The Northwestern University SuperAging Program studies a rare cohort of individuals over age 80 with episodic memory ability at least as good as middle-age adults to determine what factors contribute to their elite memory performance. As psychological well-being is positively correlated with cognitive performance in older adults, the present study examined whether aspects of psychological well-being distinguish cognitive SuperAgers from their cognitively average-for-age, same-age peers.
Thirty-one SuperAgers and 19 cognitively average-for-age peers completed the Ryff 42-item Psychological Well-Being questionnaire, comprised of 6 subscales: Autonomy, Positive Relations with Others, Environmental Mastery, Personal Growth, Purpose in Life, and Self-Acceptance.
The groups did not differ on demographic factors, including estimated premorbid intelligence. Consistent with inclusion criteria, SuperAgers had better episodic memory scores. Compared to cognitively average-for-age peers, SuperAgers endorsed greater levels of Positive Relations with Others. The groups did not differ on other PWB-42 subscales.
While SuperAgers and their cognitively average-for-age peers reported similarly high levels of psychological well-being across multiple dimensions, SuperAgers endorsed greater levels of positive social relationships. This psychological feature could conceivably have a biological relationship to the greater thickness of the anterior cingulate gyrus and higher density of von Economo neurons previously reported in SuperAgers.
Citation: Cook Maher A, Kielb S, Loyer E, Connelley M, Rademaker A, Mesulam M-M, et al. (2017) Psychological well-being in elderly adults with extraordinary episodic memory. PLoS ONE 12(10): e0186413. https://doi.org/10.1371/journal.pone.0186413
Editor: Philip Allen, University of Akron, UNITED STATES
Received: February 23, 2017; Accepted: September 29, 2017; Published: October 23, 2017
Copyright: © 2017 Cook Maher et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper and its Supporting Information files.
Funding: This work was funded by grants from the National Institute on Aging R01 AG045571 (ER & MM), Alzheimer's Disease Core Center AG13854 (MM), the Davee Foundation (MM), and the Foley Family Foundation (DM). First author additionally supported by a T32 Training Grant from the National Institute of Neurological Disorders and Stroke NS047987. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Age-related cognitive decline is widely considered to be a “normal” consequence of aging. However, evidence from the Northwestern University SuperAging Program suggests that such decline is not inevitable . SuperAgers are adults over age 80 whose performance on tests of episodic memory, the type of memory that shows decline with aging and dramatic decline in Alzheimer’s dementia, is at least as good as individuals 20 to 30 years their junior. The SuperAging Program is dedicated to identifying factors that contribute to their elite memory performance.
Initial results suggest that SuperAgers represent a rare cognitive phenotype with unique physiological brain features. SuperAgers are selected for having above-average-for-age episodic memory at the time of study entry and most maintain this high level of performance over at least 18-months, suggesting resistance to age-related memory decline . On structural magnetic resonance imaging (MRI) scans at the time of study entry, SuperAgers had a significantly thicker brain cortex than their cognitively average, same-age peers and did not show significant cortical thinning compared to cognitively average middle-age adults . SuperAgers also had a significantly larger left anterior cingulate than both the cognitively average-for-age elderly and middle-age groups . This cortical preservation is unusual as age-related cortical atrophy is well documented beginning in early adulthood [4, 5]. Further, a recent longitudinal neuroimaging study in the SuperAging Program found that SuperAgers demonstrate significantly less whole-brain cortical atrophy over 18-months compared to their cognitively average, same-age peers . While the functional significance of the difference in cortical thickness and difference in atrophy rates is currently unclear, these neuroimaging findings contribute to the hypothesis that SuperAgers may possess unique brain physiology.
This idea is furthered by post-mortem histopathologic analyses of the anterior cingulate, which demonstrated a lower frequency of Alzheimer disease pathology and a higher density of von Economo neurons (VENs) in SuperAgers compared to their cognitively average same-age peers . VENs are a type of neuron that have been identified in humans and other phylogenetically advanced species, are primarily found in the anterior cingulate and frontoinsular cortices, and are hypothesized to play a role in complex social cognition, intuitive assessment of complex, often uncertain, situations, and facilitation of fast communication with other brain regions [8, 9]. Taken together, these findings suggest that SuperAgers have unique biological characteristics that separate them from their cognitively average-for-age peers, which may contribute to their resistance to age-related involutional changes in memory [1, 7]. The present study extends these initial findings by characterizing psychological well-being in SuperAgers.
Psychological well-being is a positive psychological construct related to subjective views of one’s self and life. Higher levels of psychological well-being have been positively correlated with cognitive performance in older adults. For example, Llewellyn and colleagues (2008) demonstrated that among individuals over age 50, those who scored in the highest quintile on the CASP-19 psychological well-being scale scored higher on neuropsychological tests than those who scored in the lowest quintile . Previous research has also shown positive correlations between episodic memory performance and environmental mastery , purpose in life [12, 13], and positive relations with others as characterized by social support and number of social contacts [14, 15] in older adults. In addition, greater baseline levels of purpose in life  and increased social engagement later in life [16, 17] have both been associated with reduced risk of developing Alzheimer’s dementia, a neurodegenerative disease characterized by primary impairment in episodic memory. Because SuperAgers are selected for having superior episodic memory for their age, it is possible that they also express greater environmental mastery, purpose in life, and positive relations with others compared to their cognitively average-for-age same-age peers. The present study therefore examined whether aspects of psychological well-being distinguish cognitively above-average SuperAgers from their cognitively average-for-age peers.
Data were prospectively collected from participants enrolled in the Northwestern University SuperAging Program, an ongoing, longitudinal investigation of aging in community-dwelling adults over age 80 who have been described previously . Briefly, SuperAgers are carefully differentiated from cognitively average-for-age, same-age elderly adults based on neuropsychological test performance as shown in Table 1. Inclusion criteria for SuperAgers is as follows: 1) performance at or above normative values for average 50 to 65-year-olds (equivalent to the Superior range for their own age) on delayed recall of the Rey Auditory Verbal Learning Test (RAVLT), a 15-word list-learning episodic memory test ; 2) performance in at least the average-for-age normative range on non-memory tests including the 30-item Boston Naming Test , Trail Making Test Part-B , and Category Fluency Test . In contrast, inclusion criteria for Cognitively Average Elderly adults is as follows: 1) performance within the average-for-age normative range on episodic memory (i.e. the RAVLT); 2) performance within the average-for-age normative range on all non-memory tests listed above.
All participants were required to have preserved activities of daily living and lack clinical evidence of significant neurological or psychiatric illness. In the present study, participants were required to maintain their cognitive status (SuperAger or cognitively average elderly) from enrollment to the time questionnaires were completed to minimize the unintended inclusion of individuals with emerging Alzheimer’s dementia and maintain the integrity of our elite SuperAger sample.
The Northwestern University Institutional Review Board approved study procedures. All participants provided written informed consent.
The Ryff 42-item Psychological Well Being questionnaire (PWB-42; [22, 23] was used to assess psychological well-being. The PWB-42 is a self-report measure that includes six domains of well-being: Environmental Mastery, Personal Growth, Positive Relations with Others, Self-Acceptance, Autonomy, and Purpose in Life, (described in Table 2). This six-factor model has support for use in healthy elderly adults [22, 24]. Participants rate their agreement with 42 statements on a 6-point Likert scale ranging from “1 –strongly disagree” to “6 –strongly agree.” Scores in each domain range from 7 and 42 where higher scores indicate greater levels of well-being. One-half of items are negatively worded and reverse scored.
Examples of positively worded and negatively worded items are provided.
Because the subscale scores were not normally distributed in SuperAgers, Wilcoxon rank sum tests and Fisher’s exact tests were used to examine between-group differences in demographic variables, neuropsychological data, and PWB-42 subscale scores, as appropriate. Wilcoxon rank sum test was also used to examine potential gender differences on the PWB-42 subscales. Spearman correlations were used to examine the association between episodic memory performance and psychological well-being. All tests were two-tailed.
For each set of six rank sum and correlation tests for PWB-42 subscales, a Bonferroni criterion of p<0.0083 was used for statistical significance. With the given sample sizes, there was 80% power for the rank sum test to detect a mean difference of 4.3 in the PWB subscales between groups at the adjusted p<0.0083.
Demographic & neuropsychological characterization
Thirty-one SuperAgers (ages 80 to 96, 23 female) and 19 Cognitively Average Elderly adults (ages 80 to 102, 12 female) were actively enrolled in the SuperAging Program, met inclusion criteria, and completed the PWB-42 questionnaire. All are included in this analysis.
There were no significant group differences in age, gender, race, or education (p’s>0.05; Table 3). Consistent with inclusion criteria, SuperAgers had significantly better RAVLT performance compared to their cognitively average peers (median delay raw score (interquartile range (IQR)) SuperAgers: 11 (10–13); Cognitively Average Elderly: 7 (6–7)); p<0.001). The groups did not differ on other neuropsychological measure, including estimates of premorbid intellectual ability (p’s>0.05).
There were no significant between-group differences in age, education, gender, or race. SuperAgers outperformed their cognitively average-for-age peers on measures of episodic memory and category fluency. There were no other significant between-group differences on neuropsychological measures, including estimated premorbid intelligence.
Scores from the PWB-42 are shown in Fig 1. SuperAgers endorsed a significantly greater level of Positive Relations with Others (median overall score (IQR): 40 (36–41); mean item score: 5.5) compared to Cognitively Average Elderly adults (median overall score (IQR): 36 (33–39); mean item score: 5.1; p = 0.005). There were no other significant between-group differences on PWB-42 subscales (p’s>0.0083). There were no significant gender differences within either group on the PWB-42 subscales (p-values ranged from 0.14 to 0.94).
Boxplots for Psychological Well-Being 42-Item (PWB-42) subscale scores are shown (medians, interquartile range, and upper/lower quartile ranges). SuperAgers endorsed significantly greater levels of positive relations with others compared to their cognitively average peers (Median SuperAger: 40, Cognitively Average Elderly: 36; p = 0.005). The groups did not differ on other subscales of the PWB-42 (p’s>0.0083) including Autonomy (Median SuperAger: 34, Cognitively Average Elderly: 34), Environmental Mastery (Median SuperAger: 40.5, Cognitively Average Elderly: 37), Personal Growth (Median SuperAger: 36, Cognitively Average Elderly: 37), Purpose in Life (Median SuperAger: 37.5, Cognitively Average Elderly: 37), or Self-Acceptance (Median SuperAger: 38, Cognitively Average Elderly: 37).
Spearman correlation showed low positive associations between RAVLT performance and Environmental Mastery (Spearman r = 0.36, p = 0.013) and between RAVLT performance and Positive Relations with Others (Spearman r = 0.33, p = 0.018), but were not significant with Bonferroni correction.
While both SuperAgers and Cognitively Average Elderly adults endorsed high levels of psychological well-being, SuperAgers endorsed greater levels of positive social relationships than their cognitively average-for-age peers suggesting that perceived high-quality social relationships may be an important factor in cognitive SuperAging. This result is particularly intriguing given the previously reported higher density of von Economo neurons found in the anterior cingulate cortex of SuperAgers [1, 7] and the hypothesized role of these neurons in higher order social cognition and behaviors, such as social bonding, social intuition, and emotional regulation [8, 9, 25]. It is possible that the greater density of these neurons in SuperAgers underlies increased positive social interactions and behaviors, which in turn contribute to greater endorsement of Positive Relations with Others on the PWB-42. As von Economo neurons can only be quantified via histopathological analysis post-mortem, the relationship between von Economo neuronal density and PWB-42 endorsement remains speculative.
Our finding that SuperAgers endorse greater levels of positive social relationships than their cognitively average-for-age peers is consistent with previous research demonstrating that social integration, engagement with family, and emotional support from a social network are positively correlated with cognitive function in older adults [15, 26, 27], predict reduced rates of cognitive decline [14, 28], and are associated with reduced risk of Mild Cognitive Impairment and dementia [29, 30]. Importantly, it appears that social relationships in and of themselves are important to the maintenance of cognition as opposed to other factors that may enhance or inhibit participation in social relationships, such as sex, depressive symptoms, baseline cognitive ability, physical functioning, or social network size . In addition, the relationship between positive social relationships and cognition appears to be unidirectional in that positive social relationships influence subsequent cognitive performance while the reverse does not appear to be true . Because SuperAgers represent a rare cognitive aging phenotype and sample sizes are therefore small compared to other psychology studies, current findings should be validated in larger, more demographically diverse samples.
SuperAgers and the cognitively average-for-age elderly adults in this study shared similar levels of Autonomy, Environmental Mastery, Personal Growth, Purpose in Life, and Self-Acceptance. This suggests that these aspects of psychological well-being may not differ among cognitively average to superior adults. On average, both our cognitively average adults and SuperAgers endorse slightly higher levels of well-being than the general elderly population studied in MIDUS (Midlife in the United States: a National Longitudinal Study of Health and Well-being); , suggesting both groups in the present study may be on the higher end of the psychological well-being spectrum. However, there is a lack of literature with published average values for adults over age 80 on the PWB-42 limiting our ability to compare findings from the SuperAgers and cognitively average-for-age elderly with other populations. The correlation between episodic memory performance and Positive Relations with Others was not significant in our sample, suggesting there may not be a direct relationship among elderly individuals with average to superior memory.
The presence of gender differences in measures of psychological well-being are inconsistent across studies, with some studies showing that women tend to rate themselves higher on Positive Relations [33, 34] and others finding that men may rate themselves higher on Personal Growth  or Purpose in Life . The present study did not find gender differences on any measure of psychological well-being, although the study was not specifically designed for such comparison.
In summary, SuperAgers endorse higher levels of Positive Relations with Others compared to their cognitively healthy but average-for-age same-age peers suggesting that this aspect of psychological well-being may be an important factor for exceptional cognitive aging. Investigation of the longitudinal effects of psychological well-being on subsequent cognitive performance and investigation of the conceivable relationship between psychological well-being and von Economo neurons in SuperAgers represent intriguing future directions.
S1 File. Supporting information.
This file contains the raw data used for analyses.
We would like to acknowledge our research participants for the time they devoted to this research project and Jaiashre Sridhar, M.S. for her technical assistance creating Fig 1.
- 1. Rogalski EJ, Gefen T, Shi J, Samimi M, Bigio E, Weintraub S, et al. Youthful memory capacity in old brains: anatomic and genetic clues from the Northwestern SuperAging Project. Journal of cognitive neuroscience. 2013;25(1):29–36. pmid:23198888; PubMed Central PMCID: PMC3541673.
- 2. Gefen T, Shaw E, Whitney K, Martersteck A, Stratton J, Rademaker A, et al. Longitudinal neuropsychological performance of cognitive SuperAgers. Journal of the American Geriatrics Society. 2014;62(8):1598–600. pmid:25116988; PubMed Central PMCID: PMCPMC4135532.
- 3. Harrison TM, Weintraub S, Mesulam MM, Rogalski E. Superior memory and higher cortical volumes in unusually successful cognitive aging. Journal of the International Neuropsychological Society: JINS. 2012;18(6):1081–5. pmid:23158231; PubMed Central PMCID: PMC3547607.
- 4. Fotenos AF, Snyder AZ, Girton LE, Morris JC, Buckner RL. Normative estimates of cross-sectional and longitudinal brain volume decline in aging and AD. Neurology. 2005;64(6):1032–9. pmid:15781822.
- 5. Resnick SM, Pham DL, Kraut MA, Zonderman AB, Davatzikos C. Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2003;23(8):3295–301. pmid:12716936.
- 6. Cook AH, Sridhar J, Ohm D, Rademaker A, Mesulam MM, Weintraub S, et al. Rates of Cortical Atrophy in Adults 80 Years and Older With Superior vs Average Episodic Memory. JAMA: the journal of the American Medical Association. 2017;317(13):1373–5. pmid:28384819.
- 7. Gefen T, Peterson M, Papastefan ST, Martersteck A, Whitney K, Rademaker A, et al. Morphometric and histologic substrates of cingulate integrity in elders with exceptional memory capacity. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2015;35(4):1781–91. pmid:25632151; PubMed Central PMCID: PMCPMC4308613.
- 8. Allman JM, Watson KK, Tetreault NA, Hakeem AY. Intuition and autism: a possible role for Von Economo neurons. Trends in cognitive sciences. 2005;9(8):367–73. pmid:16002323.
- 9. Seeley WW, Carlin DA, Allman JM, Macedo MN, Bush C, Miller BL, et al. Early frontotemporal dementia targets neurons unique to apes and humans. Annals of neurology. 2006;60(6):660–7. pmid:17187353.
- 10. Llewellyn DJ, Lang IA, Langa KM, Huppert FA. Cognitive function and psychological well-being: findings from a population-based cohort. Age Ageing. 2008;37(6):685–9. pmid:18852289; PubMed Central PMCID: PMCPMC2720691.
- 11. Klaming R, Veltman DJ, Comijs HC. The impact of personality on memory function in older adults-results from the Longitudinal Aging Study Amsterdam. International journal of geriatric psychiatry. 2016. pmid:27329835.
- 12. Boyle PA, Buchman AS, Barnes LL, Bennett DA. Effect of a purpose in life on risk of incident Alzheimer disease and mild cognitive impairment in community-dwelling older persons. Arch Gen Psychiatry. 2010;67(3):304–10. pmid:20194831; PubMed Central PMCID: PMCPMC2897172.
- 13. Windsor TD, Curtis RG, Luszcz MA. Sense of purpose as a psychological resource for aging well. Dev Psychol. 2015;51(7):975–86. pmid:26010384.
- 14. Seeman TE, Lusignolo TM, Albert M, Berkman L. Social relationships, social support, and patterns of cognitive aging in healthy, high-functioning older adults: MacArthur studies of successful aging. Health Psychol. 2001;20(4):243–55. pmid:11515736.
- 15. Krueger KR, Wilson RS, Kamenetsky JM, Barnes LL, Bienias JL, Bennett DA. Social engagement and cognitive function in old age. Exp Aging Res. 2009;35(1):45–60. pmid:19173101; PubMed Central PMCID: PMCPMC2758920.
- 16. Wang HX, Karp A, Winblad B, Fratiglioni L. Late-life engagement in social and leisure activities is associated with a decreased risk of dementia: a longitudinal study from the Kungsholmen project. Am J Epidemiol. 2002;155(12):1081–7. pmid:12048221.
- 17. Marioni RE, Proust-Lima C, Amieva H, Brayne C, Matthews FE, Dartigues JF, et al. Social activity, cognitive decline and dementia risk: a 20-year prospective cohort study. BMC Public Health. 2015;15:1089. pmid:26499254; PubMed Central PMCID: PMCPMC4619410.
Schmidt M. Rey Auditory Verbal Learning Test: A handbook. Torrance, CA: Western Psychological Services; 2004.
Kaplan E, Goodglass H., & Weintraub S. The Boston Naming Test. Philadelphia: Lea and Febiger; 1983.
- 20. Reitan RM. The relation of the trail making test to organic brain damage. Journal of consulting psychology. 1955;19(5):393–4. Epub 1955/10/01. pmid:13263471.
- 21. Morris JC, Heyman A., Mohs R.C., Hughes J.P., van Belle G., Fillenbaum G., Mellits E.D., & Clark C. The Consortium to Establish a Registry for Alzheimer’s Disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer’s disease. Neurology. 1989;39:1159–65. pmid:2771064
- 22. Ryff CD, Keyes CL. The structure of psychological well-being revisited. J Pers Soc Psychol. 1995;69(4):719–27. pmid:7473027.
- 23. Ryff CD. Happiness is everything, or is it? Explorations on the meaning of psychological well-being. Journal of Personality and Social Psychology. 1989;57(6):1069–81. PubMed PMID: 1990-12288-001.
- 24. Clarke PJ, Marshall VW, Ryff CD, Wheaton B. Measuring psychological well-being in the Canadian Study of Health and Aging. International Psychogeriatrics. 2001;13(Suppl1):79–90. 2002-00898-008.
- 25. Butti C, Santos M, Uppal N, Hof PR. Von Economo neurons: clinical and evolutionary perspectives. Cortex; a journal devoted to the study of the nervous system and behavior. 2013;49(1):312–26. pmid:22130090.
- 26. Zahodne LB, Nowinski CJ, Gershon RC, Manly JJ. Which psychosocial factors best predict cognitive performance in older adults? Journal of the International Neuropsychological Society: JINS. 2014;20(5):487–95. pmid:24685143; PubMed Central PMCID: PMCPMC4493753.
- 27. Pillemer SC, Holtzer R. The differential relationships of dimensions of perceived social support with cognitive function among older adults. Aging Ment Health. 2016;20(7):727–35. pmid:25902848; PubMed Central PMCID: PMCPMC4618790.
- 28. Beland F, Zunzunegui MV, Alvarado B, Otero A, Del Ser T. Trajectories of cognitive decline and social relations. The journals of gerontology Series B, Psychological sciences and social sciences. 2005;60(6):P320–P30. pmid:16260706.
- 29. Amieva H, Stoykova R, Matharan F, Helmer C, Antonucci TC, Dartigues J-F. What aspects of social network are protective for dementia? Not the quantity but the quality of social interactions is protective up to 15 years later. Psychosomatic Medicine. 2010;72(9). 2011-26511-010. pmid:20807876
- 30. Hughes TF, Flatt JD, Fu B, Chang C-CH, Ganguli M. Engagement in social activities and progression from mild to severe cognitive impairment: The MYHAT study. International Psychogeriatrics. 2013;25(4). 2013-06560-007. pmid:23257280
- 31. Lovden M, Ghisletta P, Lindenberger U. Social participation attenuates decline in perceptual speed in old and very old age. Psychology and aging. 2005;20(3):423–34. pmid:16248702.
Ryff CD, Almeida DM, J. A, Carr DS, Cleary PD, Coe C, et al. National Survey of Midlife Development in the United States (MIDUS II), 2004–2006. Ann Arbor, MI: Inter-university Consortium for Political and Social Research [distributor], 2012.
- 33. Ryff CD, Singer B. Psychological well-being: meaning, measurement, and implications for psychotherapy research. Psychother Psychosom. 1996;65(1):14–23. pmid:8838692.
- 34. Karasawa M, Curhan KB, Markus HR, Kitayama SS, Love GD, Radler BT, et al. Cultural perspectives on aging and well-being: a comparison of Japan and the United States. International journal of aging & human development. 2011;73(1):73–98. pmid:21922800; PubMed Central PMCID: PMCPMC3183740.