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PLOS ONE  2013 

Functional Implications of Ubiquitous Semicircular Canal Non-Orthogonality in Mammals

DOI: 10.1371/journal.pone.0079585

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Abstract:

The ‘canonical model’ of semicircular canal orientation in mammals assumes that 1) the three ipsilateral canals of an inner ear exist in orthogonal planes (i.e., orthogonality), 2) corresponding left and right canal pairs have equivalent angles (i.e., angle symmetry), and 3) contralateral synergistic canals occupy parallel planes (i.e., coplanarity). However, descriptions of vestibular anatomy that quantify semicircular canal orientation in single species often diverge substantially from this model. Data for primates further suggest that semicircular canal orthogonality varies predictably with the angular head velocities encountered in locomotion. These observations raise the possibility that orthogonality, symmetry, and coplanarity are misleading descriptors of semicircular canal orientation in mammals, and that deviations from these norms could have significant functional consequences. Here we critically assess the canonical model of semicircular canal orientation using high-resolution X-ray computed tomography scans of 39 mammal species. We find that substantial deviations from orthogonality, angle symmetry, and coplanarity are the rule for the mammals in our comparative sample. Furthermore, the degree to which the semicircular canals of a given species deviate from orthogonality is negatively correlated with estimated vestibular sensitivity. We conclude that the available comparative morphometric data do not support the canonical model and that its overemphasis as a heuristic generalization obscures a large amount of functionally relevant variation in semicircular canal orientation between species.

References

[1]  Hullar TE (2006) Semicircular canal geometry, afferent sensitivity, and animal behavior. Anatomical Record Part A 288A: 466–472.
[2]  Graf W (1988) Motion detection in physical space and its peripheral and central representation. Annals of the New York Academy of Sciences 545: 154–169.
[3]  Agur AM (1999) Grant's Atlas of Anatomy. Baltimore, MD: Lippincott, Williams and Wilkins. 760 p.
[4]  Gray H (1918) Anatomy of the Human Body. Philadelphia, PA: Lea & Febiger. 1396 p.
[5]  Gulya AJ (2007) Gulya and Schuknecht's Anatomy of the Temporal Bone with Surgical Implications. New York, NY: Informa Healthcare. 356 p.
[6]  Clarke AH (2005) On the vestibular labyrinth of Brachiosaurus brancai. Journal of Vestibular Research 15: 65–71.
[7]  Kaas J (2009) Evolutionary Neuroscience. Oxford, UK: Academic Press. 1038 p.
[8]  Marugán-Lobón J, Chiappe LM, Farke AA (2013) The variability of inner ear orientation in saurischian dinosaur: testing the use of semicircular canals as a reference system for comparative anatomy. PeerJ 1: 16.
[9]  Romer AS, Parsons TS (1986) The Vertebrate Body. Saunders: Philadelphia. 679 p.
[10]  Spoor F, Zonneveld F (1995) Morphometry of the primate bony labyrinth: a new method based on high-resolution computed tomography. Journal of Anatomy 186: 271–286.
[11]  Oman CM, Marcus EN, Curthoys IS (1987) The influence of semicircular canal morphology on endolymph flow dynamics. Acta Otolaryngolica 103: 1–13.
[12]  Spoor F (2003) The semicircular canal system and locomotor behaviour, with special reference to hominin evolution. Courier Forschungsinstitut Senckenberg 243: 93–104.
[13]  Haines DE (2012) Fundamental Neuroscience for Basic and Clinical Applications. Philadelphia: Elsevier. 492 p.
[14]  Lessard C (2009) Basic Feedback Controls in Biomedicine; Enderle JD, editor. Connecticut: Morgan and Claypool Publishers. 209 p.
[15]  Highsteen SM, Rabbitt RD, Holstein GR, Boyle RD (2005) Determinants of spatial and temporal coding by semicircular canal afferents. Journal of Neurophysiology 93: 2359–2370.
[16]  Rabbitt RD, Damiano ER, Grant JW (2004) Biomechanics of the vestibular semicircular canals and otolith organs. In: Highstein SM, Popper A, Fay R, editors. The Vestibular System. Berlin, Germany: Springer-Verlag. pp. 153–201.
[17]  Blanks RHI, Curthoys IS, Markham CH (1975) Planar relationships of the semicircular canals in man. Acta Otolaryngolica 80: 185–196.
[18]  Curthoys IS, Curthoys EJ, Blanks RHI, Markham CH (1975) The orientation of the semicircular canals in the guinea pig. Acta Otolaryngolica 80: 197–205.
[19]  Ezure K, 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.
[20]  Mazza D, Winterson BJ (1984) Semicircular canal orientation in the adult resting rabbit. Acta Otolaryngolica 98: 472–480.
[21]  Blanks RHI, Torigoe Y (1989) Orientation of the semicircular canals in the rat. Brain Research 487: 278–287.
[22]  Calabrese DR, Hullar TE (2006) Planar relationships of the semicircular canals in two strains of mice. Journal of the Association for Research in Otolaryngology 7: 151–159.
[23]  Ekdale EG (2009) Variation within the bony labyrinth of mammals [PhD Dissertation]. Austin: The University of Texas. 439 p.
[24]  Ifediba MA, Rajguru SM, Hullar TE, Rabbitt RD (2007) The role of 3-canal biomechanics in angular motion transduction by the human vestibular labyrinth. Annals of Biomedical Engineering 35: 1247–1263.
[25]  Yang A, Hullar TE (2007) Relationship of semicircular canal size to vestibular-nerve afferent sensitivity in mammals. Journal of Neurophysiology 98: 3197–3205.
[26]  Rabbitt RD (1999) Directional coding of three-dimensional movements by the vestibular semicircular canals. Biological Cybernetics 80: 417–431.
[27]  Jones GM, Spells KE (1963) A theoretical and comparative study of the functional dependence of the semicircular canal upon its physical dimensions. Proceedings of the Royal Society 157: 403–419.
[28]  Silcox MT, Bloch JI, Boyer DM, Godinot M, Ryan TM, et al. (2009) Semicircular canal system in early primates. Journal of Human Evolution 56: 315–327.
[29]  Spoor F, Garland T, Krovitz G, Ryan TM, Silcox MT, et al. (2007) The primate semicircular canal system and locomotion. Proceedings of the National Academy of Science of the United States of America 104: 10808–10812.
[30]  ten Kate JH, van Barneveld HH, Kuiper JW (1970) The dimensions and sensitivities of semicircular canals. Journal of Experimental Biology 53: 501–514.
[31]  Spoor F, Wood BA, Zonneveld F (1994) Implications of early hominid labyrinthine morphology for evolution of human bipedal locomotion. Nature 369: 645–648.
[32]  Rodgers J (2011) Comparative morphology of the metatherian and eutherian bony labyrinth. Austin: University of Texas at Austin. 400 p.
[33]  Malinzak MD (2010) Experimental analyses of the relationship between semicircular canal morphology and locomotor head rotations in primates [Dissertation]. Durham, North Carolina: Duke University. 236 p.
[34]  Malinzak M, Kay RF, Hullar TE (2011) Semicircular canal orthogonality, not radius, best predicts mean speed of locomotor head rotation: a new hypothesis with implications for reconstructing behaviors in extinct species. American Journal of Physical Anthropology 144: 204.
[35]  Malinzak MD, Kay RF, Hullar TE (2012) Locomotor head movements and semicircular canal morphology in primates. Proceedings of the National Academy of Science 109: 17914–17919.
[36]  Rowe T, Kappelman J, Carlson WD, Ketcham RA, Denison C (1997) High-Resolution Computed Tomography: a breakthrough technology for Earth scientists. Geotimes 42: 23–27.
[37]  Carlson WD, Rowe T, Ketcham RA, Colbert MW (2003) Geological applications of high-resolution X-ray computed tomography in petrology, meteoritics and paleontology. In: Mees F, Swennen R, Van Geet M, Jacobs P, editors. Applications of X-ray computed tomography in the geosciences. London: Geological Society. pp. 7–22.
[38]  Romer AS (1962) The Vertebrate Body. Philadelphia, Pennsylvania: W. B. Saunders Company. 627 p.
[39]  David R, Droulez J, Allain R, Berthoz A, Janvier P, et al. (2010) Motion from the past. A new method to infer vestibular capacities of extinct species. Comptes Rendus Palevol 9: 397–410.
[40]  Venes D, editor (2005) Taber's Cyclopedic Medical Dictionary, 20th Edition. 20 ed. Philadelphia, Pennsylvania: F. A. Davis Company. 2788 p.
[41]  Cox PG, Jeffery N (2008) Geometry of the semicircular canals and extraocular muscles in rodents, lagomorphs, felids, and modern humans. Journal of Anatomy 213: 583–596.
[42]  Spoor F, Zonneveld F (1998) Comparative review of the human bony labyrinth. Yearbook of Physical Anthropology 41: 211–251.
[43]  Fisher NI (1995) Statistical analysis of circular data. Melbourne, Australia: University of Cambridge. 277 p.
[44]  Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290.
[45]  R-Development-Core-Team (2011) R: A language and environment for statistical computing. Vienna, Austria.
[46]  Pinheiro J, Bates D, DebRoy S, Sarkar D, Team RDC (2011) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3: 1–101.
[47]  Freckelton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. American Naturalist 160: 712–726.
[48]  Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, et al. (2007) The delayed rise of present-day mammals. Nature 446: 507–512.
[49]  Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, et al. (2008) Corrigendum. The delayed rise of present-day mammals. Nature 256: 274.
[50]  Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401: 877–844.
[51]  Ryan TM, Silcox MT, Walker A, Mao X, Begun DR, et al. (2012) Evolution of locomotion in Anthropoidea: the semicircular canal evidence. Proceedings of the Royal Society B 279: 3467–3475.
[52]  Sereno PC, Wilson JA, Witmer LM, Whitlock JA, Maga A, et al. (2007) Structural extremes in a Cretaceous dinosaur. PLoS ONE 11: 1–9.
[53]  Witmer LM, Chatterjee S, Franzosa J, Rowe T (2003) Neuroanatomy of flying reptiles and implications for flight, posture and behaviour. Nature 425: 950–953.
[54]  Davies KTJ, Bates PJJ, Maryanto I, Cotton JA, Rossiter SJ (2013) The evolution of bat vestibular systems in the face of potential antagonistic selection pressures for flight and echolocation. PLoS One 8: e61998.
[55]  Billet G, Hautier L, Asher RJ, Schwarz C, Crumpton N, et al. (2012) High morphological variation of vestibular system accompanies slow and infrequent locomotion in three-toed sloths. Proceedings of the Royal Society B 279: 2932–2939.

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