles in hindbrain patterning and a novel mechanism of duplicate gene retention. Development, 129, 2339–2354.
65. J.J.Milde,, & N.J.Strausfeld, (1990). Cluster Organization and Response Characteristics of the Giant Fiber Pathway of the Blowfly Calliphora erythrocephala. Journal of Comparative Neurology, 294, 57–75.
66. L.Mu,, J.P.Bacon,, K.Ito,, & N.J.Strausfeld, (2014). Responses of Drosophila giant descending neurons to visual and mechanical stimuli. Journal of Experimental Biology, 217, 2121–2129.
67. Y.Nakajima, (1974). Fine structure of the synaptic endings on the Mauthner cell of the goldfish. Journal of Comparative Neurology, 156, 375–402.
68. D.M.O’Malley,, Y.-H.Kao,, & J.R.Fetcho, (1996). Imaging the functional organization of zebrafish hindbrain segments during escape behavior. Neuron, 17, 1145–1155.
69. A.M.S.Palanca,, S.-L.Lee,, L.E.Yee,, C.Joe-Wong,, L.A.Trinh,, E.Hiroyasu,, … A.Stagasti, (2012). New transgenic reporters identify somatosensory neuron subtypes in larval zebrafish. Developmental Neurobiology, 73, 152–167.
70. D.W.Pfaff,, E.M.Martin,, & D.Faber, (2012). Origins of arousal: roles for medullary reticular neurons. Trends in Neurosciences, 35, 468–476.
71. B.D.Pfeiffer,, T.T.Ngo,, K.L.Hibbard,, C.Murphy,, A.Jenett,, J.W.Truman,, & G.M.Rubin, (2010). Refinement of tools for targeted gene expression in Drosophila. Genetics, 186, 735–755.
72. P.Phelan,, M.Nakagawa,, M.B.Wilkin,, K.G.Moffat,, C.J.O'Kane,, J.A.Davies,, & J.P.Bacon, (1996). Mutations in shaking-B prevent electrical synapse formation in the Drosophila giant fiber system. The Journal of Neuroscience, 16, 1101–1113.
73. M.E.Power, (1948). The thoracico-abdominal nervous system of an adult insect, Drosophila melanogaster. Journal of Comparative Neurology, 88, 347–409.
74. C.M.Rovainen, (1967). Physiological and anatomical studies on large neurons of central nervous system of sea lamprey (Petromyzon marinus). I. Müller and Mauthner cells. Journal of Neurophysiology, 30, 1000–1023.
75. C.Satou,, Y.Kimura,, T.Kohashi,, K.Horikawa,, H.Takeda,, Y.Oda,, & S.-I.Higashijima, (2009). Functional role of a specialized class of spinal commissural inhibitory neurons during fast escapes in zebrafish. The Journal of Neuroscience, 29, 6780–6793.
76. J.W.Scott,, S.J.Zottoli,, N.P.Beatty,, & H.Korn, (1994). Origin and function of spiral fibers projecting to the goldfish Mauthner cell. Journal of Comparative Neurology, 339, 76–90.
77. E.Sivan-Loukianova,, & D.F.Eberl, (2005). Synaptic ultrastructure of the Johnston’s organ axon terminals as revealed by an enhancer trap. Journal of Comparative Neurology, 491, 46–55.
78. K.R.Svoboda,, A.E.Linares,, & A.B.Ribera, (2001). Activity regulates programmed cell death of zebrafish Rohon-Beard neurons. Development, 128, 3511–3520.
79. M.A.Tanouye,, & R.J.Wyman, (1980). Motor outputs of giant nerve fiber in Drosophila. Journal of Neurophysiology, 44, 405–421.
80. I.Temizer,, J.C.Donovan,, H.Baier,, & J.L.Semmelhack, (2015). A visual pathway for looming-evoked escape in larval zebrafish. Current Biology, 25, 1823–1834.
81. D.H.Thorsen,, & M.E.Hale, (2007). Neural development of the zebrafish (Danio rerio) pectoral fin. Journal of Comparative Neurology, 504, 168–184.
82. J.R.Trimarchi,, & A.M.Schneiderman, (1995). Initation of flight in the unrestrained fly, Drosophila melanogaster. Journal of Zoology, 235, 211–222.
83. C.R.Von Reyn,, P.Breads,, M.Y.Peek,, G.Z.Zheng,, W.R.Williamson,, A.L.Lee,, … G.M.Card, (2014). A spike-timing mechanism for action selection. Nature Neuroscience, 17, 962–970.
84. A.Yamamoto,, L.Zwarts,, P.Callaerts,, K.Norga,, T.F.Mackay, C, & R.R.H.Anholt, (2008). Neurogenetic Networks for startle-induced locomotion in Drosophila melanogaster. PNAS, 105, 12393–12398.
85. G.M.Yasargil,, & J.Diamond, (1968). Startle response in teleost fish; an elementary circuit for neural descrimination. Nature, 220, 241–243.
86. J.S.Yeomans,, & P.W.Frankland, (1995). The acoustic startle reflex: neurons and connections. Brain Research Review, 21, 301–314.
87. J.S.Yeomans,, L.Li,, B.W.Scott,, & P.W.Frankland,, (2002). Tactile, acoustic and vestibular systems sum to elicit the startle reflex. Neuroscience & Biobehavioral Reviews, 26, 1–11.
88. S.J.Zottoli, 1978. Comparative morphology of the Mauthner cell in fish and amphibians. In: D.S.Faber,, H.Korn, ed. Neurobiology of the Mauthner Cell. New York: Raven Press, 13–45.
89. S.J.Zottoli,, & D.S.Faber, (2000). The Mauthner cell: what has it taught us? The Neuroscientist, 6, 26–38.
90. S.J.Zottoli,, A.R.Hordes,, & D.S.Faber, (1987). Localization of optic tectal input to the ventral dendrite of the goldfish Mauthner cell. Brain Research, 401, 113–121.