Age-associated loss of selectivity in human olfactory sensory neurons

Neurobiology of Aging

Volumn 33, Issue 9, 2012, Pages 1913-1919

  Rawson, Nancy E ^a,b   Gomez, George ^c   Cowart, Beverly J ^a,d   Kriete, Andres ^a,e   Pribitkin, Edmund ^a,d   Restrepo, Diego ^f  

^a MONELL CHEMICAL SENSES CENTER   (United States)

^b AFB International   (United States)

^c UNIVERSITY OF SCRANTON   (United States)

^d THOMAS JEFFERSON UNIVERSITY   (United States)

^e DREXEL UNIVERSITY   (United States)

^f UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Age related odor impairment; Intracellular calcium; Odor thresholds; Olfactory epithelium; Olfactory sensory neurons

Indexed keywords

ADULT; AGED; AGING; ARTICLE; CALCIUM CELL LEVEL; CELL FUNCTION; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MOLECULAR IMAGING; NERVE CELL STIMULATION; OLFACTORY DISCRIMINATION; PERCEPTIVE THRESHOLD; PRIORITY JOURNAL; SENSORY NERVE CELL; SMELLING DISORDER;

ADULT; AGED; AGED, 80 AND OVER; AGING; CALCIUM; CROSS-SECTIONAL STUDIES; DISCRIMINATION (PSYCHOLOGY); FEMALE; FURA-2; HUMANS; MALE; MIDDLE AGED; ODORS; OLFACTORY MUCOSA; OLFACTORY RECEPTOR NEURONS; SENSORY THRESHOLDS; STATISTICS, NONPARAMETRIC; YOUNG ADULT;

EID: 84863434140     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2011.09.036     Document Type: Article

References (48)

1. Araki T., Kato H., Fujiwara T., Itoyama Y. Age-related changes in bindings of second messengers in the rat brain. Brain Res 1995, 704:227-232.
2. Aschenbrenner K., Hummel C., Teszmer K., Krone F., Ishimaru T., Seo H.S., Hummel T. The influence of olfactory loss on dietary behaviors. Laryngoscope 2008, 118:135-144.
3. Bahar R., Hartmann C.H., Rodriguez K.A., Denny A.D., Busuttil R.A., Dollé M.E., Calder R.B., Chisholm G.B., Pollock B.H., Klein C.A., Vijg J. Increased cell-to-cell variation in gene expression in ageing mouse heart. Nature 2006, 441:1011-1014.
4. Buchholz J.N., Behringer E.J., Pottorf W.J., Pearce W.J., Vanterpool C.K. Age-dependent changes in Ca2+ homeostasis in peripheral neurones: implications for changes in function. Aging Cell 2007, 6:285-296.
5. Chen Y., Getchell T.V., Sparks D.L., Getchell M.L. Patterns of adrenergic and peptidergic innervation in human olfactory mucosa: age-related trends. J. Comp. Neurol 1993, 334:104-116.
6. Chess A., Simon I., Cedar H., Axel R. Allelic inactivation regulates olfactory receptor gene expression. Cell 1994, 78:823-834.
7. Costanzo R.M., Kobayashi M. Age-related changes in p2 odorant receptor mapping in the olfactory bulb. Chem. Sens 2010, 35:417-426.
8. Cowart B.J. Relationships between taste and smell across the adult life span. Ann. N. Y. Acad. Sci 1989, 561:39-55.
9. Doty R.L., Deems D.A., Stellar S. Olfactory dysfunction in parkinsonism: a general deficit unrelated to neurologic signs, disease stage, or disease duration. Neurology 1988, 38:1237-1244.
10. Doty R.L., Shaman P., Applebaum S.L., Giberson R., Siksorski L., Rosenberg L. Smell identification ability: changes with age. Science 1984, 226:1441-1443.
11. Enwere E., Shingo T., Gregg C., Fujikawa H., Ohta S., Weiss S. Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J. Neurosci 2004, 24:8354-8365.
12. Evans W.J., Cui L., Starr A. Olfactory event-related potentials in normal human subjects: effects of age and gender. Electroencephalogr. Clin. Neurophysiol 1995, 95:293-301.
13. Graves A.B., Bowen J.D., Rajaram L., McCormick W.C., McCurry S.M., Schellenberg G.D., Larson E.B. Impaired olfaction as a marker for cognitive decline: interaction with apolipoprotein E epsilon4 status. Neurology 1999, 53:1480-1487.
14. Herman J.P., Chen K.C., Booze R., Landfield P.W. Up-regulation of alpha1D Ca2+ channel subunit mRNA expression in the hippocampus of aged F344 rats. Neurobiol. Aging 1998, 19:581-587.
15. Hirai T., Kojima S., Shimada A., Umemura T., Sakai M., Itakura C. Age-related changes in the olfactory system of dogs. Neuropathol. Appl. Neurobiol 1996, 22:531-539.
16. 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, 264:237-243.
17. 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. Sens 2000, 25:331-337.
18. Kerr M.A., Belluscio L. Olfactory experience accelerates glomerular refinement in the mammalian olfactory bulb. Nat. Neurosci 2006, 9:484-486.
19. Lee A.C., He J., Ma M. Olfactory marker protein is critical for functional maturation of olfactory sensory neurons and development of mother preference. J. Neurosci 2011, 31:2974-2982.
20. Lee A.C., Tian H., Grosmaitre X., Ma M. Expression patterns of odorant receptors and response properties of olfactory sensory neurons in aged mice. Chem. Sens 2009, 34:695-703.
21. Loo A.T., Youngentob S.L., Kent P.F., Schwob J.E. The aging olfactory epithelium: neurogenesis, response to damage, and odorant-induced activity. Int. J. Dev. Neurosci 1996, 14:881-900.
22. Lowry L.D., Pribitkin E.A. Collection of human olfactory tissue. Experimental Cell Biology of Taste and Olfaction 1995, 47-48. CRC Press, Boca Raton. A. Spielman (Ed.).
23. Maresh A., Rodriguez Gil D., Whitman M.C., Greer C.A. Principles of glomerular organization in the human olfactory bulb-implications for odor processing. PLoS One 2008, 3:e2640.
24. Mattes R.D., Cowart B.J. Dietary assessment of patients with chemosensory disorders. J. Am. Diet. Assoc 1994, 94:50-56.
25. Meisami E., Mikhail L., Baim D., Bhatnagar K.P. Human olfactory bulb: aging of glomeruli and mitral cells and a search for the accessory olfactory bulb. Ann. N. Y. Acad. Sci 1998, 855:708-715.
26. Mirich J.M., Williams N.C., Berlau D.J., Brunjes P.C. Comparative study of aging in the mouse olfactory bulb. J. Comp. Neurol 2002, 454:361-372.
27. Mombaerts P. Axonal wiring in the mouse olfactory system. Annu. Rev. Cell Dev. Biol 2006, 22:713-737.
28. Morrison E.E., Costanzo R.M. Morphology of the human olfactory epithelium. J. Comp. Neurol 1990, 297:1-13.
29. Murphy C. The chemical senses and nutrition in older adults. J. Nutr. Elder 2008, 27:247-265.
30. Murphy C., Wetter S., Morgan C.D., Ellison D.W., Geisler M.W. Age effects on central nervous system activity reflected in the olfactory event-related potential. Evidence for decline in middle age. Ann. N. Y. Acad. Sci 1998, 855:598-607.
31. Nakashima T., Kimmelman C.P., Snow J.B. Structure of human fetal and adult olfactory neuroepithelium. Arch. Otolaryngol 1984, 110:641-646.
32. Oliva A.M., Jones K.R., Restrepo D. Sensory-dependent asymmetry for a urine-responsive olfactory bulb glomerulus. J. Comp. Neurol 2008, 510:475-483.
33. Paik S.I., Lehman M.N., Seiden A.M., Duncan H.J., Smith D.V. Human olfactory biopsy. The influence of age and receptor distribution. Arch. Otolaryngol. Head Neck Surg 1992, 118:731-738.
34. Rawson N.E., Brand J.G., Cowart B.J., Lowry L.D., Pribitkin E.A., Rao V.M., Restrepo D. Functionally mature olfactory neurons from two anosmic patients with Kallmann syndrome. Brain Res 1995, 681:58-64.
35. Rawson N.E., Gomez G., Cowart B., Brand J.G., Lowry L.D., Pribitkin E.A., Restrepo D. Selectivity and response characteristics of human olfactory neurons. J. Neurophysiol 1997, 77:1606-1613.
36. Richard M.B., Taylor S.R., Greer C.A. Age-induced disruption of selective olfactory bulb synaptic circuits. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:15613-15618.
37. Rolls B.J. Do chemosensory changes influence food intake in the elderly?. Physiol. Behav 1999, 66:193-197.
38. Santos D.V., Reiter E.R., DiNardo L.J., Costanzo R.M. Hazardous events associated with impaired olfactory function. Arch. Otolaryngol. Head Neck Surg 2004, 130:317-319.
39. Schiffman S.S. Taste and smell losses in normal aging and disease. JAMA 1997, 278:1357-1362.
40. Stevens J.C., Cain W.S., Schiet F.T., Oatley M.W. Olfactory adaptation and recovery in old age. Perception 1989, 18:265-276.
41. Sugawa M., May T. Age-related alteration in signal transduction: involvement of the cAMP cascade. Brain Res 1993, 618:57-62.
42. Tanaka Y., Ando S. Age-related changes in the subtypes of voltage-dependent calcium channels in rat brain cortical synapses. Neurosci. Res 2001, 39:213-220.
43. Thibault O., Hadley R., Landfield P.W. Elevated postsynaptic [Ca2+]i and L-type calcium channel activity in aged hippocampal neurons: relationship to impaired synaptic plasticity. J. Neurosci 2001, 21:9744-9756.
44. Weiler E., Farbman A.I. Proliferation in the rat olfactory epithelium: age-dependent changes. J. Neurosci 1997, 17:3610-3622.
45. Wilson R.S., Schneider J.A., Arnold S.E., Tang Y., Boyle P.A., Bennett D.A. Olfactory identification and incidence of mild cognitive impairment in older age. Arch. Gen. Psychiatry 2007, 64:802-808.
46. 2+]i signalling in rat cerebellar granule neurones aged in vitro. Neurobiol. Aging 2004, 25:349-359.
47. Yi M., Weaver D., Hajnóczky G. Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J. Cell Biol 2004, 167:661-672.
48. Zou D.J., Feinstein P., Rivers A.L., Mathews G.A., Kim A., Greer C.A., Mombaerts P., Firestein S. Postnatal refinement of peripheral olfactory projections. Science 2004, 304:1976-1979.