Respiratory and sniffing behaviors throughout adulthood and aging in mice

Behavioural Brain Research

Volumn 223, Issue 1, 2011, Pages 99-106

  Wesson, Daniel W ^a,b   Varga Wesson, Adrienn G ^a   Borkowski, Anne H ^a   Wilson, Donald A ^a,b  

^a NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Amyloid beta; APP; Neurodegeneration; Olfaction; Orienting; Respiration

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN;

ADULTHOOD; AGE; AGING; AMYLOID PRECURSOR PROTEIN GENE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BODY PLETHYSMOGRAPHY; BREATHING; CONTROLLED STUDY; EVOKED RESPONSE; GENE; GENE MUTATION; HABITUATION; MOTOR SYSTEM; MOUSE; NONHUMAN; ODOR; OLFACTORY SYSTEM; PRIORITY JOURNAL; SNIFFING; WILD TYPE;

AGE FACTORS; AGING; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; HABITUATION, PSYCHOPHYSIOLOGIC; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ODORS; PLETHYSMOGRAPHY; RESPIRATION; SPACE PERCEPTION;

EID: 79955961527     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.04.016     Document Type: Article

References (57)

1. Pavlov I.P. Conditioned reflexes: an investigation of the physiological activity of the cerebral cortex 1927, Oxford University Press, London.
2. Sokolov E.N., Vinogradova O.S. Neuronal mechanisms of the orienting reflex 1975, L. Erlbaum Associates (distributed by the Halsted Press Division of Wiley), Hillsdale, N.J.
3. Wesson D.W., Donahou T.N., Johnson M.O., Wachowiak M. Sniffing behavior of mice during performance in odor-guided tasks. Chem Senses 2008, 33:581-596.
4. Kepecs A., Uchida N., Mainen Z.F. Rapid and precise control of sniffing during olfactory discrimination in rats. J Neurophysiol 2007, 98:205-213.
5. Youngentob S.L., Mozell M.M., Sheehe P.R., Hornung D.E. A quantitative analysis of sniffing strategies in rats performing odor discrimination tasks. Physiol Behav 1987, 41:59-69.
6. Verhagen J.V., Wesson D.W., Netoff T.I., White J.A., Wachowiak M. Sniffing controls an adaptive filter of sensory input to the olfactory bulb. Nat Neurosci 2007, 10:631-639.
7. Welker W.I. Analysis of sniffing in the albino rat. Behavior 1964, 22:223-244.
8. Sundberg H., Doving K., Novikov S., Ursin H. A method for studying responses and habituation to odors in rats. Behav Neural Biol 1982, 34:113-119.
9. Wesson D.W., Carey R.M., Verhagen J.V., Wachowiak M. Rapid encoding and perception of novel odors in the rat. PLoS Biol 2008, 6:e82.
10. Rinberg D., Koulakov A., Gelperin A. Speed-accuracy tradeoff in olfaction. Neuron 2006, 51:351-358.
11. Abraham N.M., Spors H., Carleton A., Margrie T.W., Kuner T., Schaefer A.T. Maintaining accuracy at the expense of speed: stimulus similarity defines odor discrimination time in mice. Neuron 2004, 44:865-876.
12. Slotnick B. Odor-sampling time of mice under different conditions. Chem Senses 2007, 32:445-454.
13. Uchida N., Mainen Z.F. Speed and accuracy of olfactory discrimination in the rat. Nat Neurosci 2003, 6:1224-1229.
14. Doty R.L., Shaman P., Applebaum S.L., Giberson R., Sikorski L., Rosenberg L. Smell identification ability: changes with age. Science 1984, 226:1441-1443.
15. Mesholam R.I., Moberg P.J., Mahr R.N., Doty R.L. Olfaction in neurodegenerative disease: a meta-analysis of olfactory functioning in Alzheimer's and Parkinson's diseases. Arch Neurol 1998, 55:84-90.
16. Murphy C. Loss of olfactory function in dementing disease. Physiol Behav 1999, 66:177-182.
17. Herrup K. Reimagining Alzheimer's disease-an age-based hypothesis. J Neurosci 2010, 30:16755-16762.
18. Andrews-Hanna J.R., Snyder A.Z., Vincent J.L., Lustig C., Head D., Raichle Marcus E., et al. Disruption of large-scale brain systems in advanced aging. Neuron 2007, 56:924-935.
19. Sperling R., Laviolette P., O'Keefe K., O'Brien J., Rentz D., Pihlajamaki M., et al. Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron 2009, 63:178-188.
20. Knupfer L., Spiegel R. Differences in olfactory test performance between normal aged Alzheimer and vascular type dementia individuals. Int J Geriatr Psych 1986, 1:3-14.
21. 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.
22. Montgomery KS, Simmons RK, Edwards Iii G, Nicolle MM, Gluck MA, Myers CE, et al. Novel age-dependent learning deficits in a mouse model of Alzheimer's disease: implications for translational research. Neurobiol Aging; in press.
23. Schoenbaum G., Nugent S., Saddoris M.P., Gallagher M. Teaching old rats new tricks: age-related impairments in olfactory reversal learning. Neurobiol Aging 2002, 23:555-564.
24. Guérin D., Sacquet J., Mandairon N., Jourdan F., Didier A. Early locus coeruleus degeneration and olfactory dysfunctions in Tg2576 mice. Neurobiol Aging 2009, 30:272-283.
25. Wesson D.W., Levy E., Nixon R.A., Wilson D.A. Olfactory dysfunction correlates with β-amyloid plaque burden in an Alzheimer's disease mouse model. J Neurosci 2010, 30:505-514.
26. Sobel N., Thomason M.E., Stappen I., Tanner C.M., Tetrud J.W., Bower J.M., et al. An impairment in sniffing contributes to the olfactory impairment in Parkinson's disease. Proc Natl Acad Sci U.S.A. 2001, 98:4154-4159.
27. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., et al. Correlative memory deficits, abeta elevation, and amyloid plaques in transgenic mice. Science 1996, 274:99-102.
28. Cleland T.A., Morse A., Yue E.L., Linster C. Behavioral models of odor similarity. Behav Neurosci 2002, 116:222-231.
29. Laing D.G., Francis G.W. The capacity of humans to identify odors in mixtures. Physiol Behav 1989, 46:809-814.
30. Kadohisa M., Wilson D.A. Separate encoding of identity and similarity of complex familiar odors in piriform cortex. Proc Natl Acad Sci U.S.A. 2006, 103:15206-15211.
31. Rankin C.H., Abrams T., Barry R.J., Bhatnagar S., Clayton D.F., Colombo J., et al. Habituation revisited: an updated and revised description of the behavioral characteristics of habituation. Neurobiol Learn Mem 2009, 92:135-138.
32. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991, 82:239-259.
33. Wesson DW, Nixon RA, Levy E, Wilson DA. Mechanisms of neural and behavioral dysfunction in Alzheimer's disease. Mol Neurobiol; in press.
34. Palop J.J., Mucke L. Amyloid-[beta]-induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks. Nat Neurosci 2010, 13:812-818.
35. Carey R.M., Verhagen J.V., Wesson D.W., Pirez N., Wachowiak M. Temporal structure of receptor neuron input to the olfactory bulb imaged in behaving rats. J Neurophysiol 2009, 101:1073-1088.
36. Wachowiak M. Active sensing in olfaction. The neurobiology of olfaction. CRC Press 2009, pp. 305-328.
37. Mainland J., Sobel N. The sniff is part of the olfactory percept. Chem Senses 2006, 31:181-196.
38. Laing D.G. Natural sniffing gives optimum odour perception for humans. Perception 1983, 12:99-117.
39. Wesson D.W., Verhagen J.V., Wachowiak M. Why sniff fast? The relationship between sniff frequency odor discrimination, and receptor neuron activation in the rat. J Neurophysiol 2009, 101:1089-1102.
40. Cury K.M., Uchida N. Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 2010, 68:570-585.
41. Bathellier B., Buhl D.L., Accolla R., Carleton A. Dynamic ensemble odor coding in the mammalian olfactory bulb: sensory information at different timescales. Neuron 2008, 57:586-598.
42. Uchida N., Kepecs A., Mainen Z.F. Seeing at a glance, smelling in a whiff: rapid forms of perceptual decision making. Nat Rev Neurosci 2006, 7:485-491.
43. Nakayasu C., Kanemura F., Hirano Y., Shimizu Y., Tonosaki K. Sensitivity of the olfactory sense declines with the aging in senescence-accelerated mouse (SAM-P1). Physiol Behavior 2000, 70:135-139.
44. Apfelbach R., Russ D., Slotnick B. Ontogenetic changes in odor sensitivity, olfactory receptor area and olfactory receptor density in the rat. Chem Senses 1991, 16:209-218.
45. Patel R.C., Larson J. Impaired olfactory discrimination learning and decreased olfactory sensitivity in aged C57Bl/6 mice. Neurobiol Aging 2009, 30:829-837.
46. Mandairon N, Peace ST, Boudadi K, Boxhorn CE, Narla VA, Suffis SD, et al. Compensatory responses to age-related decline in odor quality acuity: cholinergic neuromodulation and olfactory enrichment. Neurobiol. Aging; in press.
47. Rui D.S.P., Luciano C.B., Reinaldo N.T. Caffeine reverses age-related deficits in olfactory discrimination and social recognition memory in rats: Involvement of adenosine A1 and A2A receptors. Neurobiol Aging 2005, 26:957-964.
48. Gilbert P.E., Pirogovsky E., Brushfield A., Luu T.T., Tolentino J., Renteria A. Age-related changes in associative learning for olfactory and visual stimuli in rodents. Ann NY Acad Sci 2009, 1170:718-724.
49. LaSarge C., Montgomery K., Tucker C., Slaton G.S., Griffith W., Setlow B., et al. Deficits across multiple cognitive domains in a subset of aged Fischer 344 rats. Neurobiol Aging 2007, 28:928-936.
50. Li W., Howard J.D., Gottfried J.A. Disruption of odour quality coding in piriform cortex mediates olfactory deficits in Alzheimer's disease. Brain 2010, 133:2714-2726.
51. Wattendorf E., Welge-Lussen A., Fiedler K., Bilecen D., Wolfensberger M., Fuhr P., et al. Olfactory impairment predicts brain atrophy in Parkinson's disease. J Neurosci 2009, 29:15410-15413.
52. Moessnang C., Frank G., Bogdahn U., Winkler J., Greenlee M.W., Klucken J. Altered activation patterns within the olfactory network in Parkinson's disease. Cereb Cortex 2011, Epub ahead of print.
53. Seelke A.M., Blumberg M.A. Sniffing in infant rats during sleep and wakefulness. Behav Neurosci 2004, 118:267-273.
54. Wesson D.W., Keller M., Douhard Q., Baum M.J., Bakker J. Enhanced urinary odor discrimination in female aromatase knockout (ArKO) mice. Horm Behav 2006, 49:580-586.
55. Sorwell K.G., Wesson D.W., Baum M.J. Sexually dimorphic enhancement by estradiol of male urinary odor detection thresholds in mice. Behav Neurosci 2008, 122:788-793.
56. Dalton P., Doolittle N., Breslin P.A. Gender-specific induction of enhanced sensitivity to odors. Nat Neurosci 2002, 5:199-200.
57. Good P.R., Geary N., Engen T. The effect of estrogen on odor detection. Chem Senses Flavor 1976, 2:45-50.