Early Aging Effect on the Function of the Human Central Olfactory System

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 72, Issue 8, 2017, Pages 1007-1014

  Wang, Jianli ^a   Sun, Xiaoyu ^a   Yang, Qing X ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Age; Aging; fMRI; Olfaction; Primary olfactory cortex

Indexed keywords

ADULT; AGE; AGING; BRAIN MAPPING; DIAGNOSTIC IMAGING; FEMALE; FRONTAL LOBE; HUMAN; MALE; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; ODOR; OLFACTION DISORDERS; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; SMELLING; STATISTICS;

ADULT; AGE FACTORS; AGING; BRAIN MAPPING; FEMALE; FRONTAL LOBE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; OLFACTION DISORDERS; OLFACTORY PERCEPTION; SMELL; STATISTICS AS TOPIC;

EID: 85026856451     PISSN: 10795006     EISSN: 1758535X     Source Type: Journal    
DOI: 10.1093/gerona/glw104     Document Type: Review

References (64)

1. Doty RL, Shaman P, Applebaum SL, Giberson R, Siksorski L, Rosenberg L. Smell identification ability: changes with age. Science. 1984;226(4681):1441-1443. doi:10.1126/science.6505700
2. Stevens JC, Cain WS, Schiet FT, Oatley MW. Olfactory adaptation and recovery in old age. Perception. 1989;18(2):265-276. doi:10.1068/p180265
3. Cowart BJ. Relationships between taste and smell across the adult life span. Ann NY Acad Sci. 1989;561:39-55. doi:10.1111/j.1749-6632.1989.tb20968.x
4. Kaneda H, Maeshima K, Goto N, Kobayakawa T, Ayabe-Kanamura S, Saito S. Decline in taste and odor discrimination abilities with age, and relationship between gustation and olfaction. Chem Senses. 2000;25(3):331-337. doi:10.1093/chemse/25.3.331
5. Hummel T, Kobal G, Gudziol H, Mackay-Sim A. Normative data for the "Sniffin' Sticks" including tests of odor identification, odor discrimination, and olfactory thresholds: an upgrade based on a group of more than 3,000 subjects. Eur Arch Otorhinolaryngol. 2007;264(3):237-243. doi:10.1007/s00405-006-0173-0
6. Ship JA, Weiffenbach JM. Age, gender, medical treatment, and medication effects on smell identification. J Gerontol. 1993;48(1):M26-M32. doi:10.1093/geronj/48.1.M26
7. Murphy C, Cain WS, Gilmore MM, Skinner RB. Sensory and semantic factors in recognition memory for odors and graphic stimuli: elderly versus young persons. Am J Psychol. 1991;104(2):161-192.
8. Larsson M, Finkel D, Pedersen NL. Odor identification: influences of age, gender, cognition, and personality. J Gerontol B Psychol Sci Soc Sci. 2000;55(5):P304-P310. doi:10.1093/geronb/55.5.P304
9. Pinto JM, Wroblewski KE, Kern DW, Schumm LP, McClintock MK. The Rate of Age-Related Olfactory Decline Among the General Population of Older U.S. Adults. J Gerontol A Biol Sci Med Sci. 2015;70(11): 1435-1441. doi:10.1093/gerona/glv072
10. Schubert CR, Cruickshanks KJ, Fischer ME, et al. Olfactory impairment in an adult population: the Beaver Dam Offspring Study. Chem Senses. 2012;37(4):325-334. doi:10.1093/chemse/bjr102
11. Paik SI, Lehman MN, Seiden AM, Duncan HJ, Smith DV. Human olfactory biopsy. The influence of age and receptor distribution. Arch Otolaryngol Head Neck Surg. 1992;118(7):731-738. doi:10.1001/archotol.1992.01880070061012
12. Nakashima T, Kimmelman CP, Snow JB Jr. Structure of human fetal and adult olfactory neuroepithelium. Arch Otolaryngol. 1984;110(10):641-646.
13. Rawson NE, Gomez G, Cowart BJ, Kriete A, Pribitkin E, Restrepo D. Age-associated loss of selectivity in human olfactory sensory neurons. Neurobiol Aging. 2012;33(9):1913-1919. doi:10.1016/j.neurobiolaging.2011.09.036.
14. Evans WJ, Cui L, Starr A. Olfactory event-related potentials in normal human subjects: effects of age and gender. Electroencephalogr Clin Neurophysiol. 1995;95(4):293-301.
15. Murphy C, Wetter S, Morgan CD, Ellison DW, Geisler MW. Age effects on central nervous system activity reflected in the olfactory eventrelated potential. Evidence for decline in middle age. Ann NY Acad Sci. 1998;855:598-607. doi:10.1111/j.1749-6632.1998.tb10630.x
16. Wang J, Eslinger PJ, Smith MB, Yang QX. Functional magnetic resonance imaging study of human olfaction and normal aging. J Gerontol A Biol Sci Med Sci. 2005;60(4):510-514. doi:10.1093/gerona/60.4.510
17. Suzuki Y, Critchley HD, Suckling J, et al. Functional magnetic resonance imaging of odor identification: the effect of aging. J Gerontol A Biol Sci Med Sci. 2001;56(12):M756-M760. doi:10.1093/gerona/56.12.M756
18. Cerf-Ducastel B, Murphy C. FMRI brain activation in response to odors is reduced in primary olfactory areas of elderly subjects. Brain Res. 2003;986(1-2):39-53. doi:10.1016/S0006-8993(03)03168-8
19. Wang J, You H, Liu JF, Ni DF, Zhang ZX, Guan J. Association of olfactory bulb volume and olfactory sulcus depth with olfactory function in patients with Parkinson disease. AJNR Am J Neuroradiol. 2011;32(4):677-681. doi:10.3174/ajnr.A2350
20. Buschhuter D, Smitka M, Puschmann S, et al. Correlation between olfactory bulb volume and olfactory function. Neuroimage. 2008;42(2): 498-502. doi:10.1016/j.neuroimage.2008.05.004
21. Yousem DM, Maldjian JA, Hummel T, et al. The effect of age on odor-stimulated functional MR imaging. AJNR Am J Neuroradiol. 1999;20(4):600-608.
22. Larsson M, Farde L, Hummel T, Witt M, Lindroth NE, Backman L. Agerelated loss of olfactory sensitivity: association to dopamine transporter binding in putamen. Neuroscience. 2009;161(2):422-426. doi:10.1016/j.neuroscience.2009.03.074
23. Wong KK, Muller ML, Kuwabara H, Studenski SA, Bohnen NI. Olfactory loss and nigrostriatal dopaminergic denervation in the elderly. Neurosci Lett. 2010;484(3):163-167. doi:10.1016/j.neulet.2010.08.037
24. Serby M, Corwin J, Conrad P, Rotrosen J. Olfactory dysfunction in Alzheimer's disease and Parkinson's disease. Am J Psychiatry. 1985;142(6): 781-782. doi:10.1176/ajp.142.6.aj1426781
25. Doty RL. Influence of age and age-related diseases on olfactory function. Ann NY Acad Sci. 1989;561:76-86. doi:10.1111/j.1749-6632.1989.tb20971.x
26. Murphy C, Schubert CR, Cruickshanks KJ, Klein BE, Klein R, Nondahl DM. Prevalence of olfactory impairment in older adults. JAMA. 2002;288(18):2307-2312. doi:10.1001/jama.288.18.2307
27. Graves AB, Bowen JD, Rajaram L, et al. Impaired olfaction as a marker for cognitive decline: interaction with apolipoprotein E epsilon4 status. Neurology. 1999;53(7):1480-1487.
28. Wilson RS, Schneider JA, Arnold SE, Tang Y, Boyle PA, Bennett DA. Olfactory identification and incidence of mild cognitive impairment in older age. Arch Gen Psychiatry. 2007;64(7):802-808. doi:10.1001/archpsyc.64.7.802
29. Devanand DP, Michaels-Marston KS, Liu X, et al. Olfactory deficits in patients with mild cognitive impairment predict Alzheimer's disease at follow-up. Am J Psychiatry. 2000;157(9):1399-1405. doi:10.1176/appi.ajp.157.9.1399
30. Lojkowska W, Sawicka B, Gugala M, et al. Follow-up study of olfactory deficits, cognitive functions, and volume loss of medial temporal lobe structures in patients with mild cognitive impairment. Curr Alzheimer Res. 2011;8(6):689-698. doi:10.2174/156720511796717212
31. Allen W. Studies on the level of anesthesia for the olfactory and trigeminal respiratory reflexes in dogs and rabbits. Am J Physiol. 1936;115: 579-587.
32. Patton HD. Taste, olfaction and visceral sensation. In: Ruth TC, Fulton JF, eds. Medical Physiology and Biophysics. Philadelphia, PA: Saunders; 1960: 375.
33. Wang J, Sun X, Yang QX. Methods for olfactory fMRI studies: implication of respiration. Hum Brain Mapp. 2014;35(8):3616-3624. doi:10.1002/hbm.22425
34. Friston KJ, Tononi G, Reeke GN Jr, Sporns O, Edelman GM. Valuedependent selection in the brain: simulation in a synthetic neural model. Neuroscience. 1994;59(2):229-243. doi:10.1016/0306-4522(94)90592-4
35. Collins DL, Zijdenbos AP, Kollokian V, et al. Design and construction of a realistic digital brain phantom. IEEE Trans Med Imaging. 1998;17(3):463-468. doi:10.1109/42.712135
36. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. 2002;15(1):273-289. doi:10.1006/nimg.2001.0978
37. de Araujo IE, Rolls ET, Velazco MI, Margot C, Cayeux I. Cognitive modulation of olfactory processing. Neuron. 2005;46(4):671-679. doi:10.1016/j.neuron.2005.04.021
38. Howard JD, Gottfried JA. Configural and elemental coding of natural odor mixture components in the human brain. Neuron. 2014;84(4):857-869. doi:10.1016/j.neuron.2014.10.012
39. Wu KN, Tan BK, Howard JD, Conley DB, Gottfried JA. Olfactory input is critical for sustaining odor quality codes in human orbitofrontal cortex. Nat Neurosci. 2012;15(9):1313-1319. doi:10.1038/nn.3186
40. Li W, Luxenberg E, Parrish T, Gottfried JA. Learning to smell the roses: experience-dependent neural plasticity in human piriform and orbito-frontal cortices. Neuron. 2006;52(6):1097-1108. doi:10.1016/j.neuron.2006.10.026
41. Boyle JA, Djordjevic J, Olsson MJ, Lundstrom JN, Jones-Gotman M. The human brain distinguishes between single odorants and binary mixtures. Cereb Cortex. 2009;19(1):66-71. doi:10.1093/cercor/bhn058
42. Djordjevic J, Zatorre RJ, Petrides M, Boyle JA, Jones-Gotman M. Functional neuroimaging of odor imagery. Neuroimage. 2005;24(3): 791-801. doi:10.1016/j.neuroimage.2004.09.035
43. Royet JP, Hudry J, Zald DH, et al. Functional neuroanatomy of different olfactory judgments. Neuroimage. 2001;13(3):506-519. doi:10.1006/nimg.2000.0704
44. Kjelvik G, Evensmoen HR, Brezova V, Haberg AK. The human brain representation of odor identification. J Neurophysiol. 2012;108(2):645-657. doi:10.1152/jn.01036.2010
45. Plailly J, Radnovich AJ, Sabri M, Royet JP, Kareken DA. Involvement of the left anterior insula and frontopolar gyrus in odor discrimination. Hum Brain Mapp. 2007;28(5):363-372. doi:10.1002/hbm.20290
46. Qureshy A, Kawashima R, Imran MB, et al. Functional mapping of human brain in olfactory processing: a PET study. J Neurophysiol. 2000;84(3):1656-1666.
47. Mak YE, Simmons KB, Gitelman DR, Small DM. Taste and olfactory intensity perception changes following left insular stroke. Behav Neurosci. 2005;119(6):1693-1700. doi:10.1037/0735-7044.119.6.1693
48. Heining M, Young AW, Ioannou G, et al. Disgusting smells activate human anterior insula and ventral striatum. Ann NY Acad Sci. 2003;1000: 380-384. doi:10.1196/annals.1280.035
49. Kurth F, Zilles K, Fox PT, Laird AR, Eickhoff SB. A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct Funct. 2010;214 (5-6):519-534. doi:10.1007/s00429-010-0255-z
50. Karunanayaka P, Eslinger PJ, Wang JL, et al. Networks involved in olfaction and their dynamics using independent component analysis and unified structural equation modeling. Hum Brain Mapp. 2014;35(5): 2055-2072. doi:10.1002/hbm.22312
51. Reske M, Kellermann T, Shah NJ, Schneider F, Habel U. Impact of valence and age on olfactory induced brain activation in healthy women. Behav Neurosci. 2010;124(3):414-422. doi:10.1037/a0019289
52. Rolls ET, Grabenhorst F, Parris BA. Neural systems underlying decisions about affective odors. J Cogn Neurosci. 2010;22(5):1069-1082. doi:10.1162/jocn.2009.21231
53. Dade LA, Zatorre RJ, Evans AC, Jones-Gotman M. Working memory in another dimension: functional imaging of human olfactory working memory. Neuroimage. 2001;14(3):650-660. doi:10.1006/nimg.2001.0868
54. Shen J, Kassir MA, Wu J, et al. MR volumetric study of piriform-cortical amygdala and orbitofrontal cortices: the aging effect. PLoS One. 2013;8(9):e74526. doi:10.1371/journal.pone.0074526
55. Murphy C, Morgan CD, Geisler MW, et al. Olfactory eventrelated potentials and aging: normative data. Int J Psychophysiol. 2000;36(2):133-145. doi:10.1016/S0167-8760(99)00107-5
56. Doty RL, Shaman P, Dann M. Development of the University of Pennsylvania Smell Identification Test: a standardized microencapsulated test of olfactory function. Physiol Behav. 1984;32(3):489-502. doi:10.1016/0031-9384(84)90269-5
57. Kern DW, Wroblewski KE, Schumm LP, Pinto JM, Chen RC, McClintock MK. Olfactory function in Wave 2 of the National Social Life, Health, and Aging Project. J Gerontol B Psychol Sci Soc Sci. 2014;69(suppl 2):S134-S143. doi:10.1093/geronb/gbu093
58. Schubert CR, Cruickshanks KJ, Fischer ME, Klein BE, Klein R, Pinto AA. Inflammatory and vascular markers and olfactory impairment in older adults. Age Ageing. 2015;44(5):878-882. doi:10.1093/ageing/afv075
59. Li W, Lopez L, Osher J, Howard JD, Parrish TB, Gottfried JA. Right orbitofrontal cortex mediates conscious olfactory perception. Psychol Sci. 2010;21(10):1454-1463. doi:10.1177/0956797610382121
60. Kareken DA, Sabri M, Radnovich AJ, et al. Olfactory system activation from sniffing: effects in piriform and orbitofrontal cortex. Neuroimage. 2004;22(1):456-465. doi:10.1016/j.neuroimage.2004.01.008
61. Sobel N, Prabhakaran V, Desmond JE, et al. Sniffing and smelling: separate subsystems in the human olfactory cortex. Nature. 1998;392(6673):282-286. doi:10.1038/32654
62. Craik FIM, Salthouse TA. The Handbook of Aging and Cognition. 2nd ed. Mahwah, NJ: Lawrence Erlbaum Associates; 2000:ix, 755.
63. Swan GE, Carmelli D. Impaired olfaction predicts cognitive decline in nondemented older adults. Neuroepidemiology. 2002;21(2):58-67. doi:10.1159/000048618
64. Royall DR, Chiodo LK, Polk MS, Jaramillo CJ. Severe dysosmia is specifically associated with Alzheimer-like memory deficits in nondemented elderly retirees. Neuroepidemiology. 2002;21(2):68-73. doi:10.1159/000048619