The relationship of head movements to semicircular canal size in cetaceans

Journal of Experimental Biology

Volumn 213, Issue 7, 2010, Pages 1175-1181

  Kandel, Benjamin M ^a   Hullar, Timothy E ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Artiodactyl; Cetacean; Evolution; Head movement; Semicircular canal; Vestibular

Indexed keywords

ANIMAL; ARTICLE; CATTLE; CETACEA; HEAD MOVEMENT; HISTOLOGY; ORGAN SIZE; PHYSIOLOGY; ROTATION; SEMICIRCULAR CANAL; VESTIBULE; VIDEORECORDING;

ANIMALS; CATTLE; CETACEA; HEAD MOVEMENTS; ORGAN SIZE; ROTATION; SEMICIRCULAR CANALS; VESTIBULE, LABYRINTH; VIDEO RECORDING;

ANIMALIA; ARTIODACTYLA; BOS; BOS TAURUS; CETACEA; PHOCOENIDAE; TURSIOPS; TURSIOPS TRUNCATUS; VERTEBRATA;

EID: 77951483211     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.040105     Document Type: Article

References (71)

1. Angelaki, D. E. and Cullen, K. E. (2008). Vestibular system: The many facets of a multimodal sense. Annu. Rev. Neurosci. 31, 125-150.
2. Angelaki, D. E., Shaikh, A. G., Green, A. M. and Dickman, J. D. (2004). Neurons compute internal models of the physical laws of motion. Nature 430, 560-564.
3. Armand, M. and Minor, L. B. (2001). Relationship between time- and frequencydomain analyses of angular head movements in the squirrel monkey. J. Comput. Neurosci. 11, 217-239.
4. Au, W. W. (1993). The Sonar of Dolphins. New York: Springer-Verlag.
5. Baird, R. A., Desmadryl, G., Fernandez, C. and Goldberg, J. M. (1988). The vestibular nerve of the chinchilla. II. Relation between afferent response properties and peripheral innervation patterns in the semicircular canals. J. Neurophysiol. 60, 182-203.
6. Blanks, R. H. I., Curthoys, I. S. and Markham, C. H. (1975). Planar relationships of the semicircular canals in man. Acta Otolaryngol. (Stockh.). 80, 185-196.
7. Blanks, R. H. I., Curthoys, I. S., Bennett, M. L. and Markham, C. H. (1985). Planar relationships of the semicircular canals in rhesus and squirrel monkeys. Brain Res. 340, 315-324.
8. Boenninghaus, G. (1903). Das Ohr des Zahnwales, zugleich ein Beitrag zur Theorie der Schalleitung. Zool. Jahr. (Anatomie) 17, 189-360.
9. Butterworth, A., Kestin, S. C. and McBain, J. F. (2004). Evaluation of baseline indices of sensibility in captive cetaceans. Vet. Rec. 155, 513-518.
10. Calabrese, D. R. and Hullar, T. E. (2006). MicroCT analysis of the dolphin vestibular labyrinth. Assoc. Res. Otolaryngol. Abs. 29, 447.
11. Curthoys, I. S., Curthoys, E. J., Blanks, R. H. and Markham, C. H. (1975). The orientation of the semicircular canals in the guinea pig. Acta Otolaryngol. (Stockh.). 80, 197-205.
12. Day, B. L. and Fitzpatrick, R. C. (2005). The vestibular system. Curr. Biol. 15, R583-R586.
13. Domenici, P. (2001). The scaling of locomotor performance in predator-prey encounters: from fish to killer whales. Comp. Biochem. Physiol. 131 A, 169-182.
14. Ezure, K. and Graf, W. (1984). A quantitative analysis of the spatial organization of the vestibulo-ocular reflexes in lateral- and frontal-eyed animals. I. Orientation of semicircular canals and extraocular muscles. Neuroscience 12, 85-93.
15. Fernandez, C. and Goldberg, J. M. (1971). Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. J. Neurophysiol. 34, 661-675.
16. Fetter, M. (2007). Vestibulo-ocular reflex. Dev. Ophthalmol. 40, 35-51.
17. Fish, F. (1998). Comparative kinematics and hydrodynamics of odontocete cetaceans: morphological and ecological correlates with swimming performance. J. Exp. Biol. 201, 2867-2877.
18. Fish, F. E. (2002). Balancing requirements for stability and maneuverability in cetaceans, Integr. Comp. Biol. 42, 85-93.
19. Fish, F. E., Peacock, J. E. and Rohr, J. J. (2003). Stabilization mechanism in swimming odontocete cetaceans by phased movements. Mar. Mamm. Sci. 19, 515-528.
20. Fish, F., Nicastro, A. and Weih, D. (2006). Dynamics of the aerial maneuvers of spinner dolphins. J. Exp. Biol. 209, 590-598.
21. Fitzpatrick, R. C., Butler, J. E. and Day, B. L. (2006). Resolving head rotation for human bipedalism. Curr. Biol. 16, 1509-1514.
22. Friedmann, G. (1970). The judgement of the visual vertical and horizontal with peripheral and central vestibular lesions. Brain 93, 313-328.
23. Gao, G. and Zhou, K. (1995). Fiber analysis of the vestibular nerve of small cetaceans. In Sensory Systems of Aquatic Mammals (ed. R. A. Kastelein, J. A. Thomas and P. E. Nachtigall), pp. 447-453. Woerden, Netherlands: De Spil.
24. Gingerich, P., Raza, S., Arif, M., Anwar, M. and Zhou, X. (1994). New whale from the Eocene of Pakistan and the origin of cetacean swimming. Nature 368, 844-847.
25. Gingerich, P., Haq, M., Zalmout, I., Khan, I. and Malkani, M. (2001). Origin of whales from early artiodactyls: hands and feet of Eocene Protocetidae from Pakistan. Science 293, 2239-2242.
26. Gingerich, P. D., UI-Haq, M., von Koenigswald, W., Sanders, W. J., Smith, B. H. and Zalmout, I. S. (2009). New protocetid whale from the middle Eocene of Pakistan: birth on land, precocial development, and sexual dimorphism. PLoS One 4, e4366.
27. Glasauer, S., Amorim, M. A., Viaud-Delmon, I. and Berthoz, A. (2002). Differential effects of labyrinthine dysfunction on distance and direction during blindfolded walking of a triangular path. Exp. Brain Res. 145, 489-497.
28. Gray, A. A. (1907-1908). The Labyrinth of Animals. London: Churchill.
29. Harris, C. M. (1998). The Fourier analysis of biological transients. J. Neurosci. Methods 83, 15-34.
30. Harris, C. M., Wallman, J. and Scudder, C. A. (1990). Fourier analysis of saccades in monkeys and humans. J. Neurophysiol. 63, 877-886.
31. Highstein, S. M. (1992). The efferent control of the organs of balance and equilibrium in the toadfish, Opsanus tau. Ann. NY Acad. Sci. 656, 108-123.
32. Holly, J. E. (2004). Vestibular coriolis effect differences modeled with threedimensional linear-angular interactions. J. Vest. Res. 14, 443-460.
33. Howland, H. (1971). The role of the semicircular canals in the angular orientation of fish. Ann. NY Acad. Sci. 188, 202-216.
34. Hullar, T. (2008). Neurometric and psychometric thresholds of the semicircular canals Soc. Neurosci. Abs. 168, 8.
35. Hullar, T. E. and Williams, C. D. (2006). Geometry of the semicircular canals of the chinchilla (Chinchilla laniger). Hear. Res. 213, 17-24.
36. Hullar, T. E., Della Santina, C. C., Hirvonen, T. P., Lasker, D. M., Carey, J. P. and Minor, L. B. (2005). Responses of irregularly discharging chinchilla semicircular canal vestibular-nerve afferents during high-frequency head rotations. J. Neurophysiol. 93, 2777-2786.
37. Hunter, J. (1787). Observations on the structure and oeconomy of whales. Phil. Trans. Roy. Soc. Lond. 77, 371-450.
38. Hyrtl, J. (1845). Vergleichend-anatomische Untersuchungen über das innere Gehörorgan des Menschen und der Säugethiere. Prag: Friedrich Ehrlich.
39. Jones, G. M. and Spells, K. E. (1963). A theoretical and comparative study of the functional dependence of the semicircular canal upon its physical dimensions. Proc. R. Soc. Lond. B. Biol. Sci 157, 403-419.
40. Ketten, D. R. (2000). Cetacean ears. In Hearing by Whales and Dolphins (ed. W. W. L Au, P. Popper and R. R. Fay), pp. 43-108. Heidelberg: Springer.
41. King, D. (1997). A biomechanicai analysis of the Axel: critical parameters for successful jumps. Professional Skater, 10-12.
42. Lackner, J. R. and DiZio, P. A. (2000). Aspects of body self-calibration. Trends Cogn. Sci 4, 279-288.
43. Lang, T. and Norris, K. (1966). Swimming speed of a Pacific bottlenose porpoise. Science 151, 588-590.
44. Lighthill, J. (1971). Elongated-body theory of fish locomotion. Proc. R. Soc. Lond. B. Biol. Sci 179, 125-138.
45. Long, J. J., Pabst, D., Shepherd, W. and McLellan, W. (1997). Locomotor design of dolphin vertebral columns: Bending mechanics and morphology of Delphinus delphis. J. Exp. Biol. 200, 65-81.
46. Maresh, J. L., Fish, F. E., Nowacek, D. P., Nowacek, S. M. and Wells, R. S. (2004). High performance turning capabilities during foraging by bottlenose dolphins (Tursiops truncatus). Mar. Mamm. Sci. 20, 498-509.
47. Montgelard, C., Catzeflis, F. M. and Douzery, E. (1997). Phylogenetic relationships of artiodactyls and cetaceans as deduced from the comparison of cytochrome b and 12S rRNA mitochondrial sequences. Mol. Biol. Evol. 14, 550-559.
48. Muller, M. (1999). Size limitations in semicircular duct systems. J. Theor. Biol. 198, 405-437.
49. Rabbitt, R. D. (1999). Directional coding of three-dimensional movements by the vestibular semicircular canals. Biol Cybern. 80, 417-431.
50. Ridgway, S. H. and Carder, D. A. (1990). Tactile sensitivity, somatosensory responses, skin vibrations, and the skin surface ridges of the bottlenose dolphin, Tursiops truncatus. In Sensory Abilities of Cetaceans (ed. J. A. Thomas and R. A. Kastelein), pp. 163-179. New York: Plenum Press.
51. Rogers, S. (1998). Exploring dinosaur neuropaleobiology: Computed tomography scanning and analysis of an Allosaurus fragilis endocast. Neuron 21, 673-679.
52. Sadeghi, S. G., Chacron, M. J., Taylor, M. C. and Cullen, K. E. (2007a). Neural variability, detection thresholds, and information transmission in the vestibular system. J. Neurosci. 27, 771-781.
53. Sadeghi, S. G., Minor, L. B. and Cullen, K. E. (2007b). Response of vestibular-nerve afferents to active and passive rotations under normal conditions and after unilateral labyrinthectomy. J. Neurophysiol. 97, 1503-1514.
54. Sadeghi, S. G., Goldberg, J. M., Minor, L. B. and Cullen, K. E. (2009). Efferentmediated responses in vestibular nerve afferents of the alert macaque. J. Neurophysiol. 101, 988-1001.
55. Sahlstrand, T. and Petruson, B. (1979). A study of labyrinthine function in patients with adolescent idiopathic scoliosis. I. An electro-nystagmographic study. Acta Orthop. Scand. 50, 759-769.
56. Silva, M. and Downing, J. A. (1995). CRC Handbook of Mammalian Body Masses. Boca Raton, FL: CRC Press.
57. Skrovan, R. C., Williams, T. M., Berry, P. S., Moore, P. W. and Davis, R. W. (1999). The diving physiology of bottlenose dolphins (Tursiops truncatus). II. Biomechanics and changes in buoyancy at depth. J. Exp. Biol. 202, 2749-2761.
58. Smith, P. F. and Curthoys, I. S. (1988a). Neuronal activity in the contralateral medial vestibular nucleus of the guinea pig following unilateral labyrinthectomy. Brain Res. 444, 295-307.
59. Smith, P. F. and Curthoys, I. S. (1988b). Neuronal activity in the ipsilateral medial vestibular nucleus of the guinea pig following unilateral labyrinthectomy. Brain Res. 444, 308-319.
60. Spoor, F. and Thewissen, J. G. M. (2008). Comparative and functional anatomy of balance in aquatic mammals. In Sensory Evolution on the Threshold: Adaptations in Secondarily Aquatic Vertebrates (ed. J. G. M. Thewissen and S. Nummela), pp. 257-284. Berkeley: University of California Press.
61. Spoor, F., Bajpai, S., Hussain, S. T., Kumar, K. and Thewissen, J. G. (2002). Vestibular evidence for the evolution of aquatic behaviour in early cetaceans. Nature 417, 163-166.
62. Spoor, F., Garland, T., Jr, Krovitz, G., Ryan, T. M., Silcox, M. T. and Walker, A. (2007). The primate semicircular canal system and locomotion. Proc. Natl. Acad. Sci. USA 104, 10808-10812.
63. Steinhausen, W. (1931). Über den Nachweis der Bewegung der Cupula in der intakten Bogengansampulle des Labyrinthes bei der natürlichen rotatorischen und calorischen Reizung. Arch. Ges. Physio. 228, 322-328.
64. Straka, H., Vibert, N., Vidal, P. P., Moore, L. E. and Dutia, M. B. (2005). Intrinsic membrane properties of vertebrate vestibular neurons: function, development and plasticity. Prog. Neurobiol. 76, 349-392.
65. Watt, H. (1924). Dimensions of the labyrinth correlated. Proc. R. Soc. Lond. B. Biol. Sci. 96, 334-338.
66. Weihs, D. (1972). A hydrodynamical analysis of fish turning manoeuvres. Proc. R. Soc. Lond. B. Biol. Sci 182, 59-72.
67. Weihs, D. (2002). Stability versus maneuverability in aquatic locomotion, Integr. Comp. Biol 42, 127-134.
68. Welker, K. L., Orkin, J. D. and Ryan, T. M. (2009). Analysis of intraindividual and intraspecific variation in semicircular canal dimensions using high-resolution x-ray computed tomography. J. Anat. 215, 444-451.
69. Yang, A. and Hullar, T. E. (2007). The relationship of semicircular canal size to vestibular-nerve afferent sensitivity in mammals. J. Neurophysiol. 98, 3197-3205.
70. Yates, B. J. and Bronstein, A. M. (2005). The effects of vestibular system lesions on autonomic regulation: observations, mechanisms, and clinical implications. J. Vestib. Res. 15, 119-129.
71. Youm, Y., McMurthy, R. Y., Flatt, A. E. and Gillespie, T. E. (1978). Kinematics of the wrist. I. An experimental study of radial-ulnar deviation and flexion-extension. J. Bone Joint Surg. Am. 60, 423-431.