Effects of individual experience on prevention and compensation of age-related cognitive decline: neural and behavioral evidence тема диссертации и автореферата по ВАК РФ 19.00.02, кандидат наук Галло Федерико

• Галло Федерико
• кандидат наук
• 2022

Оглавление диссертации кандидат наук Галло Федерико

Table of Contents

Approbation and introduction of results

1 Introduction

1.1 Research problem

1.2 Goals of the dissertation

1.3 Research methodology

1.4 Scientific novelty

1.4.1 Main aspects of theoretical novelty

1.4.2 Main aspects of methodological novelty

1.5 Theoretical and practical significance

1.5.1 Theoretical significance

1.5.2 Practical implications

1.6 Key ideas to be defended

1.7 Author contribution

2 Summary of the dissertation

2.1 Introduction

2.2 Overview of the scientific content

2.2.1 Study 1. Bilingualism boosts cognitive reserve during late life stages

2.2.2 Study 2. Individual differences in bilingual experience modulate the executive control network and performance

2.2.3 Study 3. How to measure cognitive reserve efficiently? A comparison of two approaches to cognitive reserve operationalization

3 Conclusions

4 References

Appendices

Appendix A - Article «Neuroplasticity across the lifespan and aging effects in bilinguals

and monolinguals»

Appendix B - Article «Individual differences in bilingual experience modulate executive control network and performance: Behavioral and structural neuroimaging evidence». . 45 Appendix C - Article «Cognitive trajectories and dementia risk: A comparison of two cognitive-reserve measures»

Введение диссертации (часть автореферата) на тему «Effects of individual experience on prevention and compensation of age-related cognitive decline: neural and behavioral evidence»

1 Introduction

1.1 Research problem

Average life expectancy has been steadily increasing worldwide over the last decades (Kontis et al., 2017). Alongside the advantages of an extended life span, this phenomenon brings about some undesirable consequences, including an ever-growing incidence of age-related deficits and disorders - most notably, dementia - and consequent increases in the expenditures for public governments' welfare systems (Wimo et al., 2017). At the neural level, aging has been linked to structural as well as functional changes (Walhovd et al., 2011), resulting in cognitive impairments (Lindenberger, 2014). Nonetheless, considerable interindividual variability has emerged in the degree of cognitive decline resulting from age-related brain damage (Cosentino & Stern, 2019). Based on existing evidence, several mechanisms of preservation and compensation of age-related cognitive impairment have been proposed. The main theoretical framework centers around the concept of cognitive reserve, defined as the level of resilience of an individual's cognitive processes to age-related brain deterioration (Stern et al., 2020). Whereas much is yet to be understood regarding the nature of cognitive reserve, what is known is that it develops gradually during the lifespan and is supported by a number of experiential factors (Stern, 2009), including maximal educational attainment, occupational complexity, and the extent of the individual's social network (Dekhtyar et al., 2019). One factor that has been linked to the build-up of cognitive reserve is bilingualism (Gallo et al., 2020; Gallo, DeLuca, et al., 2022): by means of a constant additional cognitive effort required to control dual-language use (Kroll et al., 2015), bilinguals strengthen their neural substrate - both at the structural and the functional levels (Abutalebi & Green, 2016; Bialystok, 2017). This is believed to result in a protective effect that counteracts age-related cognitive decline and is mediated by the cognitive reserve mechanism (Del Maschio et al., 2018; Gallo, Kubiak, et al., 2022).

The main aim of this dissertation was to examine the role of individual life experiences, bilingualism in particular, in promoting the development of cognitive reserve during the whole lifespan. Moreover, with the aim of tackling the long-standing issue of cognitive reserve measurability, I devised a novel method (by refining recent approaches) for measuring cognitive reserve directly and tested its validity by comparing it with traditional approaches to cognitive reserve measurement, for the first time in the literature.

1.2 Goals of the dissertation

1. To examine the role of bilingualism as a factor supporting the development of cognitive reserve during senescence;

2. To shed light on the mechanisms underlying bilingualism's effects on cognitive reserve, both at the neurostructural and behavioral levels;

3. To illuminate the relationship between bilingualism-induced consequences for the brain and bilingualism-induced consequences for cognition, and clarify how individual differences in bilingual experience may modulate such a relationship;

4. To investigate whether bilingualism-induced effects on cognitive reserve commence in youth or are exclusive to late life stages;

5. To devise a novel methodological approach to the operationalization and measurement of cognitive reserve;

6. To test the validity of this novel approach and compare its predictive power with that of traditional approaches.

1.3 Research methodology

Overall, 540 participants, including 66 young adults (18-35 years old) and 474 seniors (60+ years old) were included in the three investigations. For each of the three studies, participants signed informed consent before taking part in the experiments. All experiments were approved by ethical committees: Study 1 was approved by The Human

Research Ethics Committee at the University of Hong Kong and The Human Research Ethics Committee at Universita Vita-Salute San Raffaele, Study 2 was approved by the Institutional Review Board of the Higher School of Economics, and Study 3 was approved by The Regional Ethical Review Board in Stockholm.

Studies 1 and 2 adopted a cross-sectional design, while Study 3 was based on data from a longitudinal investigation. All experiments deployed structural magnetic resonance imaging (MRI). Studies 1 and 2 used a region-of-interest (ROI), atlas-based morphometry approach, while Study 3 adopted a whole-brain voxel-based morphometry (VBM) approach. Neuroimaging data analyses software packages utilized in the three studies included SPM 123, FreeSurfer 5.14 and CAT12 (Gaser & Dahnke, 2016).

Cognitive assessments deployed in the three studies included the Flanker Task (Fan et al., 2005), the digit cancellation task (Zazzo, 1974), the pattern comparison task (Salthouse & Babcock, 1991), word recall and word recognition tasks for episodic memory (Laukka et al., 2013), semantic memory tasks (Dureman, 1960; Nilsson et al., 1997), letter fluency and category fluency tasks, and the Mini-Mental State Examination (MMSE; Cockrell & Folstein, 2002). Stimulus presentation and response collection software used for cognitive assessment included NBS Presentation 18.1 (Neurobehavioral Systems, Inc., 2020) and Opensesame 3.0 (Mathot et al., 2012).

Statistical methods utilized in the three studies included Structural Equation Modeling, linear and logistic mixed-effects regressions and Cox proportional hazard models. The statistical analysis software utilized in the three studies included R (R Core Team, 2013) and Stata16 (StataCorp., 2017).

3 https://www.fil.ion.ucl.ac.uk/spm/

4 http://surfer.nmr.mgh.harvard.edu/

Заключение диссертации по теме «Психофизиология», Галло Федерико

CONCLUSION

In conclusion, we showed that residual-based CR derived in a population-based study of older adults was (1) associated with cognitive trajectories over 12 years of follow-up, (2) mitigated the impact of impaired brain integrity on cognitive decline, and (3) predicted dementia incidence even after accounting for brain-integrity status. In contrast, an activity-based measure derived from stimulating life experiences neither mitigated the brain integrity-cognitive change association, nor did it emerge as a predictor of dementia independent of brain integrity. Our findings provide insight into future applications of CR models of cognitive change and dementia. Both approaches possess unique advantages that can be tailored to address different aims. Ultimately, any model of CR needs to consider brain integrity, and the term reserve should be used when the measure in question modifies the link between brain integrity and cognitive outcomes or predicts dementia independent of brain integrity. In our study, only a residual-based measure of reserve fulfilled this requirement.

Список литературы диссертационного исследования кандидат наук Галло Федерико, 2022 год

REFERENCES

Altieri, M., Sicäliano, M,, Pappacena, S„ Roldän-Tapia, M, D„ Trojan o, I , and Santangelo, Cj. (2018). Psychometric properties of the Italian version of the Cognitive Reserve Scale (ICRS). Neurol Sei. 39, 1383-1390. doi: 10.1007/ sl0072-018-3432-0

Arenaza Urquijo, E. M., and Vemuri, P. (2018). Resistance vs resilience to Alzheimer disease: clarifying terminology for preclinical studies. Neurology 90, 695-703. doi: 10.1212/wnl.OOCOOOOD00005303

Barulli, D., and Stern, Y. (2013). Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn. S ci. 17, 502509. doi: 10.1016/j.tics.20l3<08,012 Iîerggren, R., Nilsson, J., and I^ovdén, M. (2018). Education does not affect cognitive decline in aging: a bayesian assessment of the association between education and change in cognitive performance, front. Psychol. 9:1138. doi: 10J389/fpsyg.2018.01138 Bcttchcr, B. M., Gross, A. L., Gavelt, B. E„ Widaman, K. F., Fletcher, E„ Dowling, N. M., et al. (2019). Dynamic change of cognitive reserve: associations with

changes in brain, cognition, and diagnosis. Neurobiol. Aging 83, 95-104. doi: 1(X I016/j,ncurobiolaging,2019.08.016 Bocancea, D. I., Cal harina van Loenhoud, A., Groot, C., Barkhof, F., van der Flier, W. M., and Ossenkoppele, R. (2021). Measuring resilience and rcsisiancc in aging and al/.heimer disease using residual methods: a systematic review and meta-analysis. Mruroio^doi: 10.1212/WN1 ,.0000000000012499 Cabeza, R„ Albert, M., Belleville, S., Craik, F, 1. M,. Duarte, A„ Grady, C. L„ et al. (2019). Reply to 'Mechanisms underlying resilience in ageing'. Nat. Rev. Neurosci. 20:247. doi: 10.l038/s4l 583-019-0139-z Cabeza, R., Albert, M., Belleville, S., Craik, F. I. M., Duarte, A., Grady, C. L., et al. (2018). Maintenance, reserve and compensation: the cognitive neuroscience of heaJlhy ageing. Nat. Rev. Neurosci. 19, 701-710. doi: 1Ü. 1038/s41583-018-0068-2

Cosemino, S., and Stem, Y. (2019). "Consideration of cogniiivc reserve," in Handbook on the Neuropsychology of Aging and Dementia. Clinical Handbooks in Neuropsychology, eds I,. Ravdin and H. Kalxen (Cham: Springer). 11-23. doi: 10.1007/978- 3-319-93 497- 6_2 Dekhtyar, S., Marseglia, A., Xu, W., Darin-Mattsson, A., Wang, H., and Fratiglioni, L. (2019). ). Genetic risk of dementia mitigated by cognitive reserve: a cohort study. Ann. Neurol. 86, ana.25501. doi: 10.1(>02/ana.25501 Dureman, I. (1960). SR£:1. Stockhohn. Sweden: Psykologiforlaget. Fcrencz, B., Laukka, E. I., Lovdén, M., Kalpouzos, G., Keller, L., Graff, C., et al. (2013). The influence of APOE and TOMM4Ü polymorphisms on hippocampal volume and episodic memory in old age. Front. Hum. Neurosci. 7:198. doi: 10,3389/fnhum.2013.00198 Fischl, B., Salat, D. H,. Busa, E„ Albert, M„ Dielerich, M., Haselgrove, C, ct al. (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341-355. doi: 10.1016/S0896-6273(02)00569-X

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. /. Psychiatr. Res. 12,189-198. Fratiglioni, L., Viitanen, M., von Strauss, E., Tontodonali, V., Herlitz, A., and Winblad, B. (1997). Very old women at highest risk of dementia and Alzheimer's disease: incidence data from the Kungsholmen Project, Stockholm. Neurology 48,132-138. doi: 10.1212/wnl.48.1.132 Frisoni, G. B., Fox, N. C., Jack, C R., Scheltens, P., and Thompson, P. M. (2010). The clinical use of structural MR! in Alzheimer disease, Nat. Rev. Neurol. 6, 67-77. doi: 10.1038/nrneurol.2009.215 Habeck, C, Razlighi, Q., Gazes, Y., Barulli, D., Steffener, J., and Stern, Y. (2017). Cognitive reserve and brain maintenance: orthogonal concepts in theory and practice. Cereb. Cortex 27> 3962-3969. doi: 10.1093/cercor/bhw208 Hohman, T. J., McLaren, D. G„ Mormino, E. C., Gifford, K, A., Libón, D. J., and JefTerson, A. L (2016). Asymptomatic Alzheimer disease. Neurology 87, 2443-2450. doi: 10J212/WNL.0000000000003397 Jack, C. R., Twomev, C, K„ Zinsmeister, A. R., Sharbrough, F. W„ Petersen, R. C., and Cascino, G. D. (1989). Anterior temporal lobes and hippocampal formations: normative volumetric measurements from MR images in young adults. Radiology 172,549-554. doi: 10.1148/radiology. 172.2.2748838 Jan.se, E. (2012). A non-auditory measure of interference predicts distraction by competing speech in older adults. Aging Neuropsychol. Cogn. 19, 741-758. doi: 10.1080/13825585.2011.652590 Tones, R. N.. Manly, I,, Glymour, M. M„ Rent/., D. M„ JclFcrson, A, L, and Stern, Y. (2011). Conceptual and measurement challenges in research on cognitive reserve. /. Int. Neuropsychol Soc. 17> 593-601. doi: 10.1017/ S1355617710001748

Kalpouzos, G.» and Nyberg, 1,. (2012). "Multimodal neuroimaging in normal aging: structure-function interactions," in Memoiy and Aging, eds M. Naveh-Benjamin and N. Ohta (London: Psychology Press), 285-316. doi: 10.4324/ 9780203156513-20

Kempton, M. J., Underwtxxl, T, S. A., Brunton, S„ Stylios, F., Sehmechtig, A., Ettinger, U., et al. (2011). A comprehensive testing protocol for MRI neuroanatomical segmentation techniques: evaluation of a novel lateral ventricle segmentation method. Neuroimage 58, 1051-1059. doi: 10.1016/j. neuroimage. 2011.06.080 Kohncke, Y., Laukka, E. J., Brehmer, Y., Kalpouzos, G., Li, T. Q., Fraliglioni, L., el al. (2016). Three-year changes in leisure activities are associated with concurrent changes in while matter microslructure and perceptual speed in

individuals aged 80 years and older. Neurobiol. Aging 41,173-186. doi: 10.1016/ j,neurobiolaging,2016.02.013 Lagergren, M., Fratiglioni, L., Hallberg, I. R., Berglund, ]., ElmsLáhl, S., Hagberg, B., el al. (2004). A longitudinal sludy integrating populalion, care and social services data. The Swedish National sludy on Aging and Care (SNAC). A^mg Clin. Exp. Res. 16,158-168. doi: 10.1007/BF03324546 Laukka, F„ j„ Kohncke, Y„ Papenberg, G., Fratiglioni, 1... and Backman, I.. (2020). Combined genetic influences on episodic memory decline in older adults without dementia. Neuropsychology 34, 654-666. doi: I0.1037/neu00 00637

Laukka, E. J., Lovden, M., Herlitz, A., Karlsson, S., Ferencz, B., Pantzar, A., et al. (2013). Genetic effects on old-age cognitive functioning: a popula lion-based study. Psychol. Aging 28,262-274. doi: 10.1037/a0030829 Laveskog, A., Wang, R., Bronge, L., Wahlund, L. O., and Qiu, C. (2018). Perivascular spaces in old age: assessment, distribuí ion, and correlation with while matter hyperintensilies. Am. J. Neuroradiol. 39,70-76. doi: 10.3174/ainr. A5455

León, L, García-García, J., and Roldán-Tapia, L. (2014). Estimating cognitive reserve in healthy adults using the cognitive reserve scale. PLoS One 9:el02632. doi: 10.1371/jouinal.pone.Ol 02632 Lindenberger, U. (2014). Human cognitive aging: corriger la fortune? Science 346,

572-578. doi: 10.1126/science.l254403 Lovdén, M.; Fratiglioni, L., Glymour, M. M., Lindenberger, U., and Tucker-Drob, E. M. (2020). Education and cognitive functioning across the life span. Psychol Sci. Public Interest 21,6-41. doi: 10.1177/1529100620920576 Maiovis, P., Joannidis, P., Nueei, M„ Gotzamani-Psarrakou, A., and Karacostas, D. (2016). Adaptation of the Cognitive Reserve Index Questionnaire (CRIq) for the Greek population. Neurol. Sci. 37, 633-636. doi: 10.1007/sl0072-015-2457-x Marseglia, A., Fratiglioni, L., Kalpouzos, G., Wang, R., Backman, L., and Xu, W. (2019). Prediabetes and diahetes accelerate cognitive decline and predict microvascular lesions: a population-based cohort study. AlzheimersDement 15, 25-33. doi: 10.1016/j.jaIz.2018.06.3060 Nelson, M. E., Jester, D. J., Pelkus, A. J., and Andel, R. (2021). Cognitive reserve, alzheimers neuropathology, and risk of dementia: a systematic review and meta-analysis. Neuropsychol Rev. 31, 233-250. doi: 10,10Q7/sl 1065-02109478-4

Nilsson, L. G., Backman, L., Emgrund, K., Nyberg, L., Adolfsson, R., Bucht, G., et al. (1997). The betula prospective cohort study: memory, health, and aging. Aging Neuropsychol. Cogn. 4, 1-32. doi: 10.1080/13825589708256633 Nucci, M„ Mapelli, D., and Montlini, S. (2012). Cognitive Reserve Index questionnaire (CRIq): a new instrument for measuring cognitive reserve. Aging Clin. Exp. Res. 24,218-226. doi: 10.3275/7800 Nyberg, L., Lovdén, M., Riklund, K., Lindenberger, U., and Backman, L. (2012).

Memory aging and brain maintenance. Trends Cogn. Sci, 16,292-305, Pettigrew, C., and Soldán, A, (2019). Defining cognitive reserve and implications for cognitive aging, Curr.Neurol Neurosci Rep. 19:1. doi: 10.1007/sll 910-019 0917-z

Reed, B. R., Miingas, D., Farias, S. i'., Harvey, D., Beckett, L., Widaman, K., et al. (2010). Measuring cognitive reserve based on the decomposition of episodic memory variance. Brain 133, 2196-2209. doi: 10.1093/brain/ awql54

Salthousc, T. A., and Babcock, R. L. (1991). Decomposing adull age differences in working memory. Develop. Psychol 27, 763-776, doi: 10.1037/0012-1649.27.5. 763

Seblova, D„ Berggren, R., and Lovdén, M. (2020), Education and age-related decline in cognitive performance: systematic review and meta-analysis of longitudinal cohort studies, AgeingRes. Rev. 58,101005. doi: 10.l016/j.arr.2019. 101005

Steffener, J„ Reuben, A., Rakitin, B. C, and Stern, Y. (2011). Supporting performance in the face of age-related neural changes: testing mechanistic roles of cognitive reserve. Brain Imaging Behuv. 5,212-221. doi: K).ltK)7/sll682-011-9125-4

Stem, Y. (2009). Cognitive reserve. Neuropsychohgia 47,2015-2028. doi: 10.1016/

j.neuropsychologia.2009.03 004 Stern, Y., Arenaza Urquijo, E. M., Bartrés-Faz, D., Belleville, S., Cantilon, M., Chctclat, G., ct al. (2020). Whitcpapcr: defining and investigating cognitive reserve, brain reserve, and brain maintenance. Alzheimers Dement. 16, 1305— 1311. doi: 10.1016/j.jalz.2018.07.219

Stern, Y., Chételat, G,, Habeck, C., Arenaza-Urquijo, E. M., Vcmuri, P., Estanga, A.} et al, (2019). Mechanisms underlying resilience in ageing. Nat, Rev, Neurosci. 20:246.

van Locnhoud, A. C., Wink, A. M., Groot, C., Verfaillie, S. C. J., Twisk, J., Barkhof, P., cL al. (2017). A ncuroimaging approach to capture cognitive reserve: application to Alzheimer's disease. Hum. Brain Mapp. 38, 4703-4715. doi: 10. 1002/hbm ,23695

Walhovd, K. B„ Westlye, L. T., Amlien, I., Espeseth, T., Reinvang, I., Ra7.v N„ et al. (2011). Consistent neuroanatomical age-related volume differences across multiple samples, Neurobiol. Aging 32, 916-932.

Wang, H.-X., MacDonald, S. W. S., Deklityar, S., and Fratiglioni, L. (2017). Association of lifelong exposure to cognitive reserve-enhancing factors with dementia risk: a communhy-based cohort study. PLoS Med. L4:ol002251. doi: 10.1371/journal.pmcd. 1002251 Wardlaw, T. M.. Smith, E. E., Biessels, G. J., Cordonnier. C.. Pazekas, F., Frayne, R., et al. (2013). Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurode generation. Lancet Neuroi 12» 822-838. doi: 10.1016/S 1474-4422(13)70124-8 Xu, H., Yang, R., Qi, X., Dintica, C, Song, R„ Bennett, D. A., et al (2019). Association of lifespan cognitive reserve indicator with dementia risk in the presence of brain pathologies. ÏAMA Neurol. 76, 1184-1191. doi: 10.1001/ jamaneurol.20i9.2455 Zahodne, L. B., Manly, J. J., Bricknian. A. M.> Narklicde, A., Griffith, E. Y., Guzman, V. A., ct al. (2015). Is residual memory variance a valid method for quantifying cognilivc reserve? A longitudinal application.

Ncuwpsychologia 77, 260-266. doi: 10.1016/j Jieuropsychologia.2015. 09.009

Zahodne, L. B., Manly, J. J., Brickman, A. M., Siedlecki, K. L., Decarli, C., and Stern, Y. (2013). Quantifying cognitive reserve in older adults by decomposing episodic memory variance: replication and extension. /. Int. Neuropsyckol. Soc. 19,854-862. doi: 10.1017/S1355617713000738 Za7.zo, R. (1974). Test Des Deux Barrages, Actualités Pédagogiques F.t Psychologiques. Neuchâtel: Delachaux et Nestlé.