Semicircular canal geometry, afferent sensitivity, and animal behavior

Anatomical Record - Part A Discoveries in Molecular, Cellular, and Evolutionary Biology

Volumn 288, Issue 4, 2006, Pages 466-472

  Hullar, Timothy E ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Evolution; Labyrinth; Torsion pendulum; Vestibular

Indexed keywords

ANIMAL BEHAVIOR; ARTICLE; CAT; INNER EAR; NONHUMAN; PIGEON; PRIORITY JOURNAL; SEMICIRCULAR CANAL; SPECIES COMPARISON; SQUIRREL MONKEY; VESTIBULAR SYSTEM;

ANIMALS; BEHAVIOR, ANIMAL; CATS; COLUMBIDAE; NEURONS, AFFERENT; SAIMIRI; SEMICIRCULAR CANALS;

ANIMALIA; COLUMBA; SAIMIRI;

EID: 33645746634     PISSN: 0003276X     EISSN: 15524892     Source Type: Journal    
DOI: 10.1002/ar.a.20304     Document Type: Article

References (107)

1. Alonso PD, Milner AC, Ketcham RA, Cookson MJ, Rowe TB. 2004. The avian nature of the brain and inner ear of Archaeopteryx. Nature 430:666-669.
2. Anastasio TJ, Correia MJ, Perachio AA. 1985. Spontaneous and driven responses of semicircular canal primary afferents in the unanesthetized pigeon. J Neurophysiol 54:335-347.
3. Anderson JH, Blanks RHI, Precht W. 1978. Response characteristics of semicircular canal and otolith systems in cat: I, dynamic responses of primary vestibular nerve fibers. Exp Brain Res 32:491-507.
4. Angelaki DE, Perachio AA. 1993. Contribution of irregular semicircular canal afferents to the horizontal vestibuloocular response during constant velocity rotation. J Neurophysiol 69:996-999.
5. Angelaki DE, McHenry MQ, Dickman JD, Perachio AA. 2000. Primate translational vestibuloocular reflexes: III, effects of bilateral labyrinthine electrical stimulation. J Neurophysiol 83:1662-1676.
6. Baird IL. 1974. Some aspects of the comparative anatomy and evolution of the inner ear in submammalian vertebrates. Brain Behav Evol 10:11-36.
7. Baker J, Goldberg J, Peterson B. 1985. Spatial and temporal response properties of the vestibulocollic reflex in decerebrate cats. J Neurophysiol 54:735-756.
8. Balaban CD. 1999. Vestibular autonomic regulation. Curr Opin Neurol 12:29-33.
9. Barnes LG, McLeod SA. 1984. The fossil record and phyletic relationships of gray whales. In: Jones ML, Swartz SL, editors. The gray whale. New York: Academic Press. p 3-28.
10. Bilotto G, Goldberg J, Peterson BW, Wilson VJ. 1982. Dynamic properties of vestibular reflexes in the decerebrate cat. Exp Brain Res 47:343-352.
11. Blanks RHI, Estes MS, Markham CH. 1975. Physiologic characteristics of vestibular first order canal neurons in the cat: II, response to constant angular acceleration. J Neurophysiol 38:1250-1268.
12. Blanks RHI, Precht W. 1976. Functional characterization of primary vestibular afferents in the frog. Exp Brain Res 25:369-390.
13. Blanks RH, Torigoe Y. 1989. Orientation of the semicircular canals in rat. Brain Res 487:278-287.
14. Boenninghaus G. 1903. Das Ohr des Zahnwales, zugleich ein Beitrag zur Theorie der Schalleitung. Zool Jahr (Anat) 17:189-360.
15. Boyle R, Highstein SM. 1990. Resting discharge and response dynamics of horizontal semicircular canal afferents of the toadfish, Opsanus tau. J Neurosci 10:1557-1569.
16. Brichta AM, Acuna DL, Peterson EH. 1988. Planar relations of semicircular canals in awake, resting turtles, Pseudemys scripta. Brain Behav Evol 32:236-245.
17. Brichta AM, Goldberg JM. 2000. Morphological identification of physiologically characterized afferents innervating the turtle posterior crista. J Neurophysiol 83:1202-1223.
18. Chen-Huang C, McCrea RA. 1998. Contribution of vestibular nerve irregular afferents to viewing distance-related changes in the vestibulo-ocular reflex. Exp Brain Res 119:116-130.
19. Clarke AH. 2005. On the vestibular labyrinth of Brachiosaurus brancai. J Vestib Res 15:65-71.
20. Correia MJ, Landolt JP. 1973. Spontaneous and driven responses from primary neurons of the anterior semicircular canal of the pigeon. Adv Otorhinolaryngol 19:134-148.
21. Curthoys IS, Markham CH, Curthoys EJ. 1977. Semicircular duct and ampulla dimensions in cat, guinea pig and man. J Morphol 151:17-34.
22. Curthoys IS. 1982. Postnatal development changes in the response of rat primary horizontal semicircular canal neurons to sinusoidal angular accelerations. Exp Brain Res 47:295-300.
23. Damiano ER, Rabbitt RD. 1996. A singular perturbation model of fluid dynamics in the vestibular semicircular canal and ampulla. J Fluid Mech 307:333-372.
24. de Beer GR. 1947. How animals hold their heads. Proc Linn Soc Lond 159:125-139.
25. de Burlet HM. 1929. Zur vergleichenden Anatomie und Physiologie des perilymphatischen Raumes. Acta Otolaryngol 13:153-187.
26. DeSmet WMA. 1977. The regions of the cetacean vertebral column. In: Harrison RJ, editor. Functional anatomy of marine mammals. London: Academic Press. p 59-79.
27. Dickman JD, Correia MJ. 1989. Responses of pigeon horizontal semicircular canal afferent fibers: I, step, trapezoid, and low-frequency sinusoid mechanical and rotational stimulation. J Neurophysiol 62:1090-1101.
28. Dickman JD. 1996. Spatial orientation of semicircular canals and afferent sensitivity vectors in pigeons. Exp Brain Res 111:8-20.
29. Erichsen JT, Hodos W, Evinger C, Bessette BB, Phillips SJ. 1989. Head orientation in pigeons: postural, locomotor and visual determinants. Brain Behav Evol 33:268-278.
30. Ezure K, Schor RH, Yoshida K. 1978. The response of horizontal semicircular canal afferents to sinusoidal rotation in the cat. Exp Brain Res 33:27-39.
31. Fernandez C, Goldberg JM. 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.
32. Fernandez C, Goldberg JM. 1976. Physiology of peripheral neurons innervating otolith organs of the squirrel monkey: I, response to static tilts and to long duration centrifugal force. J Neurophysiol 39:970-984.
33. Ghanem T, Rabbitt RD, Tresco PA. 1998. Three-dimensional reconstruction of the membranous vestibular labyrinth in the toadfish, Opsanus tau. Hear Res 124:27-43.
34. Girard L. 1923. Le plan des canau semicirculaires horizontaux considere comme plan horizontal de la tete. Bull Mem Soc Anthrop (Paris) 14:14.
35. Goldberg JM, Fernandez C. 1971. Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey: I, resting discharge and response to constant angular accelerations. J Neurophysiol 34:635-660.
36. Graf W, Baker R. 1985. The vestibuloocular reflex of the adult flatfish: I, oculomotor organization. J Neurophysiol 54:887-899.
37. Graf W, de Waele C, Vidai P-P. 1995a. Functional anatomy of the head-neck movement system of quadrupedal and bipedal mammals. J Anat 186:55-74.
38. Graf W, de Waele C, Vidai P-P, Wang DH, Evinger C. 1995b. The orientation of the cervical vertebral column in unrestrained awake animals: II, movement strategies. Brain Behav Evol 45:209-231.
39. Graf W, Vidal P-P. 1996. Semicircular canal size and upright stance are not interrelated. J Hum Evol 30:175-181.
40. Grant JW, van Buskirk WC. 1976. Experimental measurement of the stiffness of the cupula. Biophys J 16:669-678.
41. Gray O. 1955. A brief survey of the phylogenesis of the labyrinth. J Laryngol Otol 69:151-179.
42. Hadziselimovic H, Savkovic L. 1964. Appearance of semicircular canals in birds in relation to mode of life. Acta Anat (Basel) 57:306-315.
43. Hartmann R, Klinke R. 1980. Discharge properties of afferent fibres of the goldfish semicircular canal with high frequency stimulation. Pflugers Arch 388:111-121.
44. Highstein SM, Goldberg JM, Moschovakis AK, Fernandez C. 1987. Inputs from regularly and irregularly discharging vestibular nerve afferents to secondary neurons in the vestibular nuclei of the squirrel monkey: II, correlation with output pathways of secondary neurons. J Neurophysiol 58:719-738.
45. Highstein SM, Rabbitt RD, Holstein GR, Boyle RD. 2005. Determinants of spatial and temporal coding by semicircular canal afferents. J Neurophysiol 93:2359-2370.
46. Holstein GR, Rabbitt RD, Martinelli GP, Friedrich VL Jr, Boyle RD, Highstein SM. 2004. Convergence of excitatory and inhibitory hair cell transmitters shapes vestibular afferent responses. Proc Natl Acad Sci USA 101:15766-15771.
47. Honrubia V, Sitko S, Kimm J, Betts W, Schwartz I. 1981. Physiological and anatomical characteristics of primary vestibular afferent neurons in the bullfrog. Int J Neurosci 15:197-206.
48. Howland H, Masci J. 1973a. The functional allometry of semicircular canals, fins, and body dimensions in the juvenile centrarchid fish, Lepomis gibbosus (L.). J Embryol Exp Morph 29:721-743.
49. Howland HC, Masci J. 1973b. The phylogenetic allometry of the semicircular canals of small fishes. Z Morphol Tiere 75:283-296.
50. Hullar T, Armand M. 2004. Head motion of freely swimming dolphins. J Vestib Res 14:144-145.
51. Hullar TE, Della Santina CC, Hirvonen TP, Lasker DM, Carey JP, Minor LB. 2005. Responses of irregularly discharging chinchilla semicircular canal vestibular-nerve afferents during high-frequency head rotations. J Neurophysiol 93:2777-2786.
52. Hyrtl J. 1845. Vergleichend-anatomische Untersuchungen über das innere Gehörorgan des Menschen und der Säugethiere. Prague: Friedrich Ehrlich.
53. Jones GM, Spells KE. 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.
54. Keller EL. 1976. Behavior of horizontal semicircular canal afferents in alert monkey during vestibular and optokinetic stimulation. Exp Brain Res 24:459-471.
55. Landolt JP, Correia MJ. 1980. Neurodynamic response analysis of anterior semicircular canal afferents in the pigeon. J Neurophysiol 43:1746-1770.
56. Ledebkin S. 1924. Über die Lage des Canalis semicircularis lateralis bei Säugern. Anat Anz 58:447-460.
57. Ledoux A. 1961. L'adaptation du systéme vestibulaire périphérique. Acta Otolaryngol (Stockh) 53:307-316.
58. Leigh RJ, Zee DS. 1999. The neurology of eye movement, 3rd ed. Oxford: Oxford University Press.
59. Lewis ER, Leverenz EL, Bialek WS. 1985. The vertebrate inner ear. Boca Raton, FL: CRC Press.
60. Lewis ER, Parnas BR. 1994. Theoretical bases of short-latency spike volleys in the peripheral vestibular system. J Vestib Res 4:189-202.
61. Lindenlaub T, Burda H, Nevo E. 1995. Convergent evolution of the vestibular organ in the subterranean mole-rats Cryptomys and Spalax, as compared with the aboveground rat, Rattus. J Morphol 224:303-311.
62. Louie AW, Kimm J. 1976. The response of eighth nerve fibers to horizontal sinusoidal oscillation in the alert monkey. Exp Brain Res 24:447-457.
63. Lowenstein O. 1955. The effect of galvanic polarization on the impulse discharge from sense endings on the isolated labyrinth o fhte thorn back ray (Raja clavata). J Physiol (Lond) 127:104-117.
64. Lysakowski A, Minor LB, Fernandez C, Goldberg JM. 1995. Physiological identification of morphologically distinct afferent classes innervating the cristae ampullares of the squirrel monkey. J Neurophysiol 73:1270-1281.
65. Matano S, Kubo T, Niemitz C, Guenther M. 1985. Semicircular canal organ in three primate species and behavioral correlations. Fortschr Zool 30:677-680.
66. Mayne R. 1950. The dynamic characteristics of the semicircular canals. J Comp Physiol Psychol 43:309-319.
67. Mazza D, Winterson BJ. 1984. Semicircular canal orientation in the adult resting rabbit. Acta Otolaryngol 98:472-480.
68. McVean A. 1999. Are the semicircular canals of the European mole, Talpa europaea, adapted to a subterranean habitat? Comp Biochem Physiol A Mol Integr Physiol 123:173-178.
69. Muller M, Verhagen JHG. 1988a. A mathematical approach enabling the calculation of the total endolymph flow in the semicircular ducts. J Theor Biol 134:503-529.
70. Muller M, Verhagen JHG. 1988b. A new quantitative model of total endolymph flow in the system of semicircular ducts. J Theor Biol 134:473-501.
71. Muller M. 1994. Semicircular duct dimensions and sensitivity of the vertebrate vestibular system. J Theor Biol 167:239-256.
72. O'Leary DP, Dunn RF, Honrubia V. 1974. Functional and anatomical correlation of afferent responses from the isolated semicircular canal. Nature 251:225-227.
73. Oman CM, Marcus EN, Curthoys IS. 1987. The influence of semicircular canal morphology on endolymph flow dynamics. Acta Otolaryngol (Stockh) 103:1-13.
74. Perez F. 1922. Craniologie vestibienne, ethnique et zoologique. Bull Mem Soc Anthrop (Paris) 13:16.
75. Peterka RJ, Tomko DL. 1984. Differences between cats in response properties of horizontal semicircular canal primary afferents. Exp Brain Res 56:162-166.
76. Precht W, Llinas R, Clarke M. 1971. Physiological responses of frog vestibular fibers to horizontal angular rotation. Exp Brain Res 13:378-407.
77. Rabbitt RD. 1999. Directional coding of three-dimensional movements by the vestibular semicircular canals. Biol Cybern 80:417-431.
78. Rabbitt RD, Damiano ER, Grant JW. 2004. Biomechanics of the semicircular canals and otolith organs. In: Highstein S, Fay RR, Popper AN, editors. The vestibular system. New York: Springer. p 153-201.
79. Ramprashad F, Landolt JP, Money KE, Laufer J. 1984. Dimensional analysis and dynamic response characterization of mammalian peripheral vestibular structures. Am J Anat 169:295-313.
80. Ramprashad F, Landolt JP, Money KE, Laufer J. 1986. Comparative morphometric study of the vestibular system of the vertebrata: Reptilia, Aves, Amphibia, and Pisces. Acta Otolaryngol Suppl 427:1-42.
81. Raphan T, Matsuo V, Cohen B. 1979. Velocity storage in the vestibulo-ocular reflex arc (VOR). Exp Brain Res 35:229-248.
82. Raphan T, Cohen B. 2002. The vestibulo-ocular reflex (VOR) in three dimensions. Exp Brain Res 145:1-27.
83. Retzius G. 1881. Des Gehörorgan der Wirbelthiere: morphologisch-histologisch Studien: I, das Gehörorgan der der Fische und Amphibien. Stockholm: Samson and Wallin.
84. Retzius G. 1884. Des Gehörorgan der Wirbelthiere: morphologisch-histologisch Studien: II, das Gehörorgan der Reptilien, der Vögel under der Säugetiere. Stockholm: Samson and Wallin.
85. Rogers SW. 1998. Exploring dinosaur neuropaleobiology: viewpoint computed tomography scanning and analysis of an Allosaurus fragilis endocast. Neuron 21:673-679.
86. Rogers SW. 1999. Allosaurus, crocodiles, and birds: evolutionary clues from spiral computed tomography of an endocast. Anat Rec 257: 162-173.
87. Rogers SW. 2005. Reconstructing the behaviors of extinct species: an excursion into comparative paleoneurology. Am J Med Genet A 134:349-356.
88. Rommel S. 1990. Osteology of the bottlenose dolphin. In: Leather-wood S, Reeves RR, editors. The bottlenose dolphin. San Diego, CA: Academic Press. p 29-49.
89. Soodak RE, Simpson JI. 1988. The accessory optic system of rabbit: I, basic visual response properties. J Neurophysiol 60:2037-2054.
90. Spoor F, Wood B, Zonneveld F. 1994. Implications of early hominid labyrinthine morphology for evolution of human bipedal locomotion. Nature 369:645-648.
91. Spoor F, Wood B, Zonneveld F. 1996. Evidence for a link between human semicircular canal size and bipedal behaviour. J Hum Evol 30:183-187.
92. Spoor F, Zonneveld F. 1998. Comparative review of the human bony labyrinth. Am J Phys Anthropol Suppl 27:211-251.
93. Spoor F, Bajpai S, Hussain ST, Kumar K, Thewissen JG. 2002. Vestibular evidence for the evolution of aquatic behaviour in early cetaceans. Nature 417:163-166.
94. Spoor F, Hublin J, Braun M, Zonneveld F. 2003. The bony labyrinth of Neanderthals. J Hum Evol 44:141-165.
95. Squires TM. 2004. Optimizing the vertebrate vestibular semicircular canal: could we balance any better? Phys Rev Lett 93:198106.
96. Stackman RW, Clark AS, Taube JS. 2002. Hippocampal spatial representations require vestibular input. Hippocampus 12:291-303.
97. Steinhausen W. 1933. Über die Beobachtung der Cupula in den Bogengangsampullen des Labyrinths des lebenden Hechts. Arch Ges Physio 232:500-512.
98. Taube JS. 1998. Head direction cells and the neurophysiological basis for a sense of direction. Prog Neurobiol 55:225-256.
99. ten Kate JH, van Barneveld HH, Kuiper JW. 1970. The dimensions and sensitivities of semicircular canals. J Exp Biol 53:501-514.
100. ten Kate JH. 1973. Angular acceleration detection by the growing pike. Adv Otorhinolaryngol 19:110-119.
101. Turkewitsch BG. 1934. Zur Anatomie des Gehörorgans der Vögel (Canales semicirculares). Z Anat Entwicklungsgesch 103:551-608.
102. van Buskirk WC, Watts RG, Liu YK. 1976. The fluid mechanics of the semicircular canals. J Fluid Mech 78:87-98.
103. Van Egmond AAJ, van Groen JJ, Jongkees LBW. 1949. The mechanics of the semicircular canal. J Physiol (Lond) 110:1-17.
104. Vidal PP, Graf W, Berthoz A. 1986. The orientation of the cervical vertebral column in unrestrained awake animals. I. Resting position. Exp Brain Res 61:549-559.
105. Wersäll J, Bagger-Sjoback D. 1974. Morphology of the vestibular sense organ. In: Kornhuber HH, editor. Vestibular system: I, basic mechanisms. Berlin: Springer. p 123-170.
106. Yablokov AV, Bel'kovish BM, Borisov VI. 1972. Whales and dolphins. Jerusalem: Israel Programs for Scientific Translations.
107. Yamauchi A, Rabbitt RD, Boyle R, Highstein SM. 2002. Relationship between inner-ear fluid pressure and semicircular canal afferent nerve discharge. J Assoc Res Otolaryngol 3:26-44.