The fluid dynamics of canine olfaction: Unique nasal airflow patterns as an explanation of macrosmia

Journal of the Royal Society Interface

Volumn 7, Issue 47, 2010, Pages 933-943

  Craven, Brent A ^a,b   Paterson, Eric G ^a   Settles, Gary S ^b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b The Pennsylvania State University   (United States)

Author keywords

Canine olfaction; Computational fluid dynamics; Macrosmatic; Nasal airway; Olfactory acuity; Sniff

Indexed keywords

COMPUTATIONAL FLUID DYNAMICS; FLUID DYNAMICS; FLUIDS; MAGNETIC RESONANCE IMAGING; MAMMALS; NEURONS; RESONANCE; RESPIRATORY MECHANICS; THREE DIMENSIONAL;

AIRFLOW PATTERNS; ALLOMETRIC SCALING; CANINE OLFACTION; COMPUTATIONAL FLUID DYNAMICS SIMULATIONS; CRITICAL STEPS; EXPERIMENTAL DATA; HIGH RESOLUTION; INSPIRATORY AIRFLOW; NASAL CAVITY; OLFACTORY FUNCTIONS; RECEPTOR GENES; SENSORY NEURONS; SENSORY ORGANS; SOURCE LOCALIZATION; STIMULUS INTENSITY; THREE-DIMENSIONAL MODEL; TIDAL VOLUME;

TRANSPORT PROPERTIES;

ALLOMETRY; ANIMAL EXPERIMENT; ARTICLE; BODY MASS; COMPUTATIONAL FLUID DYNAMICS; CONTROLLED STUDY; DOG; FEMALE; NONHUMAN; NOSE AIRFLOW; NOSE CAVITY; NUCLEAR MAGNETIC RESONANCE IMAGING; ODOR; OLFACTORY DISCRIMINATION; PEAK INSPIRATORY FLOW; SMELLING; SNIFFING; TIDAL VOLUME;

EID: 77953146312     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2009.0490     Document Type: Article

References (65)

1. Bojsen-Møller, F. & Fahrenkrug, J. 1971 Nasal swell-bodies and cyclic changes in the air passage of the rat and rabbit nose. J. Anat. 110, 25-37.
2. Charles River Laboratories 2009 Long-Evans rats. See http://info.criver. com/flex-content-area/documents/rm-rm-c-long-evans-rats.pdf.
3. Craven, B. A. 2008. A fundamental study of the anatomy, aerodynamics, and transport phenomena of canine olfaction. University Park, PA: The Pennsylvania State University.
4. Craven, B. A., Neuberger, T., Paterson, E. G., Webb, A. G., Josephson, E. M., Morrison, E. E. & Settles, G. S. 2007 Reconstruction and morphometric analysis of the nasal airway of the dog (Canis familiaris) and implications regarding olfactory airflow. Anat. Rec. 290, 1325-1340. (doi:10.1002/ar.20592)
5. Craven, B. A., Paterson, E. G. & Settles, G. S. 2009 Development and verification of a high-fidelity computational fluid dynamics model of canine nasal airflow. J. Biomech. Eng. 131, 1-11.
6. Crawford, E. C. 1962 Mechanical aspects of panting in dogs. J. Appl. Physiol. 17, 249-251.
7. Evans, H. E. 1993 Miller's anatomy of the dog, 3rd edn. Philadelphia, PA: Saunders.
8. Finger, T. E., Bottger, B., Hansen, A., Anderson, K. T., Alimohammadi, H. & Silver, W. L. 2003 Solitary chemoreceptor cells in the nasal cavity serve as sentinels of respiration. Proc. Natl Acad. Sci. USA 100, 8981-8986. (doi:10.1073/pnas.1531172100)
9. Glebovskii, V. D. & Marevskaya, A. P. 1968 Participation of muscles of the nostrils in olfactory analysis and respiration in rabbits. Fiziol. Zh. 54, 1278-1286.
10. Gloriam, D. E. I., Bjarnadóttir, T. K., Yan, Y. L., Postlethwait, J. H., Schiöth, H. B. & Fredriksson, R. 2005 The repertoire of trace amine G-protein-coupled receptors: large expansion in zebrafish. Mol. Phylogenet. Evol. 35, 470-482. (doi:10.1016/j.ympev.2004.12.003)
11. Guilmette, R. A., Wicks, J. D. & Wolff, R. K. 1989 Morphometry of human nasal airways in vivo using magnetic resonance imaging. J. Aerosol. Med. 2, 365-377. (doi:10.1089/jam.1989.2.365)
12. Hahn, I., Scherer, P. W. & Mozell, M. M. 1993 Velocity profiles measured for airflow through a large-scale model of the human nasal cavity. J. Appl. Physiol. 75, 2273-2287.
13. Hornung, D. E. 2006 Nasal anatomy and the sense of smell. Adv. Otorhinolaryngol. 63, 1-22.
14. Hornung, D. E., Smith, D. J., Kurtz, D. B., White, T. & Leopold, D. A. 2001 Effect of nasal dilators on nasal structures, sniffing strategies, and olfactory ability. Rhinology 39, 84-87. (Pubitemid 32631619)
15. Kelly, J. T., Prasad, A. K. & Wexler, A. S. 2000 Detailed flow patterns in the nasal cavity. J. Appl. Physiol. 89, 323-337.
16. Kepecs, A., Uchida, N. & Mainen, Z. F. 2007 Rapid and precise control of sniffing during olfactory discrimination in rats. J. Neurophysiol. 98, 205-213. (doi:10.1152/jn.00071.2007) (Pubitemid 47084812)
17. Keyhani, K., Scherer, P. W. & Mozell, M. M. 1995 Numerical simulation of airflow in the human nasal cavity. J. Biomech. Eng. 117, 429-441. (doi:10.1115/1.2794204)
18. Keyhani, K., Scherer, P. W. & Mozell, M. M. 1997 A numerical model of nasal odorant transport for the analysis of human olfaction. J. Theor. Biol. 186, 279-301. (doi:10.1006/jtbi.1996.0347)
19. Kimbell, J. S., Godo, M. N., Gross, E. A., Joyner, D. R., Richardson, R. B. & Morgan, K. T. 1997 Computer simulation of inspiratory airflow in all regions of the F344 rat nasal passages. Toxicol. Appl. Pharmacol. 145, 388-398. (doi:10.1006/taap.1997.8206)
20. Kuramoto, K., Nishida, T. & Mochizuki, K. 1985 Morphological study on the nasal turbinates (Conchae) of the pika (Ochotona rufescens rufescens) and the volcano rabbit (Romerolagus diazi). Anat. Histol. Embryol. 14, 332-341.
21. Lang, J. 1989 Clinical anatomy of the nose, nasal cavity and paranasal sinuses. Stuttgart, NY: Thieme.
22. Liberles, S. D. & Buck, L. B. 2006 A second class of chemosensory receptors in the olfactory epithelium. Nature 442, 645-650. (doi:10.1038/ nature05066)
23. Lledo, P. M., Gheusi, G. & Vincent, J. D. 2005 Information processing in the mammalian olfactory system. Physiol. Rev. 85, 281-317. (doi:10.1152/physrev.00008.2004)
24. Lung, M. A. & Wang, J. C. C. 1989 Autonomic nervous control of nasal vasculature and air-flow resistance in the anesthetized dog. J. Physiol. Lond. 419, 121-139.
25. Marshall, D. A. & Moulton, D. G. 1977 Quantification of nasal air flow patterns in dogs performing an odor detection task. In Proc. Sixth International Symposium on Olfaction and Taste. Olfaction and Taste VI (eds J. LeMagnen & P. MacLeod), p. 197. Washington, DC: Information Retrieval.
26. Morrison, E. E. & Costanzo, R. M. 1990 Morphology of the human olfactory epithelium. J. Comp. Neurol. 297, 1-13. (doi:10.1002/cne.902970102)
27. Morrison, E. E.&Costanzo, R. M. 1992 Morphology of olfactory epithelium in humans and other vertebrates. Microsc. Res. Tech. 23, 49-61. (doi:10.1002/jemt.1070230105)
28. Mozell, M. M. 1964 Evidence for sorption as a mechanism of olfactory analysis of vapours. Nature 203, 1181-1182. (doi:10.1038/2031181a0)
29. Negus, V. E. 1958 The comparative anatomy and physiology of the nose and paranasal sinuses. London, UK: Livingstone.
30. Pihstrom, H., Fortelius, M., Hemila, S., Forsman, R. & Reuter, T. 2005 Scaling of mammalian ethmoid bones can predict olfactory organ size and performance. Proc. Biol. Sci. 272, 957-962.
31. Porter, J., Craven, B., Khan, R. M., Chang, S. J., Kang, I., Judkewicz, B., Volpe, J., Settles, G. & Sobel, N. 2007 Mechanisms of scent-tracking in humans. Nat. Neurosci. 10, 27-29. (doi:10.1038/nn1819)
32. Proctor, D. F. 1982 The upper airway. In The nose: upper airway physiology and the atmospheric environment (eds D. F. Proctor & I. B. Anderson), pp. 23-43. New York, NY: Elsevier Biomedical Press.
33. Quignon, P. et al. 2003 Comparison of the canine and human olfactory receptor gene repertoires. Genome Biol. 4, R80. (doi:10.1186/gb-2003-4-12-r80)
34. Rajan, R., Clement, J. P. & Bhalla, U. S. 2006 Rats smell in stereo. Science 311, 666-670. (doi:10.1126/science.1122096)
35. Rouquier, S. & Giorgi, D. 2007 Olfactory receptor gene repertoires in mammals. Mutat. Res. 616, 95-102.
36. Rouquier, S., Taviaux, S., Trask, B. J., Brand-Arpon, V., van den Engh, G., Demaille, J. & Giorgi, D. 1998 Distribution of olfactory receptor genes in the human genome. Nat. Genet. 18, 243-250. (doi:10.1038/ng0398-243)
37. Rouquier, S., Blancher, A. & Giorgi, D. 2000 The olfactory receptor gene repertoire in primates and mouse: evidence for reduction of the functional fraction in primates. Proc. Natl Acad. Sci. USA 97, 2870-2874. (doi:10.1073/pnas.040580197)
38. Schmidt-Nielsen, K. 1984 Scaling: why is animal size so important? New York, NY: Cambridge University Press.
39. Schoenfeld, T. A. & Cleland, T. A. 2005 The anatomical logic of smell. Trends Neurosci. 28, 620-627. (doi:10.1016/j.tins.2005.09.005)
40. Schreider, J. P. & Raabe, O. G. 1981 Anatomy of the nasalpharyngeal airway of experimental animals. Anat. Rec. 200, 195-205. (doi:10.1002/ar. 1092000208)
41. Settles, G. S. 2005 Sniffers: Fluid-dynamic sampling for olfactory trace detection in nature and homeland security - the 2004 Freeman Scholar Lecture. J. Fluids Eng. 127, 189-218. (doi:10.1115/1.1891146)
42. Settles, G. S., Kester, D. A. & Dodson-Dreibelbis, L. J. 2003 The external aerodynamics of canine olfaction. In Sensors and sensing in biology and engineering (eds F. G. Barth, J. A. C. Humphrey & T. W. Secomb), pp. 323-335. New York, NY: Springer.
43. Shah, A. S., Ben-Shahar, Y., Moninger, T. O., Kline, J. N. & Welsh, M. J. 2009 Motile cilia of human airway epithelia are chemosensory. Science 325, 1131-1134. (doi:10.1126/science.1173869)
44. Shepherd, G. M. 2004 The human sense of smell: are we better than we think? PLoS Biol. 2, 572-575.
45. Shi, H., Kleinstreuer, C. & Zhang, Z. 2006 Laminar airflow and nanoparticle or vapor deposition in a human nasal cavity model. J. Biomech. Eng. 128, 697-706. (doi:10.1115/1.2244574)
46. Smith, T. D., Bhatnagar, K. P., Tuladhar, P. & Burrows, A. M. 2004 Distribution of olfactory epithelium in the primate nasal cavity: are microsmia and macrosmia valid morphological concepts? Anat. Rec. 281A, 1173-1181. (doi:10.1002/ar.a.20122)
47. Smith, T. D., Rossie, J. B. & Bhatnagar, K. P. 2007 Evolution of the nose and nasal skeleton in primates. Evol. Anthropol. Issues News Rev. 16, 132-146.
48. Sobel, N., Khan, R. M., Saltman, A., Sullivan, E. V. & Gabrieli, J. D. E. 1999 Olfaction-the world smells different to each nostril. Nature 402, 35. (doi:10.1038/46944) (Pubitemid 29533504)
49. Stahl, W. R. 1967 Scaling of respiratory variables in mammals. J. Appl. Physiol. 22, 453-460.
50. Subramaniam, R. P., Richardson, R. B., Morgan, K. T., Kimbell, J. S. & Guilmette, R. A. 1998 Computational fluid dynamics simulations of inspiratory airflow in the human nose and nasopharynx. Inhal. Toxicol. 10, 473-502.
51. Swift, D. L. & Proctor, D. F. 1977 Access of air to the respiratory tract. In Respiratory defense mechanisms (eds J. D. Brain, D. F. Proctor & L. M. Reid), pp. 63-93. New York, NY: Marcel Dekker, Inc.
52. Thesen, A., Steen, J. B. & Doving, K. B. 1993 Behaviour of dogs during olfactory tracking. J. Exp. Biol. 180, 247-251.
53. Uchida, N. & Mainen, Z. F. 2003 Speed and accuracy of olfactory discrimination in the rat. Nature Neurosci. 6, 1224-1229. (doi:10.1038/nn1142) (Pubitemid 37346044)
54. Vanderburgh, P. M., Mahar, M. T. & Chou, C. H. 1995 Allometric scaling of grip strength by body mass in college-age men and women. Res. Q. Exerc. Sport 66, 80-84.
55. Van Valkenburgh, B., Theodor, J., Friscia, A., Pollack, A. & Rowe, T. 2004 Respiratory turbinates of canids and felids: a quantitative comparison. J. Zool. 264, 281-293. (doi:10.1017/S0952836904005771) (Pubitemid 39459582)
56. Walker, D. B., Walker, J. C., Cavnar, P. J., Taylor, J. L., Pickel, D. H., Hall, S. B. & Suarez, J. C. 2006 Naturalistic quantification of canine olfactory sensitivity. Appl. Anim. Behav. Sci. 97, 241-254. (doi:10.1016/j. applanim.2005.07.009)
57. Walker, J. C., Hall, S. B., Walker, D. B., Kendal-Reed, M. S., Hood, A. F. & Niu, X. F. 2003 Human odor detectability: new methodology used to determine threshold and variation. Chem. Senses 28, 817-826. (doi:10.1093/chemse/bjg075)
58. Webber, R. L., Jeffcoat, M. K., Harman, J. T. & Ruttimann, U. E. 1987 MR Demonstration of the nasal cycle in the Beagle dog. J. Comput. Assist. Tomogr. 11, 869-871.
59. Wesson, D. W., Donahou, T. N., Johnson, M. O. & Wachowiak, M. 2008 Sniffing behavior of mice during performance in odor-guided tasks. Chem. Senses 33, 581-596.
60. Wilson, D. A. 1997 Binaral interactions in the rat piriform cortex. J. Neurophysiol. 78, 160-169. (Pubitemid 27318920)
61. Wilson, D. A. & Sullivan, R. M. 1999 Respiratory airflow pattern at the rat's snout and an hypothesis regarding its role in olfaction. Physiol. Behav. 66, 41-44. (doi:10.1016/S0031-9384(98)00269-8)
62. Yang, G. C., Scherer, P. W. & Mozell, M. M. 2007 Modeling inspiratory and expiratory steady-state velocity fields in the Sprague-Dawley rat nasal cavity. Chem. Senses 32, 215-223. (doi:10.1093/chemse/bjl047)
63. Youngentob, S. L., Mozell, M. M., Sheehe, P. R. & Hornung, D. E. 1987 A quantitative-analysis of sniffing strategies in rats performing odor detection tasks. Physiol. Behav. 41, 59-69. (doi:10.1016/0031-9384(87)90131-4)
64. Zhao, K., Scherer, P. W., Hajiloo, S. A. & Dalton, P. 2004 Effect of anatomy on human nasal air flow and odorant transport patterns: implications for olfaction. Chem. Senses 29, 365-379. (doi:10.1093/chemse/bjh033) (Pubitemid 41289315)
65. Zhao, K., Dalton, P., Yang, G. C. & Scherer, P. W. 2006 Numerical modeling of turbulent and laminar airflow and odorant transport during sniffing in the human and rat nose. Chem. Senses 31, 107-118. (doi:10.1093/chemse/bjj008) (Pubitemid 43231437)