Abstract
Mounting evidence suggests that measures of phonemic fluency and semantic fluency are differentially associated with other cognitive and health phenotypes, but few studies have examined their shared and unique variance, especially using genetically-informative designs. In this study, 1464 middle-aged twins completed six fluency subtests at up to two time-points (mean age 56 and 62 years). Confirmatory factor analyses supported a two-factor solution: a General Fluency latent factor explained variation in all six subtests and a Semantic-Specific factor accounted for additional variance in semantic subtests. Both factors were explained primarily by genetic influences at both waves (a2 = 0.57–0.76). There was considerable stability of individual differences over 6 years (r = .90 for General Fluency, r = .81 for Semantic-Specific), especially for genetic influences (rg = .94 and 1.0, respectively). These results suggest that semantic fluency can be viewed as a combination of general and semantic-specific variance, but phonemic fluency is captured entirely by the general factor.
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Notes
The term “bifactor” does not actually refer to the number of factors in the model. Rather, it refers to the approach of fitting a common factor explaining variance in all the candidate indicators, and fitting specific factors as needed to capture additional variation (e.g., Semantic-Specific) not already captured by the common factor, even though in some cases there may be more than one additional factor.
References
Antila M, Tuulio-Henriksson A, Kieseppa T, Soronen P, Palo OM, Paunio T, Haukka J, Partonen T, Lonnqvist J (2007) Heritability of cognitive functions in families with bipolar disorder. Am J Med Genet B 144B:802–808. https://doi.org/10.1002/ajmg.b.30538
Baldo JV, Shimamura AP, Delis DC, Kramer J, Kaplan E (2001) Verbal and design fluency in patients with frontal lobe lesions. J Int Neuropsychol Soc 7:586–596
Boker S, Neale M, Maes H, Wilde M, Spiegel M, Brick T, Spies J, Estabrook R, Kenny S, Bates T, Mehta P (2011) OpenMx: an open source extended structural equation modeling framework. Psychometrika 76:306–317. https://doi.org/10.1007/s11336-010-9200-6
Bratko D (1996) Twin study of verbal and spatial abilities. Personality Individ Differ 21:621–624. https://doi.org/10.1016/0191-8869(96)00091-8
Delis DC, Kaplan E, Kramer JH (2001) Delis-Kaplan executive function system (D-KEFS). Psychological Corporation, San Antonio
Delis DC, Jacobson M, Bondi MW, Hamilton JM, Salmon DP (2003) The myth of testing construct validity using factor analysis or correlations with normal or mixed clinical populations: lessons from memory assessment. J Int Neuropsychol Soc 9:936–946. https://doi.org/10.1017/S1355617703960139
Elman JA, Jak AJ, Panizzon MS, Tu X, Chen T, Reynolds CA et al (2018) Under-diagnosis of MCI in longitudinal studies: the problem of not accounting for practice effects. Alzheimer’s Dement. https://doi.org/10.1016/j.dadm.2018.04.003
Fine EM, Delis DC, Paul BM, Filoteo JV (2011) Reduced verbal fluency for proper names in nondemented patients with Parkinson’s disease: a quantitative and qualitative analysis. J Clin Exp Neuropsychol 33:226–233. https://doi.org/10.1080/13803395.2010.507185
Friedman NP, Miyake A, Young SE, Defries JC, Corley RP, Hewitt JK (2008) Individual differences in executive functions are almost entirely genetic in origin. J Exp Psychol 137:201–225. https://doi.org/10.1037/0096-3445.137.2.201
Giubilei F, Medda E, Fagnani C, Bianchi V, De Carolis A, Salvetti M, Sepe-Monti M, Stazi MA (2008) Heritability of neurocognitive functioning in the elderly: evidence from an Italian twin study. Age Ageing 37:640–646. https://doi.org/10.1093/ageing/afn132
Gustavson DE, Panizzon MS, Franz CE, Friedman NP, Reynolds CA, Jacobson KC, Xian H, Lyons MJ, Kremen WS (2018a) Genetic and environmental architecture of executive functions in midlife. Neuropsychology 32:18–30. https://doi.org/10.1037/neu0000389
Gustavson DE, Panizzon MS, Elman JA, Franz CE, Reynolds CA, Jacobson KC, Friedman NP, Xian H, Toomey R, Lyons MJ, Kremen WS (2018b) Stability of genetic and environmental influences on executive functions in midlife. Psychol Aging 33:219–231. https://doi.org/10.1037/pag0000230
Harris SE, Deary IJ (2011) The genetics of cognitive ability and cognitive ageing in healthy older people. Trends Cogn Sci 15:388–394. https://doi.org/10.1016/j.tics.2011.07.004
Hedden T, Yoon C (2006) Individual differences in executive processing predict susceptibility to interference in verbal working memory. Neuropsychology 20:511–528. https://doi.org/10.1037/0894-4105.20.5.511
Henry JD, Crawford JR (2004a) 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 (2004b) 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 (2005a) 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 (2005b) A meta-analytic review of verbal fluency deficits in schizophrenia relative to other neurocognitive deficits. Cogn Neuropsychiatry 10:1–33. https://doi.org/10.1080/13546800344000309
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
Hollingshead AB (1975) Four factor index of social status. Yale University, New Haven
Hu LT, Bentler PM (1998) Fit indices in covariance structure modeling: sensitivity to underparameterized model misspecification. Psychol Methods 3:424–453. https://doi.org/10.1037//1082-989x.3.4.424
Kremen WS, Thompson-Brenner H, Leung YM, Grant MD, Franz CE, Eisen SA, Jacobson KC, Boake C, Lyons MJ (2006) Genes, environment, and time: the Vietnam era twin study of aging (VETSA). Twin Res Human Genet 9:1009–1022. https://doi.org/10.1375/183242706779462750
Kremen WS, Jacobson KC, Panizzon MS, Xian H, Eaves LJ, Eisen SA, Tsuang MT, Lyons MJ (2009) Factor structure of planning and problem-solving: a behavioral genetic analysis of the Tower of London task in middle-aged twins. Behav Genet 39:133–144. https://doi.org/10.1007/s10519-008-9242-z
Kremen WS, Panizzon MS, Xian H, Barch DM, Franz CE, Grant MD, Toomey R, Lyons MJ (2011) Genetic architecture of context processing in late middle age: more than one underlying mechanism. Psychol Aging 26:852–863. https://doi.org/10.1037/a0025098
Kremen WS, Moore CS, Franz CE, Panizzon MS, Lyons MJ (2014) Cognition in middle adulthood. In: Finkel D, Reynolds CA (eds) Behavior genetics of cognition across the lifespan. Springer, New York, pp 105–134
Kremen WS, Panizzon MS, Cannon TD (2016) Genetics and neuropsychology: a merger whose time has come. Neuropsychology 30:1–5. https://doi.org/10.1037/neu0000254
Lee T, Mosing MA, Henry JD, Trollor JN, Ames D, Martin NG, Wright MJ, Sachdev PS, OATS Research Team (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, Sachdev PS, OATS Research Team (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
Lyons MJ, York TP, Franz CE, Grant MD, Eaves LJ, Jacobson KC, Schaie KW, Panizzon MS, Boake C, Xian H, Toomey R (2009) Genes determine stability and the environment determines change in cognitive ability during 35 years of adulthood. Psychol Sci 20:1146–1152. https://doi.org/10.1111/j.1467-9280.2009.02425.x
Lyons MJ, Panizzon MS, Liu W, McKenzie R, Bluestone NJ, Grant MD, Franz CE, Vuoksimaa EP, Toomey R, Jacobson KC, Reynolds CA (2017) A longitudinal twin study of general cognitive ability over four decades. Dev Psychol 53:1170–1177. https://doi.org/10.1037/dev0000303
Markon KE, Krueger RF (2004) An empirical comparison of information-theoretic selection criteria for multivariate behavior genetic models. Behav Genetics 34:593–610. https://doi.org/10.1007/s10519-004-5587-0
Martin NG, Eaves LJ, Kearsey MJ, Davies P (1978) The power of the classical twin study. Heredity 40:97–116. https://doi.org/10.1038/hdy.1978.10
McGue M, Christensen K (2001) The heritability of cognitive functioning in very old adults: evidence from Danish twins aged 75 years and older. Psychol Aging 16:272–280. https://doi.org/10.1037//0882-7974.16.2.272
Miyake A, Friedman NP (2012) The nature and organization of individual differences in executive functions: four general conclusions. Curr Dir Psychol Sci 21:8–14. https://doi.org/10.1177/0963721411429458
Moscovitch M (1994) Cognitive resources and dual-task interference effects at retrieval in normal people: the role of the frontal lobes and medial temporal cortex. Neuropsychology 8:524–534. https://doi.org/10.1037/0894-4105.8.4.524
Panizzon MS, Vuoksimaa E, Spoon KM, Jacobson KC, Lyons MJ, Franz CE, Xian H, Vasilopoulos T, Kremen WS (2014) Genetic and environmental influences on general cognitive ability: is g a valid latent construct? Intelligence 43:65–76. https://doi.org/10.1016/j.intell.2014.01.008
Panizzon MS, Neale MC, Docherty AR, Franz CE, Jacobson KC, Toomey R, Xian H, Vasilopoulos T, Rana BK, McKenzie R, Lyons MJ (2015) Genetic and environmental architecture of changes in episodic memory from middle to late middle age. Psychol Aging 30:286–300. https://doi.org/10.1037/pag0000023
Radloff LS (1977) The CES-D scale: a self-report depression scale for research in the general population. Appl Psychol Meas 1:385–401
Rönnlund M, Nilsson LG (2006) Adult life-span patterns in WAIS-R Block Design performance: cross-sectional versus longitudinal age gradients and relations to demographic factors. Intelligence 34:63–78. https://doi.org/10.1016/j.intell.2005.06.004
Rönnlund M, Nyberg L, Bäckman L, Nilsson LG (2005) Stability, growth, and decline in adult life span development of declarative memory: cross-sectional and longitudinal data from a population-based study. Psychol Aging 20:3–18. https://doi.org/10.1037/0882-7974.20.1.3
Schoenborn CA, Heyman KM (2009) Health characteristics of adults aged 55 years and over: United States, 2004–2007. Natl Health Stat Rep 16:1–31
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
Stolwyk R, Bannirchelvam B, Kraan C, Simpson K (2015) The cognitive abilities associated with verbal fluency task performance differ across fluency variants and age groups in healthy young and old adults. J Clin Exp Neuropsychol 37:70–83. https://doi.org/10.1080/13803395.2014.988125
Swan GE, Carmelli D (2002) Evidence for genetic mediation of executive control: a study of aging male twins. J Gerontol B 57:P133-143
Troyer AK, Moscovitch M (2006) Cognitive processes of verbal fluency tasks. In: Poreh AM (ed) The quantified process approach to neuropsychological assessment. Taylor & Francis, New York, pp 143–160
Tsuang MT, Bar JL, Harley RM, Lyons MJ (2001) The Harvard twin study of substance abuse: what we have learned. Harv Rev Psychiatry 9:267–279. https://doi.org/10.1093/hrp/9.6.267
Unsworth N, Spillers GJ, Brewer GA (2011) Variation in verbal fluency: a latent variable analysis of clustering, switching, and overall performance. Q J Exp Psychol 64:447–466. https://doi.org/10.1080/17470218.2010.505292
van den Berg E, Jiskoot LC, Grosveld MJH, van Swieten JC, Papma JM (2017) Qualitative assessment of verbal fluency performance in frontotemporal dementia. Dement Geriatr Cogn Disord 44:35–44. https://doi.org/10.1159/000477538
Vasilopoulos T, Franz CE, Panizzon MS, Xian H, Grant MD, Lyons MJ, Toomey R, Jacobson KC, Kremen WS (2012) Genetic architecture of the delis-kaplan executive function system trail making test: evidence for distinct genetic influences on executive function. Neuropsychology 26:238–250. https://doi.org/10.1037/a0026768
Whiteside DM, Kealey T, Semla M, Luu H, Rice L, Basso MR, Roper B (2016) Verbal fluency: language or executive function measure? Appl Neuropsychol 23:29–34. https://doi.org/10.1080/23279095.2015.1004574
Acknowledgements
This research was supported by Grants AG050595, AG018386, AG018384, AG022381, and AG047903 from the National Institutes of Health. The content of this manuscript is the responsibility of the authors and does not represent official views of NIA/NIH, or the Veterans’ Administration. Numerous organizations provided invaluable assistance in the conduct of the VET Registry, including: U.S. Department of Veterans Affairs, Department of Defense; National Personnel Records Center, National Archives and Records Administration; Internal Revenue Service; National Opinion Research Center; National Research Council, National Academy of Sciences; the Institute for Survey Research, Temple University. The authors gratefully acknowledge the continued cooperation of the twins and the efforts of many staff members.
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This research was supported by Grants AG050595, AG018386, AG018384, AG022381, and AG047903 from the National Institutes of Health.
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Daniel E. Gustavson, Matthew S. Panizzon, Jeremy A. Elman, Carol E. Franz, Asad Beck, Chandra A. Reynolds, Kristen C. Jacobson, Hong Xian, Rosemary Toomey, Michael J. Lyons, and William S. Kremen declare that they have no conflicts of interest.
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Gustavson, D.E., Panizzon, M.S., Elman, J.A. et al. Genetic and Environmental Influences on Verbal Fluency in Middle Age: A Longitudinal Twin Study. Behav Genet 48, 361–373 (2018). https://doi.org/10.1007/s10519-018-9910-6
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DOI: https://doi.org/10.1007/s10519-018-9910-6