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Effect of Worry Level on Recall Memory for Odors in ApoE-ε4 Carriers and Non-Carriers

Published online by Cambridge University Press:  16 April 2019

Emily S. Bower ,
Jacquelyn Szajer  and
Claire Murphy
Emily S. Bower
Affiliation:
Department of Psychology, San Diego State University, San Diego, California 92182, USA SDSU/UCSD Joint Doctoral Program in Clinical Psychology, San Diego, California 92120, USA
Jacquelyn Szajer
Affiliation:
SDSU/UCSD Joint Doctoral Program in Clinical Psychology, San Diego, California 92120, USA
Claire Murphy*
Affiliation:
Department of Psychology, San Diego State University, San Diego, California 92182, USA SDSU/UCSD Joint Doctoral Program in Clinical Psychology, San Diego, California 92120, USA Department of Psychiatry, University of California San Diego School of Medicine, San Diego, California 92093, USA
*
*Correspondence and reprint requests to: Claire Murphy, Department of Psychology, San Diego State University, SDSU/UCSD Joint Doctoral Program in Clinical Psychology, 6363 Alvarado Court, San Diego, CA 92120-4913. E-mail: [email protected]
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Abstract

Objective: Increased levels of worry, age, and presence of the apolipoprotein-E (ApoE)-ε4 allele are associated with the risk of developing cognitive declines and Alzheimer’s disease (AD). Odor memory performance has been shown to vary as a function of age and ApoE genotype, and odor memory tests are sensitive to preclinical AD. Worry is known to influence verbal memory; however, its effects on odor memory are unknown. This study aimed to assess the relationships between worry, age, and ε4 status on odor memory. Method: Worry was evaluated for young (n = 53) and older (n = 45) adults using the Penn State Worry Questionnaire. Odor memory was assessed using the California Odor Learning Test, an olfactory analogue to the California Verbal Learning Test. Results: A significant main effect of worry on long-delay free recall was found, such that increasing worry was associated with better recall across age and ε4 status. A significant interaction effect between ε4 status and worry on both short-and long-delay cued recall was found, such that across age, higher worry was associated with increased cued recall scores among ε4-negative adults, and decreased scores among ε4-positive adults. Conclusions: Findings demonstrated that worry influences odor memory and exerts a particular effect on cued recall among ε4 carriers who are at a greater risk of developing AD. Worry is a modifiable predictor of cognitive decline and risk of dementia in aging. Future studies on the effects of treatments aimed at reducing worry (e.g., cognitive behavioral therapies for anxiety) on changes in cognitive functioning are warranted.

Keywords

Worryapolipoprotein geneagingodor memorycued recallfree recall
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 25 , Issue 5 , May 2019 , pp. 546 - 556
Copyright
Copyright © The International Neuropsychological Society 2019 

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Footnotes

Current address for Emily S. Bower: VISN 2 Center of Excellence for Suicide Prevention, Canandaigua VA Medical Center, Canandaigua, NY; and Department of Psychiatry, University of Rochester Medical Center, Rochester, NY

References

REFERENCES

Albers, M.W., Gilmore, G.C., Kaye, J., Murphy, C., Wingfield, A., Bennett, D.A., Boxer, A.L., Buchman, A.S., Cruickshanks, K.J., Devanand, D.P., & Zang, L.I. (2015). At the interface of sensory and motor dysfunctions and Alzheimer’s disease. Alzheimer’s & Dementia, 11, 70–98.CrossRefGoogle ScholarPubMed
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington, VA: American Psychiatric Publishing.Google Scholar
Arnsten, A.F. (2009). Stress signalling pathways that impair prefrontal cortex structure and function. Nature Reviews Neuroscience, 10(6), 410–422. doi: 10.1038/nrn2648 Google Scholar
Bannerman, D.M., Rawlins, J.N.P., McHugh, S.B., Deacon, R.M.J., Yee, B.K., Bast, T., Zhang, W.N., Pothuizen, H.H.J., & Feldon, J. (2004). Regional dissociations within the hippocampus – Memory and anxiety. Neuroscience and Biobehavioral Reviews, 28(3), 273–283. doi: 10.1016/j.neubiorev.2004.03.004 CrossRefGoogle ScholarPubMed
Beaudreau, S.A., Hantke, N.C., Mashal, N., Gould, C.E., Henderson, V.W., & O’Hara, R. (2017). Unlocking neurocognitive substrates of late-life affective symptoms using the Research Domain Criteria: Worry is an essential dimension. Frontiers in Aging Neuroscience, 9, 380.CrossRefGoogle ScholarPubMed
Beck, A.T., Steer, R.A., & Brown, G.K. (1996). Manual for the Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation.Google Scholar
Beck, J.G., Stanley, M.A., & Zebb, B.J. (1995). Psychometric properties of the Penn State Worry Questionnaire in older adults. Journal of Clinical Geropsychology, 1(1), 33–42.Google Scholar
Bekris, L.M., Yu, C.-E., Bird, T.D., & Tsuang, D.W. (2010). Genetics of Alzheimer disease. Journal of Geriatric Psychiatry and Neurology, 23(4), 213–227. doi: 10.1177/0891988710383571 CrossRefGoogle ScholarPubMed
Benarroch, E.E. (2010). Olfactory system: Functional organization and involvement in neurodegenerative disease. Neurology, 75(12), 1104–1109. doi: 10.1212/WNL.0b013e3181f3db84 CrossRefGoogle ScholarPubMed
Bird, T.D. (2008). Genetic aspects of Alzheimer disease. Genetics in Medicine: Official Journal of the American College of Medical Genetics, 10(4), 231–239. doi: 10.1097/GIM.0b013e31816b64dc CrossRefGoogle ScholarPubMed
Braak, H. & Braak, E. (1991). Neuropathological stageing of Alzheimer-related changes. Acta Neuropathologica, 82(4), 239–259. doi: 10.1007/BF00308809 CrossRefGoogle ScholarPubMed
Braam, A.W., Copeland, J.R.M., Delespaul, P.A.E.G., Beekman, A.T.F., Como, A., Dewey, M., Fichter, M., Holwerda, T.J., Lawlor, B.A., Lobo, A., & Skoog, I. (2014). Depression, subthreshold depression and comorbid anxiety symptoms in older Europeans: Results from the EURODEP concerted action. Journal of Affective Disorders, 155, 266–272. doi: 10.1016/j.jad.2013.11.011 CrossRefGoogle ScholarPubMed
Brown, T.A., Antony, M.M., & Barlow, D.H. (1992). Psychometric properties of the Penn State Worry Questionnaire in a clinical anxiety disorders sample. Behaviour Research and Therapy, 30(1), 33–37.CrossRefGoogle Scholar
Buckner, R.L., Snyder, A.Z., Shannon, B.J., LaRossa, G., Sachs, R., Fotenos, A.F., Sheline, Y.I., Klunk, W.E., Mathis, C.A., Morris, J.C., & Mintun, M.A. (2005). Molecular, structural, and functional characterization of Alzheimer‘s disease: Evidence for a relationship between default activity, amyloid, and memory. Journal of Neuroscience, 25(34), 7709–7717. doi: 10.1523/JNEUROSCI.2177-05.2005 CrossRefGoogle Scholar
Calhoun-Haney, R. & Murphy, C. (2005). Apolipoprotein epsilon4 is associated with more rapid decline in odor identification than in odor threshold or Dementia Rating Scale scores. Brain and Cognition, 58(2), 178–182. doi: 10.1016/j.bandc.2004.10.004 CrossRefGoogle ScholarPubMed
Canteras, N.S., Resstel, L.B., Bertoglio, L.J., Carobrez, A.P., & Guimarães, F.S. (2010). Neuroanatomy of anxiety. Current Topics in Behavioral Neurosciences, 2, 77–96.CrossRefGoogle ScholarPubMed
Carstensen, L.L., Turan, B., Scheibe, S., Ram, N., Ersner-Hershfield, H., Samanez-Larkin, G.R., Brooks, K.P., & Nesselroade, J. R. (2011). Emotional experience improves with age: evidence based on over 10 years of experience sampling. Psychology and Aging, 26(1), 21–33. doi: 10.1037/a0021285 CrossRefGoogle Scholar
Caselli, R.J., Reiman, E.M., Hentz, J.G., Osborne, D., & Alexander, G.E. (2004). A distinctive interaction between chronic anxiety and problem solving in asymptomatic APOE e4 homozygotes. The Journal of Neuropsychiatry and Clinical Neurosciences, 16(3), 320–329. doi: 10.1176/jnp.16.3.320 CrossRefGoogle ScholarPubMed
Cerf-Ducastel, B., Haase, L., & Murphy, C. (2012). Effect of magnitude estimation of pleasantness and intensity on fMRI activation to taste. Chemosensory Perception, 5(1), 100–109. doi: 10.1007/s12078-011-9109-1 CrossRefGoogle Scholar
Cerf-Ducastel, B. & Murphy, C. (2001). fMRI activation in response to odorants orally delivered in aqueous solutions. Chemical Senses, 26(6), 625–637.CrossRefGoogle ScholarPubMed
Christen-Zaech, S., Kraftsik, R., Pillevuit, O., Kiraly, M., Martins, R., Khalili, K., & Miklossy, J. (2003). Early olfactory involvement in Alzheimer’s disease. The Canadian Journal of Neurological Sciences. Le Journal Canadien Des Sciences Neurologiques, 30(1), 20–25.CrossRefGoogle ScholarPubMed
Cortese, B.M., Leslie, K., & Uhde, T.W. (2015). Differential odor sensitivity in PTSD: Implications for treatment and future research. Journal of Affective Disorders, 179, 23–30. doi: 10.1016/j.jad.2015.03.026 CrossRefGoogle ScholarPubMed
Crittendon, J. & Hopko, D.R. (2006). Assessing worry in older and younger adults: Psychometric properties of an abbreviated Penn State Worry Questionnaire (PSWQ-A). Journal of Anxiety Disorders, 20(8), 1036–1054. doi: 10.1016/j.janxdis.2005.11.006 CrossRefGoogle Scholar
Delis, D.C., Kramer, J.H., Kaplan, E.F., & Ober, B.A. (1987). California verbal learning test. San Antonio, TX: The Psychological Corporation.Google Scholar
Dierckx, E., Engelborghs, S., De Raedt, R., De Deyn, P.P., & Ponjaert-Kristoffersen, I. (2007). Differentiation between mild cognitive impairment, Alzheimer’s disease and depression by means of cued recall. Psychological Medicine, 37(5), 747–755. doi: 10.1017/S003329170600955X CrossRefGoogle ScholarPubMed
Dierckx, E., Engelborghs, S., De Raedt, R., Van Buggenhout, M., De Deyn, P.P., Verté, D., & Ponjaert-Kristoffersen, I. (2009). Verbal cued recall as a predictor of conversion to Alzheimer’s disease in mild cognitive impairment. International Journal of Geriatric Psychiatry, 24(10), 1094–1100. doi: 10.1002/gps.2228 CrossRefGoogle ScholarPubMed
Djordjevic, J., Jones-Gotman, M., De Sousa, K., & Chertkow, H. (2008). Olfaction in patients with mild cognitive impairment and Alzheimer’s disease. Neurobiology of Aging, 29(5), 693–706. doi: 10.1016/j.neurobiolaging.2006.11.014 CrossRefGoogle ScholarPubMed
Eysenck, M.W. & Calvo, M.G. (1992). Anxiety and performance: The processing efficiency theory. Cognition and Emotion, 6, 409–434.CrossRefGoogle Scholar
Fernández, G., Brewer, J.B., Zhao, Z., Glover, G.H., & Gabrieli, J.D. (1999). Level of sustained entorhinal activity at study correlates with subsequent cued-recall performance: A functional magnetic resonance imaging study with high acquisition rate. Hippocampus, 9(1), 35–44. doi: 10.1002/(SICI)1098-1063(1999)9:1<35::AID-HIPO4>3.0.CO;2-Z 3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
Finkel, D., Reynolds, C.A., Larsson, M., Gatz, M., & Pedersen, N.L. (2011). Both odor identification and ApoE-ε4 contribute to normative cognitive aging. Psychology and Aging, 26(4), 872–883. doi: 10.1037/a0023371 CrossRefGoogle ScholarPubMed
Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189–198.CrossRefGoogle ScholarPubMed
Forster, S., Nunez Elizalde, A.O., Castle, E., & Bishop, S.J. (2015). Unraveling the anxious mind: Anxiety, worry, and frontal engagement in sustained attention versus off-task processing. Cerebral Cortex (New York, N.Y.: 1991), 25(3), 609–618. doi: 10.1093/cercor/bht248 CrossRefGoogle ScholarPubMed
Frasnelli, J., Lundström, J.N., Boyle, J.A., Djordjevic, J., Zatorre, R.J., & Jones-Gotman, M. (2010). Neuroanatomical correlates of olfactory performance. Experimental Brain Research, 201(1), 1–11. doi: 10.1007/s00221-009-1999-7 CrossRefGoogle ScholarPubMed
Fresco, D.M., Mennin, D.S., Heimberg, R.G., & Turk, C.L. (2003). Using the Penn State Worry Questionnaire to identify individuals with generalized anxiety disorder: A receiver operating characteristic analysis. Journal of Behavior Therapy and Experimental Psychiatry, 34(3–4), 283–291. doi: 10.1016/j.jbtep.2003.09.001 CrossRefGoogle ScholarPubMed
Galliot, E., Comte, A., Magnin, E., Tatu, L., Moulin, T., & Millot, J.-L. (2013). Effects of an ambient odor on brain activations during episodic retrieval of objects. Brain Imaging and Behavior, 7(2), 213–219. doi: 10.1007/s11682-012-9218-8 CrossRefGoogle Scholar
Gilbert, P.E. & Murphy, C. (2004). The effect of the ApoE epsilon4 allele on recognition memory for olfactory and visual stimuli in patients with pathologically confirmed Alzheimer’s disease, probable Alzheimer’s disease, and healthy elderly controls. Journal of Clinical and Experimental Neuropsychology, 26(6), 779–794. doi: 10.1080/13803390490509439 CrossRefGoogle ScholarPubMed
Grober, E. & Buschke, H. (1987). Genuine memory deficits in dementia. Developmental Neuropsychology, 3, 13–36.CrossRefGoogle Scholar
Haase, L., Wang, M., Green, E., & Murphy, C. (2013). Functional connectivity during recognition memory in individuals genetically at risk for Alzheimer’s disease. Human Brain Mapping, 34(3), 530–542.Google ScholarPubMed
Hayama, H.R., Vilberg, K.L., & Rugg, M.D. (2012). Overlap between the neural correlates of cued recall and source memory: Evidence for a generic recollection network? Journal of Cognitive Neuroscience, 24(5), 1127–1137. doi: 10.1162/jocn_a_00202 CrossRefGoogle Scholar
Heindel, W.C., Salmon, D.P., & Butters, N. (1990). Pictorial priming and cued recall in Alzheimer’s and Huntington’s disease. Brain and Cognition, 13(2), 282–295. doi: 10.1016/0278-2626(90)90053-Q CrossRefGoogle ScholarPubMed
Holmes, S.E., Esterlis, I., Mazure, C.M., Lim, Y.Y., Ames, D., Rainey-Smith, S., Martins, R.N., Salvado, O., Dore, V., Villemagne, V.L., & Australian Imaging, Biomarkers, Lifestyle Research Group. (2016). β-Amyloid, APOE and BDNF genotype, and depressive and anxiety symptoms in cognitively normal older women and men. The American Journal of Geriatric Psychiatry: Official Journal of the American Association for Geriatric Psychiatry, 24(12), 1191–1195. doi: 10.1016/j.jagp.2016.08.007 CrossRefGoogle ScholarPubMed
Hopko, D.R., Stanley, M.A., Reas, D.L., Wetherell, J.L., Beck, J.G., Novy, D.M., & Averill, P.M. (2003). Assessing worry in older adults: Confirmatory factor analysis of the Penn State Worry Questionnaire and psychometric properties of an abbreviated model. Psychological Assessment, 15(2), 173–183.CrossRefGoogle ScholarPubMed
Insel, T., Cuthbert, B., Garvey, M., Heinseen, R., Pine, D.S., Quinn, K., Sanislow, C., & Wang, P. (2010). Research domain criteria (RDoC): Toward a new classification framework for research on mental disorders. American Journal of Psychiatry, 167, 748–51.CrossRefGoogle Scholar
Josefsson, M., Larsson, M., Nordin, S., Adolfsson, R., & Olofsson, J. (2017). APOE-ε4 effects on longitudinal decline in olfactory and non-olfactory cognitive abilities in middle-aged and old adults. Scientific Reports, 7(1), 1286. doi: 10.1038/s41598-017-01508-7 CrossRefGoogle Scholar
Korte, K.J., Allan, N.P., & Schmidt, N.B. (2016). Factor mixture modeling of the Penn State Worry Questionnaire: Evidence for distinct classes of worry. Journal of Anxiety Disorders, 37, 40–47. doi: 10.1016/j.janxdis.2015.11.001 CrossRefGoogle Scholar
Larsson, M., Hedner, M., Papenberg, G., Seubert, J., Bäckman, L., & Laukka, E.J. (2016). Olfactory memory in the old and very old: Relations to episodic and semantic memory and APOE genotype. Neurobiology of Aging, 38, 118–126. doi: 10.1016/j.neurobiolaging.2015.11.012 CrossRefGoogle ScholarPubMed
Lee, B.K., Glass, T.A., Wand, G.S., McAtee, M.J., Bandeen-Roche, K., Bolla, K.I., & Schwartz, B.S. (2008). Apolipoprotein E genotype, cortisol, and cognitive function in community-dwelling older adults. American Journal of Psychiatry, 165(11), 1456–1464. doi: 10.1176/appi.ajp.2008.07091532 CrossRefGoogle ScholarPubMed
Lee, L.O. & Knight, B.G. (2009). Attentional bias for threat in older adults: Moderation of the positivity bias by trait anxiety and stimulus modality. Psychology and Aging, 24(3), 741–747. doi: 10.1037/a0016409 CrossRefGoogle ScholarPubMed
Lehn, H., Kjønigsen, L.J., Kjelvik, G., & Håberg, A.K. (2013). Hippocampal involvement in retrieval of odor vs. object memories. Hippocampus, 23(2), 122–128. doi: 10.1002/hipo.22073 CrossRefGoogle ScholarPubMed
Lehrner, J., Pusswald, G., Gleiss, A., Auff, E., & Dal-Bianco, P. (2009). Odor identification and self-reported olfactory functioning in patients with subtypes of mild cognitive impairment. The Clinical Neuropsychologist, 23(5), 818–830. doi: 10.1080/13854040802585030 CrossRefGoogle ScholarPubMed
Levy, D.A., Manns, J.R., Hopkins, R.O., Gold, J.J., & Squire, L.R. (2003). Impaired visual and odor recognition memory span in patients with hippocampal lesions. Learning & Memory, 10(6), 531–536. doi: 10.1101/lm.66703 CrossRefGoogle ScholarPubMed
Long, N.M., Oztekin, I., & Badre, D. (2010). Separable prefrontal cortex contributions to free recall. The Journal of Neroscience: The Official Journal of the Society for Neuroscience, 30(33), 10967–10976. doi: 10.1523/JNEUROSCI.2611-10.2010 Google ScholarPubMed
Lucas, J.A., Ivnik, R.J., Smith, G.E., Bohac, D.L., Tangalos, E.G., Kokmen, E., Graff-Radford, N.R., & Petersen, R.C. (1998). Normative data for the Mattis Dementia Rating Scale. Journal of Clinical and Experimental Neuropsychology, 20(4), 536–547. doi: 10.1076/jcen.20.4.536.1469 CrossRefGoogle Scholar
Machulda, M.M., Jones, D.T., Vemuri, P., McDade, E., Avula, R., Przybelski, S., Boeve, B.F., Knopman, D.S., Petersen, R.C., & Jack, C. R. (2011). Effect of APOE ε4 status on intrinsic network connectivity in cognitively normal elderly subjects. Archives of Neurology, 68(9), 1131–1136. doi: 10.1001/archneurol.2011.108 CrossRefGoogle Scholar
Mah, L., Szabuniewicz, C., & Fiocco, A.J. (2016). Can anxiety damage the brain? Current Opinion in Psychiatry, 29(1), 56–63. doi: 10.1097/YCO.0000000000000223 CrossRefGoogle Scholar
Meyer, T.J., Miller, M.L., Metzger, R.L., & Borkovec, T.D. (1990). Development and validation of the Penn State Worry Questionnaire. Behaviour Research and Therapy, 28(6), 487–495.CrossRefGoogle ScholarPubMed
Mondadori, C.R., de Quervain, D.J., Buchmann, A., Mustovic, H., Wollmer, M.A., Schmidt, C.F., Boesiger, P., Hock, C., Nitsch, R.M., Papassotiropoulos, A., & Henke, K. (2007). Better memory and neural efficiency in young apolipoprotein E epsilon 4 carriers. Cerebral Cortex, 17, 1934–1947.CrossRefGoogle Scholar
Murphy, C. (2019) Olfactory and other sensory impairments in Alzheimer’s disease. Nature Reviews Neurology, 15(1), 11–24. doi: 10.1038/s41582-018-0097-5 CrossRefGoogle Scholar
Murphy, C., Cerf-Ducastel, B., Calhoun-Haney, R., Gilbert, P.E., & Ferdon, S. (2005). ERP, fMRI and functional connectivity studies of brain response to odor in normal aging and Alzheimer’s disease. Chemical Senses, 30(Suppl 1), i170–i171. doi: 10.1093/chemse/bjh168 CrossRefGoogle ScholarPubMed
Murphy, C., Gilmore, M.M., Seery, C.S., Salmon, D.P., & Lasker, B.R. (1990). Olfactory thresholds are associated with degree of dementia in Alzheimer’s disease. Neurobiology of Aging, 11(4), 465–469.CrossRefGoogle ScholarPubMed
Murphy, C., Nordin, S., & Acosta, L. (1997). Odor learning, recall, and recognition memory in young and elderly adults. Neuropsychology, 11(1), 126–137. doi: 10.1037/0894-4105.11.1.126 CrossRefGoogle Scholar
Olofsson, J.K., Josefsson, M., Ekström, I., Wilson, D., Nyberg, L., Nordin, S., Adolfsson, A.N., Adolfsson, R., Nilsson, L.G., & Larsson, M. (2016). Long-term episodic memory decline is associated with olfactory deficits only in carriers of ApoE-ε4. Neuropsychologia, 85, 1–9. doi: 10.1016/j.neuropsychologia.2016.03.004 CrossRefGoogle Scholar
Ottaviani, C., Thayer, J.F., Verkuil, B., Lonigro, A., Medea, B., Couyoumdjian, A., & Brosschot, J.F. (2016). Physiological concomitants of perseverative cognition: A systematic review and meta-analysis. Psychological Bulletin, 142, 231–259. doi: 10.1037/bul0000036 CrossRefGoogle ScholarPubMed
Ottaviano, G., Frasson, G., Nardello, E., & Martini, A. (2016). Olfaction deterioration in cognitive disorders in the elderly. Aging Clinical and Experimental Research, 28(1), 37–45. doi: 10.1007/s40520-015-0380-x CrossRefGoogle ScholarPubMed
Palmer, K., Berger, A.K., Monastero, R., Winblad, B., Bäckman, L., & Fratiglioni, L. (2007). Predictors of progression from mild cognitive impairment to Alzheimer disease. Neurology, 68(19), 1596–1602. doi: 10.1212/01.wnl.0000260968.92345.3f CrossRefGoogle ScholarPubMed
Pardon, M.-C. (2007). Stress and ageing interactions: A paradox in the context of shared etiological and physiopathological processes. Brain Research Reviews, 54(2), 251–273. doi: 10.1016/j.brainresrev.2007.02.007 CrossRefGoogle ScholarPubMed
Pardon, M.C., & Rattray, I. (2008). What do we know about the long-term consequences of stress on ageing and the progression of age-related neurodegenerative disorders? Neuroscience & Biobehavioral Reviews, 32(6), 1103–1120. doi: 10.1016/j.neubiorev.2008.03.005 CrossRefGoogle Scholar
Peavy, G.M., Lange, K.L., Salmon, D.P., Patterson, T.L., Goldman, S., Gamst, A.C., Mills, P.J., Khandrika, S., & Galasko, D. (2007). The effects of prolonged stress and APOE genotype on memory and cortisol in older adults. Biological Psychiatry, 62(5), 472–478. doi: 10.1016/j.biopsych.2007.03.013 CrossRefGoogle ScholarPubMed
Pietrzak, R.H., Maruff, P., Woodward, M., Fredrickson, J., Fredrickson, A., Krystal, J.H., Southwick, S.M., & Darby, D. (2012). Mild worry symptoms predict decline in learning and memory in healthy older adults: A 2-year prospective cohort study. The American Journal of Geriatric Psychiatry, 20(3), 266–275. doi: 10.1097/JGP.0b013e3182107e24 CrossRefGoogle ScholarPubMed
Quarmley, M., Moberg, P.J., Mechanic-Hamilton, D., Kabadi, S., Arnold, S.E., Wolk, D.A., & Roalf, D.R. (2017). Odor identification screening improves diagnostic classification in incipient Alzheimer’s disease. Journal of Alzheimer’s Disease: JAD, 55(4), 1497–1507. doi: 10.3233/JAD-160842 CrossRefGoogle ScholarPubMed
Ruscio, A.M., Seitchik, A.E., Gentes, E.L., Jones, J.D., & Hallion, L.S. (2011). Perseverative thought: A robust predictor of response to emotional challenge in Generalized Anxiety Disorder and Major Depressive Disorder. Behaviour Research and Therapy, 49, 867–874.CrossRefGoogle ScholarPubMed
Saive, A.-L., Royet, J.-P., Ravel, N., Thévenet, M., Garcia, S., & Plailly, J. (2014). A unique memory process modulated by emotion underpins successful odor recognition and episodic retrieval in humans. Frontiers in Behavioral Neuroscience, 8. Retrieved from http://search.proquest.com/docview/1650980713?accountid=14524 CrossRefGoogle ScholarPubMed
Sapolsky, R.M. (1992). Stress, The Aging Brain, and the Mechanisms of Neuron Death. Cambridge, MA: The MIT Press.Google Scholar
Schubert, C.R., Carmichael, L.L., Murphy, C., Klein, B.E.K., Klein, R., & Cruickshanks, K.J. (2008). Olfaction and the 5-year incidence of cognitive impairment in an epidemiological study of older adults. Journal of the American Geriatrics Society, 56(8), 1517–1521. doi: 10.1111/j.1532-5415.2008.01826.x CrossRefGoogle Scholar
Smitka, M., Puschmann, S., Buschhueter, D., Gerber, J.C., Witt, M., Honeycutt, N., Abolmaali, N., & Hummel, T. (2012). Is there a correlation between hippocampus and amygdala volume and olfactory function in healthy subjects? NeuroImage, 59(2), 1052–1057. doi: 10.1016/j.neuroimage.2011.09.024 CrossRefGoogle Scholar
Soudry, Y., Lemogne, C., Malinvaud, D., Consoli, S.-M., & Bonfils, P. (2011). Olfactory system and emotion: Common substrates. European Annals of Otorhinolaryngology, Head and Neck Diseases, 128(1), 18–23. doi: 10.1016/j.anorl.2010.09.007 CrossRefGoogle ScholarPubMed
Stonnington, C.M., Locke, D.E., Dueck, A.C., & Caselli, R.J. (2011). Anxiety affects cognition differently in healthy apolipoprotein E ε4 homozygotes and non-carriers. The Journal of Neuropsychiatry and Clinical Neurosciences, 23(3), 294–299. doi: 10.1176/jnp.23.3.jnp294 CrossRefGoogle Scholar
Sullivan, R.M., Wilson, D.A., Ravel, N., & Mouly, A.-M. (2015). Olfactory memory networks: From emotional learning to social behaviors. Frontiers in Behavioral Neuroscience, 9, 36.CrossRefGoogle ScholarPubMed
Vogel, A., Mortensen, E.L., Gade, A., & Waldemar, G. (2007). The Category Cued Recall test in very mild Alzheimer’s disease: Discriminative validity and correlation with semantic memory functions. European Journal of Neurology, 14(1), 102–108. doi: 10.1111/j.1468-1331.2006.01568.x CrossRefGoogle ScholarPubMed
Yesavage, J.A., Brink, T.L., Rose, T.L., Lum, O., Huang, V., Adey, M., & Leirer, V.O. (1982). Development and validation of a geriatric depression screening scale: A preliminary report. Journal of Psychiatric Research, 17(1), 37–49.CrossRefGoogle ScholarPubMed