Abstract
Aims
We investigated whether the longitudinal relation between memory complaints and subsequent decline in executive functioning over 6 years differed by leisure activity engagement as major contributor to cognitive reserve in old age.
Methods
We analyzed longitudinal data from 897 older adults (M = 74.33 years) tested on the Trail Making Test (TMT) in two waves 6 years apart. Participants reported information on memory complaints and leisure activity engagement.
Results
There was a significant interaction of memory complaints with leisure activity engagement on latent change in executive functioning. Specifically, only for individuals with less (but not those with greater) leisure activity engagement, memory complaints significantly predicted a steeper subsequent decline in executive functioning across 6 years (i.e., increases in TMT completion time).
Conclusion
The role of memory complaints as an early predictor of decline in executive functioning seems to vary by individuals' cognitive reserve.
Keywords: Memory complaints, Decline in executive functioning, Cognitive reserve, Leisure activities
Introduction
Memory complaints are an early indicator of cognitive decline and cognitive impairments in midlife and old age [1, 2, 3]. Yet, the predictive role of memory complaints does not always seem to become evident [4] and thus may be dependent on other influencing factors such as the individual's amount of cognitive reserve. In general, the cognitive reserve concept [5] aims to explain individual differences in the course of aging and neurodegenerative development. Cognitive reserve is built up through cognitive stimulation and serves later on as buffer for coping with brain alterations in order to preserve cognitive functioning in aging [5]. In this regard, leisure activity engagement is a major contributor to the buildup of cognitive reserve in old age [5] and has for example found to be related to better executive functioning in healthy older adults [6, 7, 8].
Evidence showed that cognitive reserve is related to better cognitive functioning in individuals with memory complaints [9, 10]. Yet, research on the interplay of memory complaints with cognitive reserve to explain the diversity in results regarding the predictive role of memory complaints for subsequent cognitive decline is still in its infancy. For instance, there is no empirical longitudinal investigation to date regarding the role of cognitive reserve in modifying the long-term relation between memory complaints and decline in executive functioning over a broader time frame. Therefore, we investigated whether the longitudinal relation between memory complaints and subsequent decline in executive functioning over 6 years as measured through performance changes in the Trail Making Test (TMT) differed by leisure activity engagement as major contributor to cognitive reserve in old age.
Materials and Methods
Participants
We analyzed data from 897 individuals who participated in the two waves of the Vivre-Leben-Vivere (VLV) survey [11]. Respondents were first interviewed during 2011 (wave 1; W1) and again in 2017 (wave 2; W2) using face-to-face computer-assisted personal interviewing and paper-pencil questionnaires. For further details regarding the rationale, design, recruitment, materials, and procedures of the VLV survey, see [8, 11, 12, 13, 14]. Mean age of these respondents in W1 was 74.33 years (SD = 6.50, range 64–96); 51.4% were men.
Materials
In both waves, we administered the TMT parts A and B (TMT A and TMT B, respectively [15]). In W1, participants reported memory complaints as well as current leisure activity engagement at that time (see [8] for further methodological details).
Statistical Analyses
Using latent change score modeling, we modeled latent executive functioning factors of TMT completion time in W1 (constructed from TMT parts A and B in W1) and W2 (constructed from TMT parts A and B in W2) as well as a latent change in executive functioning variable regarding change in TMT completion time from W1 to W2. We included the following covariates to predict latent change: memory complaints in W1, leisure activity engagement in W1, age in W1, sex, and the interaction of memory complaints in W1 with leisure activity engagement in W1 (while taking the dependencies among all covariates into account).
Results
Memory complaints in W1 (β = 0.14, p < 0.001) and older age in W1 (β = 0.26, p < 0.001) significantly predicted a larger increase in TMT completion time from W1 to W2 (i.e., steeper decline in executive functioning). Sex and leisure activity engagement in W1 per se did not predict changes in TMT completion time (p > 0.05). Yet, most importantly, there was a significant interaction of memory complaints with leisure activity engagement (β = −0.25, p = 0.031). Specifically, for individuals with less leisure activity engagement in W1 (−1 SD), memory complaints in W1 significantly predicted a larger subsequent increase in TMT completion time from W1 to W2 (i.e., steeper decline in executive functioning, β = 0.21, p < 0.001). In contrast, for individuals with greater leisure activity engagement in W1 (+1 SD), this longitudinal relation between memory complaints in W1 and subsequent decline in executive functioning was not significant (β = 0.07, p = 0.241).
Discussion
To explain the diversity in results regarding the predictive role of memory complaints for subsequent cognitive decline [1, 2, 3, 4], present longitudinal results have important implications. Using latent change score modeling (extracting measurement-error variance), we demonstrated a substantial interaction of memory complaints with leisure activity engagement on subsequent latent change in executive functioning. Specifically, only for individuals with less (but not those with greater) leisure activity engagement, memory complaints significantly predicted a steeper subsequent decline in executive functioning across 6 years (i.e., indicated by increases in TMT completion time).
Our observations corroborate the key role of leisure activity engagement as major contributor to cognitive reserve for modifying the pathways of cognitive aging [5, 6, 7, 8, 16, 17, 18] and thereby its public importance [19, 20, 21]. In this regard, the present study reveals cognitive reserve as crucial factor moderating the predictive role of memory complaints for subsequent cognitive development. Specifically, our findings suggest that especially in vulnerable populations, such as in those with less cognitive reserve accumulated [22], memory complaints may serve as early indicator of decline in executive functioning, while in less vulnerable individuals, such as in those with greater cognitive reserve accumulated, this predictive role loses its strength.
Statement of Ethics
All participants gave their written informed consent for inclusion in the study before participating. The present study was conducted in accordance with the Declaration of Helsinki, and the study protocol had been approved by the ethics commission of the Faculty of Psychology and Social Sciences of the University of Geneva (project identification codes: CE_FPSE_14.10.2010 and CE_FPSE_05.04.2017).
Conflict of Interest Statement
The authors have no conflicts of interest to disclose.
Funding Sources
This work was supported by the Swiss National Centre of Competence in Research LIVES – Overcoming vulnerability: life course perspectives, granted by the Swiss National Science Foundation (grant number: 51NF40-185901). The APC of this article was financed by the Swiss National Science Foundation. E.R.G. and B.R.G. acknowledge support from LARSyS – Portuguese national funding agency for science, research and technology (FCT) pluriannual funding 2020–2023 (reference: UIDB/50009/2020). The funding sources had no role in the preparation of data or the manuscript. Moreover, the authors have not entered into an agreement with the funding organization that has limited their ability to complete the research as planned and publish the results. The authors have had full control of all the primary data.
Author Contributions
A.I., E.R.G., and B.R.G. formulated the research question, analyzed the data, and wrote the manuscript. M.K. formulated the research question, conceptualized the study, supervised the data collection, and participated in writing.
Acknowledgement
The authors are grateful to the Swiss National Science Foundation for its financial assistance. The authors also thank the participants of the Vivre-Leben-Vivere (VLV) study, as well as all members of the LIVES project IP213 and LINK institute who contributed to the realization of the VLV study.
References
- 1.Dardenne S, Delrieu J, Sourdet S, Cantet C, Andrieu S, Mathiex-Fortunet H, et al. Memory Complaints and Cognitive Decline: data from the GUIDAGE Study1. J Alzheimers Dis. 2017;60((4)):1567–78. doi: 10.3233/JAD-170229. [DOI] [PubMed] [Google Scholar]
- 2.Dik MG, Jonker C, Comijs HC, Bouter LM, Twisk JW, van Kamp GJ, et al. Memory complaints and APOE-epsilon4 accelerate cognitive decline in cognitively normal elderly. Neurology. 2001 Dec;57((12)):2217–22. doi: 10.1212/wnl.57.12.2217. [DOI] [PubMed] [Google Scholar]
- 3.Schaafsma M, Homewood J, Taylor A. Subjective cognitive complaints at menopause associated with declines in performance of verbal memory and attentional processes. Climacteric. 2010 Feb;13((1)):84–98. doi: 10.3109/13697130903009187. [DOI] [PubMed] [Google Scholar]
- 4.Weaver Cargin J, Collie A, Masters C, Maruff P. The nature of cognitive complaints in healthy older adults with and without objective memory decline. J Clin Exp Neuropsychol. 2008 Feb;30((2)):245–57. doi: 10.1080/13803390701377829. [DOI] [PubMed] [Google Scholar]
- 5.Stern Y. Cognitive reserve in ageing and Alzheimer's disease. Lancet Neurol. 2012 Nov;11((11)):1006–12. doi: 10.1016/S1474-4422(12)70191-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Opdebeeck C, Martyr A, Clare L. Cognitive reserve and cognitive function in healthy older people: a meta-analysis. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn. 2016;23((1)):40–60. doi: 10.1080/13825585.2015.1041450. [DOI] [PubMed] [Google Scholar]
- 7.Wang HX, Jin Y, Hendrie HC, Liang C, Yang L, Cheng Y, et al. Late life leisure activities and risk of cognitive decline. J Gerontol A Biol Sci Med Sci. 2013 Feb;68((2)):205–13. doi: 10.1093/gerona/gls153. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Ihle A, Grotz C, Adam S, Oris M, Fagot D, Gabriel R, et al. The association of timing of retirement with cognitive performance in old age: the role of leisure activities after retirement. Int Psychogeriatr. 2016 Oct;28((10)):1659–69. doi: 10.1017/S1041610216000958. [DOI] [PubMed] [Google Scholar]
- 9.Lojo-Seoane C, Facal D, Guàrdia-Olmos J, Juncos-Rabadán O. Structural model for estimating the influence of cognitive reserve on cognitive performance in adults with subjective memory complaints. Arch Clin Neuropsychol. 2014 May;29((3)):245–55. doi: 10.1093/arclin/acu007. [DOI] [PubMed] [Google Scholar]
- 10.Lojo-Seoane C, Facal D, Guàrdia-Olmos J, Pereiro AX, Juncos-Rabadán O. Effects of Cognitive Reserve on Cognitive Performance in a Follow-Up Study in Older Adults With Subjective Cognitive Complaints. The Role of Working Memory. Front Aging Neurosci. 2018 Jun;10:189. doi: 10.3389/fnagi.2018.00189. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Ihle A, Zuber S, Gouveia ÉR, Gouveia BR, Mella N, Desrichard O, et al. Cognitive Reserve Mediates the Relation between Openness to Experience and Smaller Decline in Executive Functioning. Dement Geriatr Cogn Disord. 2019;48((1-2)):39–44. doi: 10.1159/000501822. [DOI] [PubMed] [Google Scholar]
- 12.Ihle A, Oris M, Fagot D, Chicherio C, van der Linden BW, Sauter J, et al. Associations of educational attainment and cognitive level of job with old age verbal ability and processing speed: the mediating role of chronic diseases. Appl Neuropsychol Adult. 2018 Jul-Aug;25((4)):356–62. doi: 10.1080/23279095.2017.1306525. [DOI] [PubMed] [Google Scholar]
- 13.Ihle A, Oris M, Fagot D, Kliegel M. The relation of the number of languages spoken to performance in different cognitive abilities in old age. J Clin Exp Neuropsychol. 2016 Dec;38((10)):1103–14. doi: 10.1080/13803395.2016.1197184. [DOI] [PubMed] [Google Scholar]
- 14.Ihle A, Mons U, Perna L, Oris M, Fagot D, Gabriel R, et al. The Relation of Obesity to Performance in Verbal Abilities, Processing Speed, and Cognitive Flexibility in Old Age: The Role of Cognitive Reserve. Dement Geriatr Cogn Disord. 2016;42((1-2)):117–26. doi: 10.1159/000448916. [DOI] [PubMed] [Google Scholar]
- 15.Reitan RM. Validity of the Trail Making Test as an indicator of organic brain damage. Percept Mot Skills. 1958 Dec;8((3)):271–6. [Google Scholar]
- 16.Ihle A, Gouveia ÉR, Gouveia BR, Freitas DL, Jurema J, Odim AP, et al. The relation of education, occupation, and cognitive activity to cognitive status in old age: the role of physical frailty. Int Psychogeriatr. 2017 Sep;29((9)):1469–74. doi: 10.1017/S1041610217000795. [DOI] [PubMed] [Google Scholar]
- 17.Ihle A, Gouveia ÉR, Gouveia BR, Freitas DL, Jurema J, Tinôco MA, et al. High-Density Lipoprotein Cholesterol Level Relates to Working Memory, Immediate and Delayed Cued Recall in Brazilian Older Adults: The Role of Cognitive Reserve. Dement Geriatr Cogn Disord. 2017;44((1-2)):84–91. doi: 10.1159/000477846. [DOI] [PubMed] [Google Scholar]
- 18.Ihle A, Gouveia ÉR, Gouveia BR, Freitas DL, Jurema J, Machado FT, et al. The Relation of Hypertension to Performance in Immediate and Delayed Cued Recall and Working Memory in Old Age: The Role of Cognitive Reserve. J Aging Health. 2018 Sep;30((8)):1171–87. doi: 10.1177/0898264317708883. [DOI] [PubMed] [Google Scholar]
- 19.Ihle A, Borella E, Rahnfeld M, Müller SR, Enge S, Hacker W, et al. The role of cognitive resources for subjective work ability and health in nursing. Eur J Ageing. 2015 Jan;12((2)):131–40. doi: 10.1007/s10433-014-0331-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Schnitzspahn KM, Scholz U, Ballhausen N, Hering A, Ihle A, Lagner P, et al. Age differences in prospective memory for everyday life intentions: A diary approach. Memory. 2016;24((4)):444–54. doi: 10.1080/09658211.2015.1018276. [DOI] [PubMed] [Google Scholar]
- 21.Suzman R, Beard JR, Boerma T, Chatterji S. Health in an ageing world—what do we know? Lancet. 2015 Feb;385((9967)):484–6. doi: 10.1016/S0140-6736(14)61597-X. [DOI] [PubMed] [Google Scholar]
- 22.Ihle A, Oris M, Sauter J, Rimmele U, Kliegel M. Cognitive Reserve and Social Capital Accrued in Early and Midlife Moderate the Relation of Psychological Stress to Cognitive Performance in Old Age. Dement Geriatr Cogn Disord. 2018;45((3-4)):190–7. doi: 10.1159/000488052. [DOI] [PubMed] [Google Scholar]