Abstract
Despite the relevance of semantic fluency measures to risk for dementia and psychiatric disorders, little is known about their genetic and environmental architecture in mid-to-late life. Participants represent 21,684 middle-aged and older adult twins (M = 60.84 years, SD = 11.21; Range 40-89) from six studies from three countries participating in the Interplay of Genes and Environment across Multiple Studies (IGEMS) consortium. All completed the same measure of semantic fluency (naming animals in 60 seconds). Results revealed small-to-moderate phenotypic associations with age and education, with education more strongly and positively associated with fluency performance in females than males. Heritability and environmental influences did not vary by age. Environmental variance was smaller with higher levels of education, but this effect was observed only in males. This is the largest study to examine the genetic and environmental architecture of semantic fluency, and the first to demonstrate that environmental influences vary based on levels of education.
Similar content being viewed by others
References
Ahrenfeldt LJ, Lindahl-Jacobsen R, Rizzi S, Thinggaard M, Christensen K, Vaupel JW (2018) Comparison of cognitive and physical functioning of Europeans in 2004–05 and 2013. Int J Epidemiol 47:1518–1528. https://doi.org/10.1093/ije/dyy094
Alexander KL, Eckland BK (1974) Sex differences in the educational attainment process. Am Sociol Rev 39:668–682. https://doi.org/10.2307/2094313
Alley D, Suthers K, Crimmins E (2007) Education and cognitive decline in older americans: results from the AHEAD sample. Research on Aging 29:73–94. https://doi.org/10.1177/0164027506294245
Barry TR (2014) The Midlife in the United States (MIDUS) series: A national longitudinal study of health and well-being. Open Health Data 2
Bates TC, Lewis GJ, Weiss A (2013) Childhood socioeconomic status amplifies genetic effects on adult intelligence. Psychol Sci 24:2111–2116. https://doi.org/10.1177/0956797613488394
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Statist Software. https://doi.org/10.18637/jss.v067.i01
Bates TC, Hansell NK, Martin NG, Wright MJ (2016) When does socioeconomic status (SES) moderate the heritability of IQ? No evidence for g × SES interaction for IQ in a representative sample of 1176 Australian adolescent twin pairs. Intelligence 56:10–15. https://doi.org/10.1016/j.intell.2016.02.003
Beam CR, Kaneshiro C, Jang JY, Reynolds CA, Pedersen NL, Gatz M (2018) Differences between women and men in incidence rates of dementia and Alzheimer’s disease. J Alzheimer’s Dis 64:1077–1083. https://doi.org/10.3233/JAD-180141
Boots EA, Schultz SA, Almeida RP, Oh JM, Koscik RL, Dowling MN, Bendlin BB (2015) Occupational complexity and cognitive reserve in a middle-aged cohort at risk for Alzheimer’s disease. Arch Clin Neuropsychol 30:634–642
Bratko D (1996) Twin study of verbal and spatial abilities. Personal Individ Diff 21:621–624. https://doi.org/10.1016/0191-8869(96)00091-8
Briley DA, Harden KP, Bates TC, Tucker-Drob EM (2015) Nonparametric estimates of gene x environment interaction using local structural equation modeling. Behav Genet 45:581–596. https://doi.org/10.1007/s10519-015-9732-8
Christensen K, Holm NV, McGue M, Corder L, Vaupel JW (1999) A danish population-based twin study on general health in the elderly. J Ag Health 11:49–64. https://doi.org/10.1177/089826439901100103
Dekhtyar S, Wang HX, Fratiglioni L, Herlitz A (2016) Childhood school performance, education and occupational complexity: A life-course study of dementia in the Kungsholmen Project. Int J Epidemiol 45:1207–1215. https://doi.org/10.1093/ije/dyw008
Giubilei F, Medda E, Fagnani C, Bianchi V, De Carolis A, Salvetti M, Stazi MA (2008) Heritability of neurocognitive functioning in the elderly: evidence from an Italian twin study. Age Ag 37:640–646. https://doi.org/10.1093/ageing/afn132
Gustavson DE, Panizzon MS, Elman JA, Beck A, Franz CE, Reynolds CA, Kremen WS (2018) Genetic and environmental influences on verbal fluency in middle age: A longitudinal twin study. Behav Genet 48:361–373. https://doi.org/10.1007/s10519-018-9910-6
Gustavson DE, Panizzon MS, Franz CE, Reynolds CA, Corley RP, Hewitt JK, Friedman NP (2019) Integrating verbal fluency with executive functions: evidence from twin studies in adolescence and middle age. J Exp Psychol: General 148:2104–2119. https://doi.org/10.1037/xge0000589
Henry JD, Crawford JR (2004) Verbal fluency deficits in Parkinson’s disease: a meta-analysis. J Int Neuropsychol Soc 10:608–622. https://doi.org/10.1017/S1355617704104141
Henry JD, Crawford JR (2004) A meta-analytic review of verbal fluency performance following focal cortical lesions. Neuropsychology 18:284–295. https://doi.org/10.1037/0894-4105.18.2.284
Henry JD, Crawford JR (2005) A meta-analytic review of verbal fluency deficits in schizophrenia relative to other neurocognitive deficits. Cognit Neuropsychiatry 10:1–33. https://doi.org/10.1080/13546800344000309
Henry JD, Crawford JR (2005) A meta-analytic review of verbal fluency deficits in depression. J Clin Exp Neuropsychol 27:78–101. https://doi.org/10.1080/138033990513654
Henry JD, Crawford JR, Phillips LH (2004) Verbal fluency performance in dementia of the Alzheimer’s type: a meta-analysis. Neuropsychologia 42:1212–1222. https://doi.org/10.1016/j.neuropsychologia.2004.02.001
Kremen WS, Franz CE, Lyons MJ (2013) VETSA: the vietnam era twin study of aging. Twin Res Human Genet 16:399–402. https://doi.org/10.1017/thg.2012.86
Kremen WS, Beck A, Elman JA, Gustavson DE, Reynolds CA, Tu XM, Franz CE (2019) Influence of young adult cognitive ability and additional education on later-life cognition. Proceed Natl Acad Sci 116:2021–2026. https://doi.org/10.1073/pnas.1811537116
Kunkle BW, Grenier-Boley B, Sims R, Bis JC, Damotte V, Naj AC, Environmental Risk for Alzheimer’s Disease C (2019) Genetic meta-analysis of diagnosed Alzheimer’s disease identifies new risk loci and implicates Abeta, tau, immunity and lipid processing. Nat Genet 51:414–430. https://doi.org/10.1038/s41588-019-0358-2
Lee T, Mosing MA, Henry JD, Trollor JN, Ames D, Martin NG, Team O. R (2012) Genetic influences on four measures of executive functions and their covariation with general cognitive ability: the older australian twins study. Behav Genet 42(528):538. https://doi.org/10.1007/s10519-012-9526-1
Lee T, Thalamuthu A, Henry JD, Trollor JN, Ames D, Wright MJ (2018) Genetic and environmental influences on language ability in older adults: findings from the older australian twins study. Behav Genet. https://doi.org/10.1007/s10519-018-9897-z
Markon KE, Krueger RF (2004) An empirical comparison of information-theoretic selection criteria for multivariate behavior genetic models. Behav Genet 34:593–610. https://doi.org/10.1007/s10519-004-5587-0
Mielke MM, Vemuri P, Rocca WA (2014) Clinical epidemiology of Alzheimer’s disease: assessing sex and gender differences. Clin Epidemiol 6:37–48. https://doi.org/10.2147/CLEP.S37929
Neale MC, Hunter MD, Pritikin JN, Zahery M, Brick TR, Kirkpatrick RM, Boker SM (2016) OpenMx 2.0: Extended structural equation and statistical modeling. Psychometrika 81:535–549. https://doi.org/10.1007/s11336-014-9435-8
Nyberg L, Lovden M, Riklund K, Lindenberger U, Backman L (2012) Memory aging and brain maintenance. Trends Cognit Sci 16:292–305. https://doi.org/10.1016/j.tics.2012.04.005
Osler M, McGue M, Lund R, Christensen K (2008) Marital status and twins’ health and behavior: an analysis of middle-aged Danish twins. Psychosom Med 70:482–487. https://doi.org/10.1097/PSY.0b013e31816f857b
Pahlen S, Hamdi NR, Dahl Aslan AK, Horwitz BN, Panizzon MS, Petersen I, McGue M (2018) Age-moderation of genetic and environmental contributions to cognitive functioning in mid- and late-life for specific cognitive abilities. Intelligence 68:70–81. https://doi.org/10.1016/j.intell.2017.12.004
Pedersen NL, Christensen K, Dahl AK, Finkel D, Franz CE, Gatz M, Reynolds CA (2013) IGEMS: the consortium on interplay of genes and environment across multiple studies. Twin Res Human Genet 16:481–489. https://doi.org/10.1017/thg.2012.110
Pedersen NL, Gatz M, Finch BK, Finkel D, Butler DA, Dahl Aslan A, Whitfield KE (2019) IGEMS: the consortium on interplay of genes and environment across multiple studies - an update. Twin Res Human Genet 22:809–816. https://doi.org/10.1017/thg.2019.76
Purcell S (2002) Variance components models for gene-environment interaction in twin analysis. Twin Res 5:554–571. https://doi.org/10.1375/136905202762342026
Sachdev PS, Lammel A, Trollor JN, Lee T, Wright MJ, Ames D, Team, O. R. (2009) A comprehensive neuropsychiatric study of elderly twins: the older australian twins study. Twin Res Hum Genet 12:573–582. https://doi.org/10.1375/twin.12.6.573
Shao Z, Janse E, Visser K, Meyer AS (2014) What do verbal fluency tasks measure? Predictors of verbal fluency performance in older adults. Front Psychol 5:772. https://doi.org/10.3389/fpsyg.2014.00772
Stern Y (2012) Cognitive reserve in ageing and Alzheimer’s disease. Lancet Neurol 11:1006–1012. https://doi.org/10.1016/S1474-4422(12)70191-6
Tucker-Drob EM, Briley DA, Harden KP (2013) Genetic and environmental influences on cognition across development and context. Curr Direct Psychol Sci 22:349–355. https://doi.org/10.1177/0963721413485087
Turkheimer E, Horn EE (2014) Interactions Between Socioeconomic Status and Components of Variation in Cognitive Ability Behavior Genetics of Cognition Across the Lifespan Springer pp. 41-68
UNESCO Institute for Statistics (2012) International standard classification of education: ISCED 2011: UNESCO Institute for Statistics Montreal.
van der Sluis S, Posthuma D, Dolan CV (2012) A note on false positives and power in G x E modelling of twin data. Behav Genet 42:170–186. https://doi.org/10.1007/s10519-011-9480-3
Weiss EM, Ragland JD, Brensinger CM, Bilker WB, Deisenhammer EA, Delazer M (2006) Sex differences in clustering and switching in verbal fluency tasks. J Int Neuropsychol Soc 12:502–509
Whiteside DM, Kealey T, Semla M, Luu H, Rice L, Basso MR, Roper B (2016) Verbal fluency: Language or executive function measure? Appl Neuropsychol: Adult 23:29–34. https://doi.org/10.1080/23279095.2015.1004574
Wilson RS, Beckett LA, Barnes LL, Schneider JA, Bach J, Evans DA, Bennett DA (2002) Individual differences in rates of change in cognitive abilities of older persons. Psychol Ag 17:179–193
Zavala C, Beam CR, Finch BK, Gatz M, Johnson W, Kremen WS, Reynolds CA (2018) Attained SES as a moderator of adult cognitive performance: testing gene-environment interaction in various cognitive domains. Dev Psychol 54:2356–2370. https://doi.org/10.1037/dev0000576
Funding
IGEMS is supported by the National Institutes of Health Grants No. R01 AG037985, R56 AG037985, R01 AG059329, R01 AG060470, RF1 AG058068. The Danish Twin Registry has been supported by grants from The National Program for Research Infrastructure 2007 from the Danish Agency for Science and Innovation, the Velux Foundation and the US National Institute of Health (P01 AG08761). VETSA was supported by National Institute of Health grants NIA R01 AG050595, R01 AG022381, and R01 AG022982. The Cooperative Studies Program of the Office of Research & Development of the United States Department of Veterans Affairs (VA) has provided financial support for the development and maintenance of the Vietnam Era Twin (VET) Registry. The MIDUS study was supported by the John D. and Catherine T. MacArthur Foundation Research Network on Successful Midlife Development and by National Institute on Aging Grant AG20166. We acknowledge the contribution of the OATS research team (https://cheba.unsw.edu.au/project/older-australian-twins-study) to this study. The OATS study has been funded by a National Health & Medical Research Council (NHMRC) and Australian Research Council (ARC) Strategic Award Grant of the Ageing Well, Ageing Productively Program (ID No. 401162) and NHMRC Project Grants (ID 1045325 and 1085606). OATS participant recruitment was facilitated through Twins Research Australia, a national resource in part supported by a Centre for Research Excellence Grant (ID: 1079102), from the National Health and Medical Research Council. We thank the participants for their time and generosity in contributing to this research. The content of this manuscript is solely the responsibility of the authors and does not necessarily represent the official views of the NIA/NIH, or the VA. The first author was also supported by NIH Grants R03 AG065643, R01 DC016977, and DP2 HD098859.
Author information
Authors and Affiliations
Consortia
Contributions
DG conceived the study, conducted the analyses, and drafted the manuscript with assistance from all other authors. All authors assisted in revising the manuscript and approved of the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
Daniel E. Gustavson, Matthew S. Panizzon, William S. Kremen, Chandra A. Reynolds, Shandell Pahlen, Marianne Nygaard, Mette Wod, Vibeke S. Catts, Teresa Lee, Margaret Gatz, and Carol E. Franz for the IGEMS Consortium report no conflict of interest.
Ethical Approval
All studies included within IGEMS received approval from relevant Institutional Review Boards at participating institutions. Analyses of de-identified data presented here was approved by Vanderbilt University Medical Center.
Consent to Participate
All subjects in participating studies completed informed consent.
Consent for Publication
No data from specific individuals are presented here.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Edited by Eric Turkheimer.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gustavson, D.E., Panizzon, M.S., Kremen, W.S. et al. Genetic and Environmental Influences on Semantic Verbal Fluency Across Midlife and Later Life. Behav Genet 51, 99–109 (2021). https://doi.org/10.1007/s10519-021-10048-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10519-021-10048-w