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Effects of stress on emotional memory in patients with Alzheimer's disease and in healthy elderly

Published online by Cambridge University Press:  14 December 2017

María Gómez-Gallego*
Affiliation:
Faculty of Health Sciences, Catholic University of Murcia, Murcia, Spain
Juan Gómez-García
Affiliation:
Department of Quantitative Methods, Faculty of Economics, University of Murcia, Murcia, Spain
*
Correspondence should be addressed to: María Gómez-Gallego, 135 Campus of Jerónimos, 30107 Murcia, Spain. Phone: (+34) 968 27 88 01585. Email: mgomezg@um.es.

Abstract

Objective:

We aimed at examining the relation between stress markers (cortisol levels and state anxiety) with memory for emotional information in AD patients and in healthy elderly.

Design, Setting, and participants:

Baseline and changes in stress markers during memory testing were assessed in a sample of 98 elderly (46 mild-to-moderate Alzheimer's disease patients and 52 controls) recruited from dementia day centers and adult day centers, respectively.

Measurements:

Salivary cortisol, state anxiety, and measures of immediate recall and delayed recognition using the International Affective Pictures System.

Results:

Patients’ performance in memory tasks was not associated with either cortisol levels or anxiety. In controls, quadratic and linear associations were found between cortisol and immediate recall scores (total and bias, respectively). Besides, quadratic and linear associations were observed between anxiety and delayed recognition scores (total and bias, respectively).

Conclusions:

The emotional memory of patients with Alzheimer´s disease is not related to stress markers as healthy older adults’ is. Future studies that include moderating variables are needed to explain the lack of association.

Type
Original Research Article
Copyright
Copyright © International Psychogeriatric Association 2017 

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References

Abrisqueta-Gomez, J., Bueno, O. F. A., Oliveira, M. G. M. and Bertolucci, P. H. F. (2002). Recognition memory for emotional pictures in Alzheimer's patients. Acta Neurologica Scandinavica, 105, 5154. doi: 10.1034/j.1600-0404.2002.00035.x.Google Scholar
Ackermann, K., Schwabe, L., Scho, P., Schönfeld, P., Ackermann, K. and Schwabe, L. (2014). Remembering under stress: different roles of autonomic arousal and glucocorticoids in memory retrieval. Psychoneuroendocrinology, 39, 249256. doi: 10.1016/j.psyneuen.2013.09.020.Google Scholar
Ackermann, S., Hartmann, F., Papassotiropoulos, A., Quervain, D. J. De and Rasch, B. (2012). Associations between basal cortisol levels and memory retrieval in healthy young individuals. Journal of Cognitive Neuroscience, 25, 18961907. doi: 10.1162/jocn.Google Scholar
Aiken, L. S., West, S. G. and Reno, R. R. (1991). Multiple Regression: Testing and Interpreting Interactions. Newbury Park, CA: Sage.Google Scholar
Army Individual Test Battery. (1944). Manual of Directions and Scoring. Whashington, DC: War Department, Adjutant's Generals' Office.Google Scholar
Beluche, I., Carriere, I., Ritchie, K. and Ancelin, M. L. (2010). A prospective study of diurnal cortisol and cognitive function in community-dwelling elderly people. Psychological Medicine, 40, 10391049. doi: 10.1017/S0033291709991103.Google Scholar
Bierman, E. J. M., Comijs, H. C., Jonker, C., Scheltens, P. and Beekman, A. T. F. (2009). The effect of anxiety and depression on decline of memory function in Alzheimer's disease. International Psychogeriatrics, 21, 11421147. doi: 10.1017/S1041610209990512.Google Scholar
Bierman, E. J. M., Comijs, H. C., Rijmen, F., Jonker, C. and Beekman, A. T. F. (2008). Anxiety symptoms and cognitive performance in later life: results from the longitudinal aging study Amsterdam. Aging and Mental Health, 12, 517523.Google Scholar
Buchanan, T. W., Denburg, N. L., Tranel, D. and Adolphs, R. (2001). Verbal and nonverbal emotional memory following unilateral amygdala damage. Learning Memory, 8, 326335. doi: 10.1101/lm.40101.et.Google Scholar
Chainay, H., Sava, A., Michael, G. A., Landré, L., Versace, R. and Krolak-Salmon, P. (2014). Impaired emotional memory enhancement on recognition of pictorial stimuli in Alzheimer's disease: no influence of the nature of encoding. Cortex, 50, 3244. doi: 10.1016/j.cortex.2013.10.001.Google Scholar
Charney, D. S. and Drevets, W. C. (2002). Neurobiological basis of anxiety disorders. In Kenneth, D., Charney, D., Coyle, J. T. and Charles, Nemeroff. C. (eds.), Neuropsychopharmacology: The Fifth Generation of Progress (pp. 901930). American College of Neuropsychopharmacology. Philadelphia, PA: Lippincott Williams & Wilkins.Google Scholar
Csernansky, J. G. et al. (2006). Plasma cortisol and progression of dementia in DAT subjects. American Journal of Psychiatry, 163, 21642169.Google Scholar
Curiel, A. R., Miller, K. J., Pollard, K., Kim, J. and Kravitz, J. (2012). Anxiety and verbal memory performance in APOE-4 carriers and noncarriers aged 50 years and above. Aging Health, 8, 99104.Google Scholar
Eysenck, M. W., Derakshan, N., Santos, R. and Calvo, M. G. (2007). Anxiety and cognitive performance: attentional control theory. Emotion, 7, 336353. doi: 10.1037/1528-3542.7.2.336.Google Scholar
Fiocco, A. J., Wan, N., Weekes, N., Pim, H. and Lupien, S. J. (2006). Diurnal cycle of salivary cortisol in older adult men and women with subjective complaints of memory deficits and/or depressive symptoms: relation to cognitive functioning. Stress, 9, 143152.Google Scholar
Fleming, K., SH, K., Doo, M., Maguire, G. and Potkin, S. (2003). Memory for emotional stimuli in patients with Alzheimer's disease. American Journal of Alzheimer's Disease and Other Dementias, 18, 340342.Google Scholar
Folstein, M. F., Folstein, S. E. and 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, 189198.Google Scholar
Gaffey, A. E., Bergeman, C. S., Clark, L. A. and Wirth, M. M. (2016). Aging and the HPA axis: stress and resilience in older adults. Neuroscience and Biobehavioral Reviews, 68, 928945. doi: 10.1016/j.neubiorev.2016.05.036.Google Scholar
Gil-Bea, F. J. et al. (2010). HPA axis dysregulation associated to apolipoprotein E4 genotype in Alzheimer's disease. Journal of Alzheimer's Disease, 22, 829838. doi: 10.3233/JAD-2010-100663.Google Scholar
Giubilei, F. et al. (2001). Altered circadian cortisol secretion in Alzheimer's disease: clinical and neuroradiological aspects. Journal of Neuroscience Research, 66, 262265.Google Scholar
Gómez-Gallego, M. and Gómez-García, J. (2017). Negative bias in the perception and memory of emotional information in Alzheimer disease. Journal of Geriatric Psychiatry and Neurology, 30, 131139. doi: 10.1177/0891988716686833.Google Scholar
Herrera, S., Montorio, I. and Cabrera, I. (2015). Effect of anxiety on memory for emotional information in older adults. Aging and Mental Health, 21, 17. doi: 10.1080/13607863.2015.1093601.Google Scholar
Holland, J. M. et al. (2014). Psychosocial predictors of salivary cortisol among older adults with depression. International Psychogeriatrics, 26, 15311539. doi: 10.1017/S1041610214000489.Google Scholar
Jiang, L. et al. (2016). Cholinergic signaling controls conditioned fear behaviors and enhances plasticity of cortical-amygdala circuits. Neuron, 90, 10571070. doi: 10.1016/j.neuron.2016.04.028.Google Scholar
Kirschbaum, C. and Hellhammer, D. H. (2000). Salivary cortisol. In Fink, G. (ed.), Encyclopedia of Stress (pp. 379383). San Diego, CA: Academic Press.Google Scholar
Krugers, H. J., Lucassen, P. J., Karst, H. and Joëls, M. (2010). Chronic stress effects on hippocampal structure and synaptic function: relevance for depression and normalization by anti-glucocorticoid treatment. Frontiers in Synaptic Neuroscience, 2, 110. doi: 10.3389/fnsyn.2010.00024.Google Scholar
Lang, P., Bradley, M. and Cuthbert, B. N. (2008). International Affective Picture System (IAPS): Affective Ratings of Pictures and Instruction Manual. Technical Report A-8. Gainesville, FL: University of Florida.Google Scholar
Lupien, S. J. et al. (1998). Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nature Neuroscience, 1, 6973. doi: 10.1038/271.Google Scholar
Lupien, S. J. et al. (2005). Stress hormones and human memory function across the lifespan. Psychoneuroendocrinology, 30, 225242. doi: 10.1016/j.psyneuen.2004. 08.003.Google Scholar
Mah, L., Anderson, N. D., Verhoeff, N. P. L. G. and Pollock, B. G. (2017). Negative emotional verbal memory biases in mild cognitive impairment and late-onset depression. The American Journal of Geriatric Psychiatry, 25, 11601170. doi: 10.1016/j.jagp.2017.05.005.Google Scholar
Mah, L., Binns, M. A. and Steffens, D. C. (2015). Anxiety symptoms in amnestic mild cognitive impairment are associated with medial temporal atrophy and predict conversion to Alzheimer disease. American Journal of Geriatric Psychiatry, 23, 466476. doi: 10.1016/j.jagp.2014.10.005.Google Scholar
Maheu, F. S., Collicutt, P., Kornik, R., Moszkowski, R. and Lupien, S. J. (2005). The perfect time to be stressed: a differential modulation of human memory by stress applied in the morning or in the afternoon. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 29, 12811288. doi: 10.1016/j.pnpbp.2005.08.012.Google Scholar
Mahoney, F. I. and Barthel, D. W. (1965). Baltimore city medical society functional evaluation: the Barthel index. Maryland State Medical Journal, 14, 61–5.Google Scholar
McCullough, A. M., Ritchey, M., Ranganath, C. and Yonelinasa, A. (2016). Differential effects of stress-induced cortisol responses on recollection and familiarity-based recognition memory. Neurobiology of Learning and Memory, 110. doi: 10.1016/j.nlm.2015.04.007.Google Scholar
McKeown, J., Clarke, A., Ingleton, C. and Repper, J. (2010). Actively involving people with dementia in qualitative research. Journal of Clinical Nursing, 19, 19351943. doi: 10.1111/j.1365-2702.2009.03136.x.Google Scholar
McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D. and Stadlan, E. M. (1984). Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA work group under the auspices of department of health and human services task force on Alzheimer's disease. Neurology, 34, 939944.Google Scholar
Moltó, J. et al. (1999). Un método para el estudio experimental de las emociones: el International Affective Picture System (IAPS). Adaptación española. Revista de Psicología General y Aplicada, 52, 5587.Google Scholar
Moltó, J. et al. (2013). Adaptación española del “international affective picture system” (IAPS). Tercera parte. Anales de Psicología, 29, 965984. doi: 10.6018/analesps.29.3.153591.Google Scholar
Nebreda, M. C., García-Caballero, A., Asensio, E., Revilla, P., Rodriguez-Girondo, M. and Mateos, R. (2011). A short-form version of the Boston naming test for language screening in dementia in a bilingual rural community in Galicia (Spain). International Psychogeriatrics, 23, 435441. doi: 10.1017/S1041610210001481.Google Scholar
Neupert, S. D., Miller, L. M. S. and Lachman, M. E. (2006). Physiological reactivity to cognitive stressors: variations by age and socioeconomic status. International Journal of Aging and Human Development, 62, 221235.Google Scholar
Perpiñá-Galvañ, J., Richart-Martínez, M. and Cabañero-Martínez, M. J. (2011). Fiabilidad y validez de una versión corta de la escala de medida de la ansiedad STAI en pacientes respiratorios. Archivos de Bronconeumología, 47, 184189. doi: 10.1016/j.arbres.2010.11.006.Google Scholar
Perrin, M., Henaff, M. A., Padovan, C., Faillenot, I., Merville, A. and Krolak-Salmon, P. (2012). Influence of emotional content and context on memory in mild Alzheimer's disease. Journal of Alzheimer's Disease, 28, 817826.Google Scholar
Pfeffer, R. I., Kurosaki, T. T., Harrah, C. H. J., Chance, J. M. and Filos, S. (1982). Measurement of functional activities in older adults in the community. Journal of Gerontology, 37, 323329.Google Scholar
Poulin, S. P., Dautoff, R., Morris, J. C., Barrett, L. F. and Dickerson, B. C. (2011). Amygdala atrophy is prominent in early Alzheimer's disease and relates to symptom severity, Psychiatry Research, 194, 713. doi: 10.1016/j.pscychresns.2011.06.014.Google Scholar
Preuß, D., Schoofs, D. and Wolf, O. T. (2009). Associations between endogenous cortisol levels and emotional memory in young women: influence of encoding instructions. Stress, 12, 379387. doi: 10.1080/10253890802524592.Google Scholar
Rami, L., Bosch, B., Sanchez-Valle, R. and Molinuevo, J. L. (2010). The memory alteration test (M@T) discriminates between subjective memory complaints, mild cognitive impairment and Alzheimer's disease. Archives of Gerontology and Geriatrics, 50, 171174. doi: 10.1016/j.archger.2009.03.005Google Scholar
Reisberg, B., Ferris, S. H., de Leon, M. J. and Crook, T. (1988). Global Deterioration Scale (GDS). Psychopharmacology Bulletin, 24, 661663.Google Scholar
Rosnick, C. B., Rawson, K. S., Butters, M. A. and Lenze, E. J. (2013). Association of cortisol with neuropsychological assessment in older adults with generalized anxiety disorder. Aging and Mental Health, 17, 432440.Google Scholar
Rothman, S. M. and Mattson, M. P. (2010). Adverse stress, hippocampal networks, and Alzheimer's disease. Neuromolecular Medicine, 12, 5670. doi: 10.1007/s12017-009-8107-9.Google Scholar
Satler, C. and Tomaz, C. (2011). Emotional working memory in Alzheimer's disease patients. Dementia and Geriatric Cognitive Disorders Extra, 1, 124–38. doi: 10.1159/000329155.Google Scholar
Schultz, R. R., De Castro, C. C. and Bertolucci, P. H. F. (2009). Memory with emotional content, brain amygdala and Alzheimer's disease. Acta Neurologica Scandinavica, 120, 101110. doi: 10.1111/j.1600-0404.2008.01132.x.Google Scholar
Souza-Talarico, J. N., Chaves, E. C., Lupien, S. J., Nitrini, R. and Caramelli, P. (2010). Relationship between cortisol levels and memory performance may be modulated by the presence or absence of cognitive impairment: evidence from healthy elderly, mild cognitive impairment and Alzheimer's disease subjects. Journal of Alzheimer's Disease, 19, 839848. doi: 10.3233/JAD-2010-1282Google Scholar
Swanwick, G. et al. (1998). Hypothalamic-pituitary-adrenal axis dysfunction in Alzheimer's disease: lack of association between longitudinal and cross-sectional findings. American Journal of Psychiatry, 155, 286289.Google Scholar
Tappen, R. M., Williams-burgess, C., Edelstein, J. and Touhy, T. (1997). Communication with individual with Alzheimer's disease: examination of recommended strategies. Archives of Psychiatric Nursing, 11, 249256.Google Scholar
ter Heegde, F., De Rijk, R. H. and Vinkers, C. H. (2015). The brain mineralocorticoid receptor and stress resilience. Psychoneuroendocrinology, 52, 92110.Google Scholar
Thompson, E. R. (2007). Development and validation of an internationally reliable short-form of the Positive and Negative Affect Schedule (PANAS). Journal of Cross-Cultural Psychology, 38, 227242. doi: 10.1177/0022022106297301.Google Scholar
Ulrich-Lay, Y. and Herman, P. (2014). Neural regulation of endocrine and autonomic stress responses. Nature Reviews Neuroscience, 10, 397409. doi: 10.1038/nrn2647.Google Scholar
Vila, J. et al. (2001). El Sistema Internacional de Imágenes Afectivas (IAPS): adaptación española. Segunda parte. Revista de Psicología General y Aplicada, 54, 635657.Google Scholar
Weiner, M. F., Vobach, S., Olsson, K., Svetlik, D. and Risser, R. C. (1997). Cortisol secretion and Alzheimer's disease progression. Biological Psychiatry, 42, 10301038.Google Scholar
Wolf, O. T. (2009). Stress and memory in humans: twelve years of progress? Brain Research, 1293, 142154. doi: 10.1016/j.brainres.2009.04.013.Google Scholar
Wolf, O. T., Convit, A., Thorn, E. and J de Leon, M. (2002). Salivary cortisol day profiles in elderly with mild cognitive impairment. Psychoneuroendocrinology, 27, 777789.Google Scholar
Yerkes, R. M. and Dodson, J. D. (1908). The relation of strength of stimulus to rapidity of habit-formation. Journal of Comparative Neurology and Psychology, 18, 459482.Google Scholar
Yesavage, J. A. (1988). Geriatric depression scale. Psychopharmacology Bulletin, 24, 709711.Google Scholar