Functional MRI of the olfactory system in conscious dogs

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Jia, Hao ^a   Pustovyy, Oleg M ^b   Waggoner, Paul ^b   Beyers, Ronald J ^a   Schumacher, John ^b   Wildey, Chester ^c   Barrett, Jay ^b   Morrison, Edward ^b   Salibi, Nouha ^d   Denney, Thomas S ^a,b   Vodyanoy, Vitaly J ^b   Deshpande, Gopikrishna ^a,b  

^a AUBURN UNIVERSITY   (United States)

^b AUBURN UNIVERSITY   (United States)

^c MRRA Inc   (United States)

^d MR RandD Siemens Healthcare   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BOLD SIGNAL; BRAIN REGION; CEREBELLUM; COMPUTER SYSTEM; CONSCIOUSNESS; CONTROLLED STUDY; DOG; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEAD MOVEMENT; MALE; MOTION ANALYSIS SYSTEM; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; ODOR; OLFACTORY BULB; OLFACTORY SYSTEM; PYRIFORM CORTEX; TRAINING;

ANIMALS; BRAIN MAPPING; CONSCIOUSNESS; DOGS; FRONTAL LOBE; MAGNETIC RESONANCE IMAGING; OLFACTORY BULB; OLFACTORY PATHWAYS; OLFACTORY PERCEPTION;

EID: 84899832240     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086362     Document Type: Article

References (76)

1. Jensen P (2007) The behavioral biology of dogs. Cambridge, MA: CAB International.
2. Harel D, Carmel L, Lancet D (2003) Towards an odor communication system. Comput Biol Chem 27: 121-133.
3. Haberly L (2001) Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem Senses 26: 551-576.
4. Zald D, Pardo J (1997) Emotion, olfaction, and the human amygdala: amygdala activation during aversive olfactory stimulation. Proc Natl Acad Sci U S A 94: 4119-4124. (Pubitemid 27180509)
5. Shepherd G (1994) Discrimination of molecular signals by the olfactory receptor neuron. Neuron 13: 771-790.
6. Ramnani N, Owen A (2004) Anterior prefrontal cortex: insights into function from anatomy and neuroimaging. Nat Rev Neurosci 5: 184-194. (Pubitemid 38252475)
7. Zobel S, Hummel T, Ilgner J, Finkelmeyer A, Habel U, et al. (2010) Involvement of the human ventrolateral thalamus in olfaction. J Neurol 257: 2037-2043.
8. Bear M, Connors B, Paradiso M (2007) Neuroscience: Exploring the brain. Baltimore: Lippincott Williams & Wilkins. pp. 265-275.
9. Nadi NS, Hirsch JD, Margolis FL (1980) Laminar distribution of putative neurotransmitter amino acids and ligand binding sites in the dog olfactory bulb. J Neurochem 34: 138-146. (Pubitemid 10172689)
10. Price S (1978) Anisole binding protein from dog olfactory epithelium. Chem Senses 3: 51-55.
11. Hirai T, Kojima S, Shimada A, Umemura T, Sakai M, et al. (1996) Age-related changes in the olfactory system of dogs. Neuropathol Appl Neurobiol 22: 531-539. (Pubitemid 27023370)
12. Doty RL, Kreiss DS, Frye RE (1990) Human odor intensity perception: correlation with frog epithelial adenylate cyclase activity and transepithelial voltage response. Brain Res. 527: 130-134. (Pubitemid 20290594)
13. Lowe G, Nakamura T, Gold GH (1988) Eog amplitude is correlated with odor-stimulated adenylate-cyclase activity in the bullfrog olfactory epithelium. Chem Senses 13: 710-710.
14. Viswaprakash N, Dennis J, Globa L, Pustovyy O, Josephson E, et al. (2009) Enhancement of odorant-induced responses in olfactory receptor neurons by zinc nanoparticles. Chem Senses 34: 547-557.
15. Szetei V, Miklósi Á, Topál J, Csányi V (2003) When dogs seem to lose their nose: an investigation on the use of visual and olfactory cues in communicative context between dog and owner. Appl Anim Behav Sci 83: 141-152. (Pubitemid 37078113)
16. Williams M, Johnston J (2002) Training and maintaining the performance of dogs (Canis familiaris) on an increasing number of odor discriminations in a controlled setting. Appl Anim Behav Sci 78: 55-65. (Pubitemid 34973583)
17. Ross H, Murray D (1996) (Ed. and Transl.) E.H.Weber on the tactile senses. 2nd ed. Hove: Erlbaum (UK) Taylor & Francis.
18. Bandettini P, Wong E, Hinks R, Tifosky R, Hyde J (1992) Time course EPI of human brain function during task activation. Magn Reson Med 25: 390-398.
19. Ogawa S, Tank DW, Menon R, Ellermann JM, Kim SG, et al. (1992) Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci U S A 89: 5951-5955.
20. Sicard K, Shen Q, Brevard M, Sullivan R, Ferris C, et al. (2003) Regional cerebral blood flow and BOLD responses in conscious and anesthetized rats under basal and hypercapnic conditions: implications for functional MRI studies. J Cereb Blood Flow Metab 23: 472-481. (Pubitemid 36403029)
21. Peeters R, Tindemans I, De Schutter E, Van Der Linden A (2001) Comparing BOLD fMRI signal changes in the awake and anesthetized rat during electrical forepaw stimulation. Magn Reson Imaging 19: 821-826. (Pubitemid 32845949)
22. De Groof G, Jonckers E, Güntürkün O, Denolf P, Auderkerke JV, et al. (2013) Functional MRI and functional connectivity of the visual system of awake pigeons. Behav Brain Res 239: 43-50.
23. Wildey C, MacFarlane D, Goyal A, Gopinath K, Cheshkov S, et al. (2011) Single-camera motion measurement and monitoring for magnetic resonance applications. Appl Opt 50: 2088-2097.
24. Savic I (2005) Brain imaging studies of the functional organization of human olfaction. Chem Senses 30 Suppl 1: i222-i223.
25. Zald D, Pardo J (2000) Functional neuroimaging of the olfactory system in humans. Int J Psychophysiol 36: 165-181. (Pubitemid 30160744)
26. Boyett-Anderson J, Lyons D, Reiss A, Schatzberg A, Menon V (2003) Functional brain imaging of olfactory processing in monkeys. Neuroimage 20: 257-264. (Pubitemid 37203402)
27. Mori K, Takahashi Y, Igarashi K, Nagayama S (2005) Odor maps in the dorsal and lateral surfaces of the rat olfactory bulb. Chem Senses 30 Suppl 1: i103-i104.
28. The Welcome Trust Centre for NeuroImaging, Institute of Neurology at University College London (UCL), UK. Available: http://www.fil.ion.ucl.ac.uk/ spm/software/spm8/. Accessed 2013 Dec 3.
29. Berns G, Brooks A, Spivak M (2012) Functional MRI in awake unrestrained dogs. PLoS One 7: e38027.
30. Lorig T, Elmes D, Zald D, Pardo J (1999) A computer-controlled olfactometer for fMRI and electrophysiological studies of olfaction. Behav Res Methods Instrum Comput 31: 370-375.
31. Sommer J, Maboshe W, Griebe M, Heiser C, Hörmann K, et al. (2012) A mobile olfactometer for fMRI-studies. J Neurosci Methods 209: 189-194.
32. Lowen S, Lukas S (2006) A low-cost, MR-compatible olfactometer. Behav Res Methods 38: 307-313.
33. Popp R, Sommer M, Müller J, Hajak G (2004) Olfactometry in fMRI studies: odor presentation using nasal continuous positive airway pressure. Acta Neurobiol Exp (Wars) 64: 171-176. (Pubitemid 38649378)
34. Slotnick B, Restrepo D (2005) Olfactometry with Mice. Hoboken (NJ): Wiley InterScience. p. unit 8.20.
35. Warner Instruments. Available: http://vt-8-valve-timer.software.informer. com/. Accessed 2013 Dec 3.
36. Smiths Medical. Available: http://www.surgivet.com/pet-oxygen-masks/ index.html. Accessed 2013 Dec 3.
37. Pathirana S, Neely W, Myers L, Vodyanoy V (1992) Chiral Recognition of Odorants (+)-Carvone and (-)-Carvone by Phospholipid Monolayers. J Am Chem Soc 114: 1404-1405.
38. Bednarski R, Grimm K, Harvey R, Lucasik V, Penn W, et al. (2011) AAHA anesthesia guidelines for dogs and cats. J Am Anim Hosp Assoc 47: 377-385.
39. Ferris C, Smerkers B, Kulkarni P, Caffrey M, Afacan O, et al. (2011) Functional magnetic resonance imaging in awake animals. Rev Neurosci 22: 665-674.
40. Macfarlane D, Wildey C (2010) fMRI headtracking using a single camera and a lightweight fiducial. Conf Proc IEEE Eng Med Biol Soc 2010: 5673-5676.
41. Martin C, Grenier D, Thévenet M, Vigouroux M, Bertrand B, et al. (2007) fMRI visualization of transient activations in the rat olfactory bulb using short odor stimulations. Neuroimage 36: 1288-1293. (Pubitemid 47008960)
42. Ottoson D (1955) Analysis of the electrical activity of the olfactory epithelium. Acta Physiol Scand Suppl 35: 1-83, 1955.
43. Poellinger A, Thomas R, Lio P, Lee A, Makris N, et al. (2001) Activation and habituation in olfaction-an fMRI study. Neuroimage 13: 547-60. (Pubitemid 34184979)
44. Yang X, Renken R, Hyder F, Siddeek M, Greer C, et al. (1998) Dynamic mapping at the laminar level of odor-elicited responses in rat olfactory bulb by functional MRI. Proc Natl Acad Sci U S A 95: 7715-7720. (Pubitemid 28293319)
45. Wilson D (1998) Habituation of odor responses in the rat anterior piriform cortex. J Neurophysiol 79: 1425-1440.
46. Butts K, Riederer SJ, Ehman RL, Thompson RM, Jack CR (1994) Interleaved echo planar imaging on a standard MRI system. Magn Reson Med 31: 67-72.
47. Brant-Zawadzki M, Gillan G, Nitz W (1992) MP RAGE: a three-dimensional, T1-weighted, gradient-echo sequence-initial experience in the brain. Radiology 182: 769-775.
48. Ashburner J, Friston K (1999) Nonlinear spatial normalization using basis functions. Hum Brain Mapp 7: 254-266. (Pubitemid 29269964)
49. Frey S, Pandya D, Chakravarty M, Bailey L, Petrides M, et al. (2011) An MRI based average macaque monkey stereotaxic atlas and space (MNI monkey space). Neuroimage 55: 1435-1442.
50. Datta R, Lee J, Duda J, Avants B, Vite C, et al. (2012) A digital atlas of the dog brain. PLoS One 7: e52140.
51. Forman S, Cohen J, Fitzgerald M, Eddy W, Mintun M, et al. (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med 33: 636-647.
52. Xiong J, Gao J, Lancaster JL, Fox PT (1995) Clustered pixels analysis for functional MRI activation studies of the human brain. Hum Brain Mapp 3: 287-301.
53. Ward B (2000) Available: http://afni.nimh.nih.gov/pub../pub/dist/doc/ manual/AlphaSim.pdf. Accessed 2013 Oct. 3.
54. Fletcher T, Saveraid T. Canine Brain MRI Atlas website. Available: http://vanat.cvm.umn.edu/mriBrainAtlas/index.html. Accessed 2013 Oct. 3.
55. Kondoh T, Yamada S, Shioda S, Torii K (2005) Central olfactory pathway in response to olfactory stimulation in rats detected by magnetic resonance imaging. Chem Senses Suppl 1: i172.
56. Krestel D, Passe D, Smith J, Jonsson L (1984) Behavioral determination of olfactory thresholds to amyl acetate in dogs. Neurosci Biobehav Rev 8: 169-174. (Pubitemid 14098411)
57. Walker D, Walker J, Cavnar P, Talyor J, Pickel D, et al. (2006) Naturalistic quantification of canine olfactory sensitivity. Appl Anim Behav Sci 97: 241-254.
58. Frederick BR, Edward KJ, Markee JE (1962) Studies on olfactory discrimination in dogs: II. Discriminatory behavior in a free environment. J Comp Physiol Psychol 55: 773-780.
59. Williams M, Johnston J, Cicoria M, Paletz E, Waggoner P, et al. (1998) Canine detection odor signatures for explosives. Proc SPIE 3575: 291-301.
60. Kandel E, Schwartz J, Jessell T (2000) Priciples of neural science. 4th ed. New York: McGraw-Hill.
61. Orban G (2001) Imaging image processing in the human brain. Curr Opin Neurol 14: 47-54.
62. Olfactory System Anatomy website. Available: http://emedicine.medscape. com/article/835585-overview. Accessed 2013 Oct. 3.
63. Gottfried J, Zald D (2005) On the scent of human olfactory orbitofrontal cortex: meta-analysis and comparison to non-human primates. Brain Res Rev 50: 287-304. (Pubitemid 41654399)
64. Bensafi M, Iannilli E, Gerber J, Hummel T (2008) Neural coding of stimulus concentration in the human olfactory and intranasal trigeminal systems. Neuroscience 154: 832-838.
65. Sobel N, Prabhakaran V, Desmond JE, Glover GH, Goode RL, et al. (1998) Sniffing and smelling: separate subsystems in the human olfactory cortex. Nature 392: 282-286. (Pubitemid 28155100)
66. Friston K, Mechelli A, Turner R, Price C (2000) Nonlinear responses in fMRI: the Ballon model, Volterra kernels, and other hemodynamics. Neuroimage 12: 466-477.
67. Studzinski C, Araujo J, Milgram N (2005) The canine model of human cognitive aging and demintia: pharmacological validity of the model for assessment of human cognitive-enhancing drugs. Prog Neuropsychopharmacol Biol Psychiatry 29: 489-498. (Pubitemid 40417601)
68. Oxley J, Waggoner P (2009) Detection of explosives by dogs. In: Marshall M, Oxley J, eds. Aspects of Explosives Detection. Elsevier: Amsterdam. pp. 27-40.
69. Youngentob S, Johnson B, Leon M (2006) Predicting odorant quality from multidimensional scaling of olfactory bulb glomerular activity patterns. Behav Neurosci 120: 1337-1345. (Pubitemid 46058709)
70. Kruse A (2007) Defense Sciences Research and Technology Special Focus Area: RealNose. Available: https://www.fbo.gov/index?s=opportunity&mode= form&tab=core&id=32bb6977f45cc0b870f0837f32ad7fcf&-cview=0. Accessed 2013 Oct. 3.
71. Howell T, Conduit R, Toukhsati S, Bennett P (2012) Auditory stimulus discrimination recorded in dogs, as indicated by mismatch negativity (MMN). Behav Processes 89: 8-13.
72. Kujala M, Törnqvist H, Somppi S, Hänninen L, Krause C (2013) Reactivity of dogs' brain oscillations to visual stimuli measured with non-invasive electroencephalography. PLoS One 8: e61818.
73. Törnqvist H, Kujala M, Somppi S, Hänninen L, Pastell M, et al. (2013) Visual event-related potentials of dogs: a non-invasive electroencephalography study. Anim Cogn 16: 973-982.
74. Vodyanoy V, Morrison E (2005) Apparatus and method for the measurement of the aerodynamics of olfaction in animals and man. US Patent 6,979,298, 27 12 2005.
75. Qin L, van Gelderen P, Derbyshire JA, Jin F, Lee J, et al. (2009) Prospective head movement correction for high resolution MRI using an in-bore optical tracking system. Magn Reson Med 62: 924-934.
76. Tremblay M, Tam F, Graham SJ (2005) Retrospective coregistration of functional magnetic resonance imaging data using external monitoring. Magn Reson Med 53: 141-149. (Pubitemid 40110487)