Emotional content typically facilitates subsequent memory, known as the emotional enhancement effect. We investigated whether emotional content facilitates spatial and item memory in patients with Alzheimer's dementia (AD). Twenty-three AD patients, twenty-three healthy elderly, and twenty-three young adults performed a picture relocation task and a delayed recognition task with positive, negative, and neutral stimuli. AD patients showed a benefit in immediate spatial memory for positive pictures, while healthy young and older participants did not benefit from emotional content. No emotional enhancement effects on delayed item recognition were seen. We conclude that AD patients may have a memory bias for positive information in spatial memory. Discrepancies between our findings and earlier studies are discussed. 1. Introduction There is abundant evidence that emotional events can be preserved in memory, even in patients with memory deficits. For example, amnesic patients could remember details of the terrorist attack of 9/11, 2001, while already suffering from profound anterograde amnesia at the time of the event [1]. This effect is generally referred to as the “emotional enhancement effect” [2]. Several experiments have shown that the emotional content of both pictures [3, 4] and words [5–7] facilitates subsequent memory for these items, although pictures evoke more arousal than words [8]. Furthermore, although enhancing effects of both valence (the subjective experience of a stimulus as positive or negative to a certain extent) [7] and arousal (physiological and psychological excitement evoked by the stimulus) have been demonstrated, most robust findings have been found when using highly arousing pictures (cf. [4]). Fleming et al. [9] speculated that there may be an evolutionary advantage to not becoming overwhelmed by emotional stimuli at the time of the event, because it would interfere with survival instincts, but rather to recall and retain the information after a delay. Indeed, emotional arousal has been reported to impair task performance in a short-term memory task, but to enhance subsequent long-term memory for the emotional items compared with neutral ones [8]. Bower [10] suggested that emotional stimuli “consume” cognitive resources because of their attention-grabbing nature and therefore hamper short-term memory functioning. Evidence suggests that emotionally arousing stimuli attract attention already in the early perceptual stages. For example, both young and older adults notice threatening stimuli (e.g., pictures of dangerous animals)
References
[1]
I. Candel, M. Jelicic, H. Merckelbach, and A. Wester, “Korsakoff patients' memories of September 11, 2001,” Journal of Nervous and Mental Disease, vol. 191, no. 4, pp. 262–265, 2003.
[2]
S. Hamann, “Cognitive and neural mechanisms of emotional memory,” Trends in Cognitive Sciences, vol. 5, no. 9, pp. 394–400, 2001.
[3]
S. B. Hamann, T. D. Ely, S. T. Grafton, and C. D. Kilts, “Amygdala activity related to enhanced memory for pleasant and aversive stimuli,” Nature Neuroscience, vol. 2, no. 3, pp. 289–293, 1999.
[4]
M. M. Bradley, M. K. Greenwald, M. C. Petry, and P. J. Lang, “Remembering pictures: pleasure and arousal in memory,” Journal of Experimental Psychology: Learning, Memory, and Cognition, vol. 18, no. 2, pp. 379–390, 1992.
[5]
K. A. Nielson, D. Yee, and K. I. Erickson, “Memory enhancement by a semantically unrelated emotional arousal source induced after learning,” Neurobiology of Learning and Memory, vol. 84, no. 1, pp. 49–56, 2005.
[6]
T. M. Libkuman, C. L. Stabler, and H. Otani, “Arousal, valence, and memory for detail,” Memory, vol. 12, no. 2, pp. 237–247, 2004.
[7]
E. A. Kensinger and S. Corkin, “Memory enhancement for emotional words: are emotional words more vividly remembered than neutral words?” Memory and Cognition, vol. 31, no. 8, pp. 1169–1180, 2003.
[8]
E. A. Kensinger and S. Corkin, “Effect of negative emotional content on working memory and long-term memory,” Emotion, vol. 3, no. 4, pp. 378–393, 2003.
[9]
K. Fleming, S. H. Kim, M. Doo, G. Maguire, and S. G. Potkin, “Memory for emotional stimuli in patients with Alzheimer's disease,” American Journal of Alzheimer's Disease and other Dementias, vol. 18, no. 6, pp. 340–342, 2003.
[10]
G. H. Bower, “How might emotions affect learning?” in The Handbook of Emotion and Memory: Research and Theory, S. Christianson, Ed., pp. 245–268, Lawrence Erlbaum Associates, New Jersey, NJ, USA, 1992.
[11]
M. Mather and M. R. Knight, “Angry faces get noticed quickly: threat detection is not impaired among older adults,” Journals of Gerontology—Series B Psychological Sciences and Social Sciences, vol. 61, no. 1, pp. P54–P57, 2006.
[12]
K. S. LaBar, M. M. Mesulam, D. R. Gitelman, and S. Weintraub, “Emotional curiosity: modulation of visuospatial attention by arousal is preserved in aging and early-stage Alzheimer's disease,” Neuropsychologia, vol. 38, no. 13, pp. 1734–1740, 2000.
[13]
M. Mather, K. J. Mitchell, C. L. Raye, D. L. Novak, E. J. Greene, and M. K. Johnson, “Emotional arousal can impair feature binding in working memory,” Journal of Cognitive Neuroscience, vol. 18, no. 4, pp. 614–625, 2006.
[14]
M. Mather and K. Nesmith, “Arousal-enhanced location memory for pictures,” Journal of Memory and Language, vol. 58, no. 2, pp. 449–464, 2008.
[15]
C. B. Hadley and D. G. MacKay, “Does emotion help or hinder immediate memory? Arousal versus priority-binding mechanisms,” Journal of Experimental Psychology: Learning, Memory, and Cognition, vol. 32, no. 1, pp. 79–88, 2006.
[16]
S. Doerksen and A. P. Shimamura, “Source memory enhancement for emotional words,” Emotion, vol. 1, no. 1, pp. 5–11, 2001.
[17]
M. Mather, “Emotional arousal and memory binding. An object-based framework,” Perspectives on Psychological Science, vol. 2, pp. 33–52, 2007.
[18]
M. T. Reinitz and S. L. Hannigan, “False memories for compound words: role of working memory,” Memory and Cognition, vol. 32, no. 3, pp. 463–473, 2004.
[19]
D. Chan, N. C. Fox, R. I. Scahill et al., “Patterns of temporal lobe atrophy in semantic dementia and Alzheimer's disease,” Annals of Neurology, vol. 49, no. 4, pp. 433–442, 2001.
[20]
K. K. Zakzanis, S. J. Graham, and Z. Campbell, “A meta-analysis of structural and functional brain imaging in dementia of the Alzheimer's type: a neuroimaging profile,” Neuropsychology Review, vol. 13, no. 1, pp. 1–18, 2003.
[21]
S. Lehericy, M. Baulac, J. Chiras et al., “Amygdalohippocampal MR volume measurements in the early stages of Alzheimer disease,” American Journal of Neuroradiology, vol. 15, no. 5, pp. 929–937, 1994.
[22]
J. L. McGaugh, “The amygdala modulates the consolidation of memories of emotionally arousing experiences,” Annual Review of Neuroscience, vol. 27, pp. 1–28, 2004.
[23]
G. Richter-Levin and I. Akirav, “Emotional tagging of memory formation—in the search for neural mechanisms,” Brain Research Reviews, vol. 43, no. 3, pp. 247–256, 2003.
[24]
J. Abrisqueta-Gomez, O. F. A. Bueno, M. G. M. Oliveira, and P. H. F. Bertolucci, “Recognition memory for emotional pictures in Alzheimer's patients,” Acta Neurologica Scandinavica, vol. 105, no. 1, pp. 51–54, 2002.
[25]
S. B. Hamann, E. S. Monarch, and F. C. Goldstein, “Memory enhancement for emotional stimuli is impaired in early Alzheimer's disease,” Neuropsychology, vol. 14, no. 1, pp. 82–92, 2000.
[26]
S. E. Moayeri, L. Cahill, Y. Jin, and S. G. Potkin, “Relative sparing of emotionally influenced memory in Alzheimer's disease,” NeuroReport, vol. 11, no. 4, pp. 653–655, 2000.
[27]
R. R. Schultz, C. C. de Castro, and P. H. F. Bertolucci, “Memory with emotional content, brain amygdala and Alzheimer's disease,” Acta Neurologica Scandinavica, vol. 120, no. 2, pp. 101–110, 2009.
[28]
E. Mori, M. Ikeda, N. Hirono, H. Kitagaki, T. Imamura, and T. Shimomura, “Amygdalar volume and emotional memory in Alzheimer's disease,” American Journal of Psychiatry, vol. 156, no. 2, pp. 216–222, 1999.
[29]
K. Nashiro and M. Mather, “How arousal affects younger and older adults' memory binding,” Experimental Aging Research, vol. 37, no. 1, pp. 108–128, 2011.
[30]
G. McKhann, D. Drachman, and M. Folstein, “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, vol. 34, no. 7, pp. 939–944, 1984.
[31]
B. Dubois, H. H. Feldman, C. Jacova et al., “Research criteria for the diagnosis of Alzheimer's disease: revising the NINCDS-ADRDA criteria,” The Lancet Neurology, vol. 6, no. 8, pp. 734–746, 2007.
[32]
J. I. Sheikh and J. A. Yesavage, “Geriatric Depression Scale (GDS): recent evidence and development of a shorter version,” Clinical Gerontologist, vol. 5, no. 1-2, pp. 165–173, 1986.
[33]
M. F. Folstein, S. E. Folstein, and P. R. McHugh, “'Mini mental state'. A practical method for grading the cognitive state of patients for the clinician,” Journal of Psychiatric Research, vol. 12, no. 3, pp. 189–198, 1975.
[34]
H. E. Nelson, National Adult Reading Test (NART): Test Manual, NFER-Nelson, Windsor, UK, 1982.
[35]
B. Schmand, J. Lindeboom, and F. Van Harskamp, NLV: Nederlandse Leestest Voor Volwassenen: Handleiding, Swets & Zeitlinger, Lisse, The Netherlands, 1992.
[36]
F. Verhage, Intelligentie en Leeftijd: Onderzoek bij Nederlanders van Twaalf tot Zevenenzeventig Jaar, Van Gorcum, Assen, The Netherlands, 1964.
[37]
O. Meulenbroek, M. Vernooij-Dassen, R. P. C. Kessels et al., “Informed consent in dementia research. Legislation, theoretical concepts and how to assess capacity to consent,” European Geriatric Medicine, vol. 1, no. 1, pp. 58–63, 2010.
[38]
R. P. C. Kessels, A. Postma, and E. H. F. De Haan, “Object Relocation: a program for setting up, running, and analyzing experiments on memory for object locations,” Behavior Research Methods, Instruments, and Computers, vol. 31, no. 3, pp. 423–428, 1999.
[39]
P. J. Lang, M. M. Bradley, and B. N. Cuthbert, “International affective picture system (IAPS): instruction manual and affective ratings,” Tech. Rep. A-6, The Center for Research in Psychophysiology, University of Florida, Gainesville, Fla, USA, 2005.
[40]
D. M. Green and J. A. Swets, Signal Detection Theory and Psychophysics, John Wiley & Sons, New York, NY, USA, 1966.
[41]
M. A. Parra, S. Abrahams, K. Fabi, R. Logie, S. Luzzi, and S. D. Sala, “Short-term memory binding deficits in Alzheimers disease,” Brain, vol. 132, no. 4, pp. 1057–1066, 2009.
[42]
B. L. Chalfonte and M. K. Johnson, “Feature memory and binding in young and older adults,” Memory and Cognition, vol. 24, no. 4, pp. 403–416, 1996.
[43]
R. P. C. Kessels, D. Hobbel, and A. Postma, “Aging, context memory and binding: a comparison of “what, where and when” in young and older adults,” International Journal of Neuroscience, vol. 117, no. 6, pp. 795–810, 2007.
[44]
J. R. Brockmole, M. A. Parra, S. D. Sala, and R. H. Logie, “Do binding deficits account for age-related decline in visual working memory?” Psychonomic Bulletin and Review, vol. 15, no. 3, pp. 543–547, 2008.
[45]
S. T. Charles, M. Mather, and L. L. Carstensen, “Aging and emotional memory: the forgettable nature of negative images for older adults,” Journal of Experimental Psychology: General, vol. 132, no. 2, pp. 310–324, 2003.
[46]
L. A. Leigland, L. E. Schulz, and J. S. Janowsky, “Age related changes in emotional memory,” Neurobiology of Aging, vol. 25, no. 8, pp. 1117–1124, 2004.
[47]
M. Mather and M. Knight, “Goal-directed memory: the role of cognitive control in older adults' emotional memory,” Psychology and Aging, vol. 20, no. 4, pp. 554–570, 2005.
[48]
D. P. Smith, C. H. Hillman, and A. R. Duley, “Influences of age on emotional reactivity during picture processing,” Journals of Gerontology—Series B Psychological Sciences and Social Sciences, vol. 60, no. 1, pp. P49–P56, 2005.
