Alternative forms of axial startle behaviors in fishes

Zoology

Volumn 117, Issue 1, 2014, Pages 36-47

  Liu, Yen Chyi ^a   Hale, Melina E ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Axial movement; Motor control; Neural circuit; Startle response; Swimming

Indexed keywords

ANIMALIA; PETROMYZONTIDAE; PISCES; VERTEBRATA;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; AXIAL MOVEMENT; BIOMECHANICS; CLASSIFICATION; EVOLUTION; FISH; MOTOR CONTROL; NERVOUS SYSTEM FUNCTION; NEURAL CIRCUIT; PHYSIOLOGY; STARTLE REFLEX; SWIMMING;

AXIAL MOVEMENT; MOTOR CONTROL; NEURAL CIRCUIT; STARTLE RESPONSE; SWIMMING;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION; BIOMECHANICAL PHENOMENA; FISHES; NERVOUS SYSTEM PHYSIOLOGICAL PHENOMENA; SWIMMING;

EID: 84893741070     PISSN: 09442006     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.zool.2013.10.008     Document Type: Article

References (126)

1. Azizi E., Landberg T. Effects of metamorphosis on the aquatic escape response of the two-lined salamander (Eurycea bislineata). J. Exp. Biol. 2002, 205:841-849.
2. Barry M.A., Bennett M.V. Projections of giant fibers, a class of reticular interneurons, in the brain of the silver hatchetfish. Brain Behav. Evol. 1990, 36:391-400.
3. Batty R.S., Blaxter J.H.S. The effect of temperature on the burst swimming performance of fish larvae. J. Exp. Biol. 1992, 170:187-201.
4. Bhatt D.H., McLean D.L., Hale M.E., Fetcho J.R. Grading movement strength by change in firing intensity versus recruitment of spinal interneurons. Neuron 2007, 53:91-102.
5. Bierman H.S., Schriefer J.E., Zottoli S.J., Hale M.E. The effects of head and tail stimulation on the withdrawal startle response of the rope fish (Erpetoichthys calabaricus). J. Exp. Biol. 2004, 207:3985-3997.
6. Bierman H.S., Zottoli S.J., Hale M.E. Evolution of the Mauthner axon cap. Brain Behav. Evol. 2009, 73:174-187.
7. Bohorquez-Herrera J., Kawano S.M., Domenici P. Foraging behavior delays mechanically-stimulated escape responses in fish. Integr. Comp. Biol. 2013, 53:780-786.
8. Borazjani I. The functional role of caudal and anal/dorsal fins during the C-start of a bluegill sunfish. J. Exp. Biol. 2013, 216:1658-1669.
9. Brainerd E.L., Patek S.N. Vertebral column morphology, C-start curvature, and the evolution of mechanical defenses in tetraodontiform fishes. Copeia 1998, 1998:971-984.
10. Buchanan J.T. Identification of interneurons with contralateral, caudal axons in the lamprey spinal cord: synaptic interactions and morphology. J. Neurophysiol. 1982, 47:961-975.
11. Buchanan J.T. Contributions of identifiable neurons and neuron classes to lamprey vertebrate neurobiology. Prog. Neurobiol. 2001, 63:441-466.
12. Buchanan J.T. Spinal locomotor inputs to individually identified reticulospinal neurons in the lamprey. J. Neurophysiol. 2011, 106:2346-2357.
13. Buchanan J.T., Cohen A.H. Activities of identified interneurons, motoneurons, and muscle fibers during fictive swimming in the lamprey and effects of reticulospinal and dorsal cell stimulation. J. Neurophysiol. 1982, 47:948-960.
14. Budick S.A., O'Malley D.M. Locomotor repertoire of the larval zebrafish swimming, turning and prey capture. J. Exp. Biol. 2000, 203:2565-2579.
15. Burgess H.A., Granato M. Sensorimotor gating in larval zebrafish. J. Neurosci. 2007, 27:4984-4994.
16. Canfield J.G., Rose G.J. Activation of Mauthner neurons during prey capture. J. Comp. Physiol. A 1993, 172:611-618.
17. Chadwell B.A., Standen E.M., Lauder G.V., Ashley-Ross M.A. Median fin function during the escape response of bluegill sunfish (Lepomis macrochirus). I: fin-ray orientation and movement. J. Exp. Biol. 2012, 215:2869-2880.
18. Chadwell B.A., Standen E.M., Lauder G.V., Ashley-Ross M.A. Median fin function during the escape response of bluegill sunfish (Lepomis macrochirus). II: fin-ray curvature. J. Exp. Biol. 2012, 215:2881-2890.
19. Cochran S.L., Hackett J.T., Brown D.L. The anuran Mauthner cell and its synaptic bed. Neuroscience 1980, 5:1629-1646.
20. Currie S.N. Vibration-evoked startle behavior in larval lampreys. Brain Behav. Evol. 1991, 37:260-271.
21. Currie S., Carlsen R.C. A rapid startle response in larval lampreys. Brain Res. 1985, 358:367-371.
22. Currie S.N., Carlsen R.C. Functional significance and neural basis of larval lamprey startle behavior. J. Exp. Biol. 1987, 133:121-135.
23. Currie S.N., Carlsen R.C. Cranial components of startle behavior in larval and adult lampreys. Neuroscience 1988, 24:709-718.
24. Deliagina T.G., Zelenin P.V., Fagerstedt P., Grillner S., Orlovsky G.N. Activity of reticulospinal neurons during locomotion in the freely behaving lamprey. J. Neurophysiol. 2000, 83:853-863.
25. Di Prisco G.V., Pearlstein E., Le Ray D., Robitaille R., Dubuc R. A cellular mechanism for the transformation of a sensory input into a motor command. J. Neurosci. 2000, 20:8169-8176.
26. Diamond J. The Mauthner cell. Fish Physiology 1971, vol. V:265-346. Academic Press, New York.
27. Domenici P., Blake R. The kinematics and performance of the escape response in the angelfish (Pterophyllum eimekei). J. Exp. Biol. 1991, 156:187-205.
28. Domenici P., Blake R. The kinematics and performance of fish fast-start swimming. J. Exp. Biol. 1997, 200:1165-1178.
29. Domenici P., Standen E.M., Levine R.P. Escape manoeuvres in the spiny dogfish (Squalus acanthias). J. Exp. Biol. 2004, 207:2339-2349.
30. Eaton R.C., Bombardieri R.A., Meyer D.L. Mauthner-initiated startle response in teleost fish. J. Exp. Biol. 1977, 66:65-81.
31. Eaton R.C., Lavender W.A., Wieland C.M. Identification of Mauthner-initiated response patterns in goldfish - evidence from simultaneous cinematography and electrophysiology. J. Comp. Physiol. 1981, 144:521-531.
32. Eaton R.C., Lavender W.A., Wieland C.M. Alternative neural pathways initiate fast-start responses following lesions of the Mauthner neuron in goldfish. J. Comp. Physiol. 1982, 145:485-496.
33. Eaton R.C., Nissanov J., Wieland C.M. Differential activation of Mauthner and non-Mauthner startle circuits in the zebrafish-implications for functional substitution. J. Comp. Physiol. 1984, 155:813-820.
34. Eaton R.C., Hofve J.C., Fetcho J.R. Beating the competition - the reliability hypothesis for Mauthner axon size. Brain Behav. Evol. 1995, 45:183-194.
35. Faber D.S., Korn H. Neurobiology of the Mauthner Cell 1978, Raven Press, New York.
36. Faber D.S., Fetcho J.R., Korn H. Neuronal networks underlying the escape response in goldfish: general implications for motor control. Ann. N. Y. Acad. Sci. 1989, 563:11-33.
37. Faber D.S., Korn H., Lin J.W. Role of medullary networks and postsynaptic membrane properties in regulating Mauthner cell responsiveness to sensory excitation. Brain Behav. Evol. 1991, 37:286-297.
38. Fetcho J.R. Spinal network of the Mauthner cell. Brain Behav. Evol. 1991, 37:298-316.
39. Fetcho J.R. Excitation of motoneurons by the Mauthner axon in goldfish-complexities in a simple reticulospinal pathway. J. Neurophysiol. 1992, 67:1574-1586.
40. Fetcho J.R., Faber D.S. Identification of motoneurons and interneurons in the spinal network for escapes initiated by the Mauthner cell in goldfish. J. Neurosci. 1988, 8:4192-4213.
41. Fitzpatrick B.M., Benard M.F., Fordyce J.A. Morphology and escape performance of tiger salamander larvae (Ambystoma tigrinum mavortium). J. Exp. Zool. A 2003, 297:147-159.
42. Foreman M.B., Eaton R.C. The direction change concept for reticulospinal control of goldfish escape. J. Neurosci. 1993, 13:4101-4113.
43. Fricke H., Hissmann K. Locomotion, fin coordination and body form of the living coelacanth Latimeria chalumnae. Environ. Biol. Fish. 1992, 34:329-356.
44. Frith H., Blake R. Mechanics of the startle response in the northern pike, Esox lucius. Can. J. Zool. 1991, 69:2831-2839.
45. Frith H., Blake R. The mechanical power output and hydromechanical efficiency of northern pike (Esox lucius) fast-starts. J. Exp. Biol. 1995, 198:1863-1873.
46. Furukawa T., Furshpan E.J. Two inhibitory mechanisms in Mauthner neurons of goldfish. J. Neurophysiol. 1963, 26:140-176.
47. Gahtan E., O'Malley E.M. Visually guided injection of identified reticulospinal neurons in zebrafish: a survey of spinal arborization patterns. J. Comp. Neurol. 2003, 459:186-200.
48. Gilat E., Hall D.H., Bennett M.V.L. The giant fiber and pectoral fin adductor motoneuron system in the hatchetfish. Brain Res. 1986, 365:96-104.
49. Grillner S. Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 2006, 52:751-766.
50. Hackett J.T., Faber D.S. Relay neurons mediate collateral inhibition of the goldfish Mauthner cell. Brain Res. 1983, 264:302-306.
51. Hackett J.T., Cochran S.L., Brown D.L. Functional properties of afferents which synapse on the Mauthner neuron in amphibian tadpole. Brain Res. 1979, 176:148.
52. Hale M.E. The development of fast-start performance in fishes: escape kinematics of the chinook salmon (Oncorhynchus tshawytscha). Am. Zool. 1996, 36:695-709.
53. Hale M.E. Locomotor mechanics during early life history: effects of size and ontogeny on fast-start performance of salmonid fishes. J. Exp. Biol. 1999, 202:1465-1479.
54. Hale M.E. S- and C-start escape responses of the muskellunge (Esox masquinongy) require alternative neuromotor mechanisms. J. Exp. Biol. 2002, 205:2005-2016.
55. Hale M.E., Long J.H., McHenry M.J., Westneat M.W. Evolution of behavior and neural control of the fast-start escape response. Evolution 2002, 56:993-1007.
56. Harper D.G., Blake R.W. Fast-start performance of rainbow trout Salmo gairdneri and northern pike Esox lucius. J. Exp. Biol. 1990, 150:321-342.
57. Hatta K., Korn H. Physiological properties of the Mauthner system in the adult zebrafish. J. Comp. Neurol. 1998, 395:493-509.
58. Hoff K.vS., Wassersug R.J. Tadpole locomotion: axial movement and tail functions in a largely vertebraeless vertebrate. Am. Zool. 2000, 40:62-76.
59. Hoke K., Schwartz A., Soares D. Evolution of the fast start response in the cavefish Astyanax mexicanus. Behav. Ecol. Sociobiol. 2012, 66:1157-1164.
60. Jayne B.C., Lauder G.V. Red and white muscle activity and kinematics of the escape response of the bluegill sunfish during swimming. J. Comp. Physiol. A 1993, 173:495-508.
61. Jayne B.C., Lauder G.V. New data on axial locomotion in fishes: how speed affects diversity of kinematics and motor patterns. Am. Zool. 1996, 36:642-655.
62. Johnson T.P., Bennett A.F., McLister J.D. Thermal dependence and acclimation of fast start locomotion and its physiological basis in rainbow trout (Oncorhynchus mykiss). Physiol. Zool. 1996, 69:276-292.
63. Kasapi M.A., Domenici P., Blake R.W., Harper D. The kinematics and performance of escape responses of the knifefish Xenomystus nigri. Can. J. Zool. 1993, 71:189-195.
64. Kasicki S., Grillner S. Müller cells and other reticulospinal neurons are phasically active during fictive locomotion in the isolated nervous system of the lamprey. Neurosci. Lett. 1986, 69:239-243.
65. Kasicki S., Grillner S., Ohta Y., Dubuc R., Brodin L. Phasic modulation of reticulospinal neurons during fictive locomotion and other types of spinal motor activity in lamprey. Brain Res. 1989, 484:203-216.
66. Kimmel C.B., Eaton R.C., Powell S.L. Decreased fast-start performance of zebrafish larvae lacking Mauthner neurons. J. Comp. Physiol. 1980, 140:343-350.
67. Kimura Y., Okamura Y., Higashijima S.I. alx, a zebrafish homolog of chx10, marks ipsilateral descending excitatory interneurons that participate in the regulation of spinal locomotor circuits. J. Neurosci. 2006, 26:5684-5697.
68. Korn H., Faber D.S. An electrically mediated inhibition in goldfish medulla. J. Neurophysiol. 1975, 38:452-471.
69. Korn H., Faber D.S. The Mauthner cell half a century later: a neurobiological model for decision-making?. Neuron 2005, 47:13-28.
70. Koyama M., Kinkhabwala A., Satou C., Higashijima S., Fetcho J. Mapping a sensory-motor network onto a structural and functional ground plan in the hindbrain. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:1170-1175.
71. Liao J.C., Fetcho J.R. Shared versus specialized glycinergic spinal interneurons in axial motor circuits of larval zebrafish. J. Neurosci. 2008, 28:12982-12992.
72. Lippolis G., Joss J.M.P., Rogers L.J. Australian lungfish (Neoceratodus forsteri): a missing link in the evolution of complementary side biases for predator avoidance and prey capture. Brain Behav. Evol. 2009, 73:295-303.
73. Liu K.S., Fetcho J.R. Laser ablations reveal functional relationships of segmental hindbrain neurons in zebrafish. Neuron 1999, 23:325-335.
74. Liu Y.C., Bailey I., Hale M.E. Alternative startle motor patterns and behaviors in the larval zebrafish (Danio rerio). J. Comp. Physiol. A 2012, 198:11-24.
75. Lorent K., Liu K.S., Fetcho J.R., Granato M. The zebrafish space cadet gene controls axonal pathfinding of neurons that modulate fast turning movements. Development 2001, 128:2131-2142.
76. Marras S., Killen S.S., Claireaux G., Domenici P., McKenzie D.J. Behavioural and kinematic components of the fast-start escape response in fish: individual variation and temporal repeatability. J. Exp. Biol. 2011, 214:3102-3110.
77. McClenahan P., Troup M., Scott E.K. Fin-tail coordination during escape and predatory behavior in larval zebrafish. PLoS ONE 2012, 7:e32295.
78. McLean D.L., Fan J., Higashijima S., Hale M.E., Fetcho J.R. A topographic map of recruitment in spinal cord. Nature 2007, 446:71-75.
79. McLean D.L., Masino M.A., Koh I.Y., Lindquist W.B., Fetcho J.R. Continuous shifts in the active set of spinal interneurons during changes in locomotor speed. Nat. Neurosci. 2008, 11:1419-1429.
80. Menelaou E., McLean D.L. A gradient in endogenous rhythmicity and oscillatory drive matches recruitment order in an axial motor pool. J. Neurosci. 2012, 32:10925-10939.
81. Metcalfe W.K., Mendelson B., Kimmel C.B. Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva. J. Comp. Neurol. 1986, 251:147-159.
82. Meyers J.R., Copanas E.H., Zottoli S.J. Comparison of fast startle responses between two elongate bony fish with an anguilliform type of locomotion and the implications for the underlying neuronal basis of escape behavior. Brain Behav. Evol. 1998, 52:7-22.
83. Mirjany M., Preuss T., Faber D.S. Role of the lateral line mechanosensory system in directionality of goldfish auditory evoked escape response. J. Exp. Biol. 2011, 214:3358-3367.
84. Nakajima Y., Kohno K. Fine structure of the Mauthner cell: synaptic topography and comparative study. Neurobiology of the Mauthner Cell 1978, 133-166. Raven Press, New York. D.S. Faber, H. Korn (Eds.).
85. Nakayama H., Oda Y. Common sensory inputs and differential excitability of segmentally homologous reticulospinal neurons in the hindbrain. J. Neurosci. 2004, 24:3199-3209.
86. Nissanov J., Eaton R.C., Didomenico R. The motor output of the Mauthner cell, a reticulospinal command neuron. Brain Res. 1990, 517:88-98.
87. O'Malley D.M., Kao Y.H., Fetcho J.R. Imaging the functional organization of zebrafish hindbrain segments during escape behaviors. Neuron 1996, 17:1145-1155.
88. O'Steen S., Cullum A.J., Bennett A.F. Rapid evolution of escape ability in Trinidadian guppies (Poecilia reticulata). Evolution 2002, 56:776-784.
89. Roberts A., Hill N.A., Hicks R. Simple mechanisms organize orientation of escape swimming in embryos and hatchling tadpoles of Xenopus laevis. J. Exp. Biol. 2000, 203:1869-1885.
90. Rock M.K. Functional properties of Mauthner cell in the tadpole Rana catesbeiana. J. Neurophysiol. 1980, 44:135-150.
91. Rovainen C.M. Physiological and anatomical studies on large neurons of central nervous system of sea lamprey (Petromyzon marinus). I. Müller and Mauthner cells. J. Neurophysiol. 1967, 30:1000-1023.
92. Rovainen C.M. Müller cells, Mauthner cells, and other identified reticulospinal neurons in the lamprey. Neurobiology of the Mauthner Cell 1978, 245-269. Raven Press, New York. D.S. Faber, H. Korn (Eds.).
93. Rovainen C.M. Electrophysiology of vestibulospinal and vestibuloreticulospinal systems in lampreys. J. Neurophysiol. 1979, 42:745-766.
94. Rovainen C.M. Neurobiology of lampreys. Physiol. Rev. 1979, 59:1007-1077.
95. Satou C., Kimura Y., Kohashi T., Horikawa K., Takeda H., Oda Y., Higashijima S. Functional role of a specialized class of spinal commissural inhibitory neurons during fast escapes in zebrafish. J. Neurosci. 2009, 29:6780-6793.
96. Schriefer J.E., Hale M.E. Strikes and startles of northern pike (Esox lucius): a comparison of muscle activity and kinematics between S-start behaviors. J. Exp. Biol. 2004, 207:535-544.
97. Scott J.W., Zottoli S.J., Beatty N.P., Korn H. Origin and function of spiral fibers projecting to the goldfish Mauthner cell. J. Comp. Neurol. 1994, 339:76-90.
98. Sillar K.T., Robertson R.M. Thermal activation of escape swimming in post-hatching Xenopus laevis frog larvae. J. Exp. Biol. 2009, 212:2356-2364.
99. Spierts I.L., Van Leeuwen J.L. Kinematics and muscle dynamics of C- and S-starts of carp (Cyprinus carpio L.). J. Exp. Biol. 1999, 202:393-406.
100. Starosciak A.K., Kalola R.P., Perkins K.P., Riley J.A., Saidel W.M. Fast and singular muscle responses initiate the startle response of Pantodon buchholzi (Osteoglossomorpha). Brain Behav. Evol. 2008, 71:100-114.
101. Svoboda K.R., Fetcho J.R. Interactions between the neural networks for escape and swimming in goldfish. J. Neurosci. 1996, 16:843-852.
102. Swanson B.O., Gibb A.C. Kinematics of aquatic and terrestrial escape responses in mudskippers. J. Exp. Biol. 2004, 207:4037-4044.
103. Turesson H., Satta A., Domenici P. Preparing for escape: anti-predator posture and fast-start performance in guppies. J. Exp. Biol. 2009, 212:2925-2933.
104. Tytell E.D., Lauder G.V. The C-start escape response of Polypterus senegalus: bilateral muscle activity and variation during stage 1 and 2. J. Exp. Biol. 2002, 205:2591-2603.
105. Tytell E.D., Lauder G.V. Hydrodynamics of the escape response in bluegill sunfish, Lepomis macrochirus. J. Exp. Biol. 2008, 211:3359-3369.
106. Van Buskirk J., McCollum S.A. Influence of tail shape on tadpole swimming performance. J. Exp. Biol. 2000, 203:2149-2158.
107. Walker J.A., Ghalambor C.K., Griset O.L., McKenney D., Reznick D.N. Do faster starts increase the probability of evading predators?. Funct. Ecol. 2005, 19:808-815.
108. Ward A.B., Azizi E. Convergent evolution of the head retraction escape response in elongate fishes and amphibians. Zoology 2004, 107:205-217.
109. Webb P.W. Effect of size on fast-start performance of rainbow trout Salmo gairdneri, and a consideration of piscivorous predator-prey interactions. J. Exp. Biol. 1976, 65:157-177.
110. Webb P.W. Effects of median-fin amputation on fast-start performance of rainbow trout (Salmo gairdneri). J. Exp. Biol. 1977, 68:123-135.
111. Webb P.W. Fast-start performance of and body form in seven species of teleost fish. J. Exp. Biol. 1978, 74:211-226.
112. Weihs D. The mechanism of rapid starting of slender fish. Biorheology 1973, 10:343-350.
113. Weiss S.A., Zottoli S.J., Do S.C., Faber D.S., Preuss T. Correlation of C-start behaviors with neural activity recorded from the hindbrain in free-swimming goldfish (Carassius auratus). J. Exp. Biol. 2006, 209:4788-4801.
114. Westneat M.W., Hale M.E., McHenry M.J., Long J.H. Mechanics of the fast-start: muscle function and the role of intramuscular pressure in the escape behavior of Amia calva and Polypterus palmas. J. Exp. Biol. 1998, 201:3041-3055.
115. Wilcox S.C., Lappin A.K. Burst swimming performance predicts the outcome of cannibalistic interactions in green poison frog larvae (Dendrobates auratus). J. Exp. Zool. 2013, 9999:1-10.
116. Will U. Amphibian Mauthner cells. Brain. Behav. Evol. 1991, 37:317-332.
117. Wilson R.S., Franklin C.E. Thermal acclimation of locomotor performance in tadpoles of the frog Limnodynastes peronii. J. Comp. Physiol. B. 1999, 169:445-451.
118. Wilson R.S., Franklin C.E. Effect of ontogenetic increases in body size on burst swimming performance in tadpoles of the striped marsh frog Limnodynastes peronii. Physiol. Biochem. Zool. 2000, 73:142-152.
119. Zelenin P.V., Grillner S., Orlovsky G.N., Deliagina T.G. Heterogeneity of the population of command neurons in the lamprey. J. Neurosci. 2001, 21:7793-7803.
120. Zelenin P.V., Orlovsky G.N., Deliagina T.G. Sensory-motor transformation by individual command neurons. J. Neurosci. 2007, 27:1024-1032.
121. Zottoli S.J. Correlation of the startle reflex and Mauthner cell auditory responses in unrestrained goldfish. J. Exp. Biol. 1977, 66:243-254.
122. Zottoli S.J. Comparative morphology of the Mauthner cell in fish and amphibians. Neurobiology of the Mauthner Cell 1978, 13-45. Raven Press, New York. D.S. Faber, H. Korn (Eds.).
123. Zottoli S.J., Faber D.S. The Mauthner cell: what has it taught us?. Neuroscientist 2000, 6:26-38.
124. Zottoli S.J., Hordes A.R., Faber D.S. Localization of optic tectal input to the ventral dendrite of the goldfish Mauthner cell. Brain Res. 1987, 401:113-121.
125. Zottoli S.J., Newman B.C., Rieff H.I., Winters D.C. Decrease in occurrence of fast startle responses after selective Mauthner cell ablation in goldfish (Carassius auratus). J. Comp. Physiol. A 1999, 184:207-218.
126. Zottoli S.J., Wong T.W., Agostini M.A., Meyers J.R. Axon cap morphology of the sea robin (Prionotus carolinus): Mauthner cell is correlated with the presence of signature field potentials and a C-type startle response. J. Comp. Neurol. 2011, 519:1979-1998.