Verbal and visuospatial executive functions in healthy elderly: The impact of education and frequency of reading and writing

Branco, Laura Damiani; Cotrena, Charles; Pereira, Natalie; Kochhann, Renata; Fonseca, Rochele Paz

doi:10.1590/S1980-57642014DN82000011

ABSTRACT

Objective:

To assess the predictive role of education and frequency of reading and writing habits (FRWH) on the cognitive flexibility, inhibition and planning abilities of healthy elderly individuals.

Methods:

Fifty-seven healthy adults aged between 60 and 75 years with 2 to 23 years of formal education were assessed as to the frequency with which they read and wrote different types of text, as well as their number of years of formal education. Executive functions were evaluated using the Hayling Test and the Modified Wisconsin Card Sorting Test (MWCST).

Results:

Weak to moderate positive correlations were found between education, FRWH and the number of categories completed in the MWCST, while negative correlations were identified between these variables and the number of perseverative and non-perseverative errors on the task. Only the FRWH was significantly correlated with the number of failures to maintain set. Speed and accuracy on the Hayling Test were only correlated with participant education. Both education and FRWH significantly predicted performance on the MWCST, and the combination of these two variables had a greater predictive impact on performance on this task than either of the two variables alone. Variability in scores on the Hayling Test was best accounted for by participant education.

Conclusion:

In this sample of elderly subjects, cognitive flexibility was sufficiently preserved to allow for adequate performance on verbal tasks, but may have benefitted from the additional stimulation provided by regular reading and writing habits and by formal education in the performance of more complex non-verbal tasks.

Key words
aging; education; reading; writing; executive function

RESUMO

Objetivo:

Avaliar o papel preditivo da educação e da frequência de hábitos de leitura e de escrita (FHLE) na flexibilidade cognitiva e planejamento de idosos saudáveis.

Métodos:

Cinquenta e sete adultos saudáveis com idade entre 60 e 75 anos e de 2 a 23 anos de escolaridade foram avaliados quanto à frequência com que liam e escreviam diferentes tipos de texto, assim como seu número de anos de educação formal. Ainda, suas funções executivas foram examinadas pelos Testes Hayling e Wisconsin de Classificação de Cartas Modificado (MWCST).

Resultados:

Correlações positivas de fracas a moderadas foram encontradas entre a educação, a FHLE e o número de categorias completadas no MWCST. Ainda, estas variáveis correlacionaram-se negativamente com o número de erros perseverativos e não perseverativos na tarefa. Somente a FRWH correlacionou-se com o número de rupturas no MWCST. O tempo e acurácia no Teste Hayling correlacionaram-se apenas com a educação de participantes. Tanto a educação quanto a FHLE foram preditores significativos do desempenho no MWCST, e a combinação destas duas variáveis teve maior impacto no desempenho da tarefa do que qualquer uma delas isoladamente. A variabilidade no desempenho no teste Hayling foi melhor explicada pela educação dos idosos.

Conclusão:

Nesta amostra de indivíduos idosos, a flexibilidade cognitiva esteve suficientemente preservada para permitir um desempenho adequado em tarefas verbais. No entanto, pode ter se beneficiado do estímulo adicional fornecido por hábitos de leitura e escrita regulares e por maior quantidade de anos de estudo formal em demandas não-verbais mais complexas.

Palavras-chave
envelhecimento; educação; leitura; redação; função executiva

Texto completo disponível apenas em PDF.

Full text available only in PDF format.

REFERENCES

¹
Ardila R. The nature of psychology: the great dilemmas. Am Psychol 2007;62:904-912.
²
Sánchez JL, Torrellas C, Martín J, Barrera I. Study of sociodemographic variables linked to lifestyle and their possible influence on cognitive reserve. J Clin Exp Neuropsychol. 2011;33:874-891.
³
Ska B, Joanette Y. Normal aging and cognition. Med Sci (Paris). 2006;22:284-287
⁴
Wasylyshyn C, Verhaeghen P, Sliwinski MJ. Aging and task switching: a meta-analysis. Psychol Aging. 2011;26:15-20.
⁵
Wong CEI, Cotrena C, Cardoso C, Fonseca RP. Memoria visual: relación con factores sociodemográficos. Rev Mex Neuropsicol 2010;5:10-18.
⁶
Peña-Casanova J, Gramunt-Fombuena N, Quiñones-Úbeda S, et al. Spanish Multicenter Normative Studies (NEURONORMA Project): norms for the Rey-Osterrieth complex figure (copy and memory), and free and cued selective reminding test. Arch Clin Neuropsychol 2009;24:371-393.
⁷
Jang SN, Choi YJ, Kim DH. Association of socioeconomic status with successful ageing: differences in the components of successful ageing. J Biosoc Sci 2009;41:207-219.
⁸
Varnava A, Halligan PW. Influence of age and sex on line bisection: A study of normal performance with implications for visuospatial neglect. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn 2007;14:571-585.
⁹
Jefferson AL, Gibbons LE, Rentz DM, et al. A life course model of cognitive activities, socioeconomic status, education, reading ability, and cognition. J Am Geriatr Soc 2011;59:1403-1411.
¹⁰
Pawlowski J, Remor E, Parente MAMP, de Salles JF, Fonseca RP, Bandeira DR. The influence of reading and writing habits associated with education on the neuropsychological performance of Brazilian adults. Read Writ 2012;25:2275-2289.
¹¹
Parente MAMP, Scherer LC, Zimmermann N, Fonseca RP. Evidências do papel da escolaridade na organização cerebral. Neuropsicol Latinoam 2009;1:72-80.
¹²
Ardila A, Rosselli M. Illiterates and cognition: The impact of education. In: Uzzell BP, Ponton MO, Ardila A, editors. International handbook of cross-cultural neuropsychology. New Jersey: Lawrence Erlbaum Associates, Inc.; 2007:181-98.
¹³
Ardila A, Ostrosky-Solis F, Rosselli M, Gómez C. Age-related cognitive decline during normal aging: the complex effect of education. Arch Clin Neuropsychol 2000;15:495-513.
¹⁴
Byrd DA, Jacobs DM, Hilton HJ, Stern Y, Manly JJ. Sources of errors on visuoperceptual tasks: Role of education, literacy, and search strategy. Brain Cogn 2005;58:251-7.
¹⁵
Seo EH, Lee DY, Choo IH, et al. Performance on the Benton Visual Retention Test in an educationally diverse elderly population. J Gerontol Ser B Psychol Sci Soc Sci 2007;62:191-193.
¹⁶
Valenzuela MJ, Sachdev P. Brain reserve and dementia: a systematic review. Psychol Med 2006;36:441-454.
¹⁷
Cabeza R. Hemispheric asymmetry reduction in older adults: the {HAROLD} model. Psychol Aging 2002;17:85.
¹⁸
Stern Y. Cognitive Reserve. Neuropsychologia 2009;47:2015-2028.
¹⁹
Lezak MD, Howieson DB, Bigler ED, Tranel D. Neuropsychological Assessment. 5th ed. New York: Oxford University Press; 2012.
²⁰
Gee GC, Walsemann KM, Takeuchi DT. English proficiency and language preference: testing the equivalence of two measures. Am J Public Health 2010;100:563.
²¹
Dotson VM, Kitner-Triolo MH, Evans MK, Zonderman AB. Effects of race and socioeconomic status on the relative influence of education and literacy on cognitive functioning. J Int Neuropsychol Soc 2009; 15:580-589.
²²
Chan RC, Shum D, Toulopoulou T, Chen EY. Assessment of executive functions: Review of instruments and identification of critical issues. Arch Clin Neuropsychol 2008;23:201-216.
²³
Matsuoka K, Kotani I, Yamasato M. Correct information unit analysis for determining the characteristics of narrative discourse in individuals with chronic traumatic brain injury. Brain Inj 2012;26:1723-1730.
²⁴
Coelho CA, Grela B, Corso M, Gamble A, Feinn R. Microlinguistic deficits in the narrative discourse of adults with traumatic brain injury. Brain Inj 2005;19:1139-1145.
²⁵
Head D, Kennedy KM, Rodrigue KM, Raz N. Age differences in perseveration: Cognitive and neuroanatomical mediators of performance on the Wisconsin Card Sorting Test. Neuropsychologia 2009;47:1200-1203.
²⁶
Bielak AA, Mansueti L, Strauss E, Dixon RA. Performance on the Hayling and Brixton tests in older adults: norms and correlates. Arch Clin Neuropsychol 2006;21:141-149.
²⁷
Burgess PW, Shallice T. The Hayling and Brixton Tests: Thames Valley Test Company Bury St. Edmonds, England. 1997.
²⁸
Nelson HE. A modified card sorting test sensitive to frontal lobe defects. Cortex 1976;12:313-324.
²⁹
Ashendorf L, McCaffrey RJ. Exploring age-related decline on the Wisconsin Card Sorting Test. Clin Neuropsychol 2008;22:262-272.
³⁰
Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD. The Unity and Diversity of Executive Functions and Their Contributions to Complex "' Frontal Lobe '" Tasks: A Latent Variable Analysis. Cogn Psychol 2000;41:49-100.
³¹
Marton K. Visuo-spatial processing and executive functions in children with specific language impairment. Int J Lang Commun Disord 2008;43:181-200.
³²
Borella E, Ghisletta P, De Ribaupierre A. Age differences in text processing: The role of working memory, inhibition, and processing speed. J Gerontol Ser B Psychol Sci Soc Sci 2011;66:311-320.
³³
Persad CC, Abeles N, Zacks RT, Denburg NL. Inhibitory changes after age 60 and their relationship to measures of attention and memory. J Gerontol Ser B Psychol Sci Soc Sci 2002;57:P223-P232.
³⁴
Anderson MC, Reinholz J, Kuhl BA, Mayr U. Intentional suppression of unwanted memories grows more difficult as we age. Psychol Aging 2011;26:397-405.
³⁵
Friedman NP, Miyake A, Corley RP, Young SE, Defries JC, Hewitt JK. Not all executive functions are related to intelligence. Psychol Sci 2006;17:172-179.
³⁶
Tombaugh TN. Trail Making Test A and B: normative data stratified by age and education. Arch Clin Neuropsychol 2004;19:203-214.
³⁷
Drag LL, Bieliauskas LA. Contemporary review 2009: cognitive aging. J Geriatr Psychiatry Neurol 2010;23:75-93.
³⁸
Steffener J, Barulli D, Habeck C, O'Shea D, Razlighi Q, Stern Y. The Role of Education and Verbal Abilities in Altering the Effect of Age-Related Gray Matter Differences on Cognition. PLoS One 2014;9:e91196.
³⁹
Soto-Añari M, Flores-Valdivia G, Fernández-Guinea S. Nivel de lectura como medida de reserva cognitiva en adultos mayores. Rev Neurol 2013;56:79-85.
⁴⁰
Chaves MLF, Izquierdo I. Differential diagnosis between dementia and depression: a study of efficiency increment. Acta Neurol Scand 1992; 85:378-82.
⁴¹
Kochhann R, Varela JS, Lisboa CSM, Chaves MLF. The Mini Mental State Examination Review of cutoff points adjusted for schooling in a large Southern Brazilian sample. Dement Neuropsychol 2010;4:35-41.
⁴²
Associação Brasileira de Empresas de Pesquisa (ABEP). Critério de classificação econômica Brasil/2008 [Internet]. 2008. Available from: http://www.abep.org/codigosguias/criterio_brasil_2008.pdf
» http://www.abep.org/codigosguias/criterio_brasil_2008.pdf
⁴³
Fonseca RP, Zimmermann N, Pawlowski J, Oliveira CR, Gindri G, Scherer LC, et al. Métodos em avaliação neuropsicológica: pressupostos gerais, neurocognitivos, neuropsicolingüísticos e psicométricos no uso e desenvolvimento de instrumentos. In: Landeira-Fernandez J, Fukusima SS, editors. Métodos de pesquisa em neurociência clínica e experimental. São Paulo: Manole; 2012. p. 266-96.
⁴⁴
Amaral RA, Malbergier A. Effectiveness of the {CAGE} questionnaire, gamma-glutamyltransferase and mean corpuscular volume of red blood cells as markers for alcohol-related problems in the workplace. Addict Behav 2008;33:772-781.
⁴⁵
Fonseca RP, Oliveira C, Gindri G, Zimmermann N, Reppold C, Parente M. Teste Hayling: um instrumento de avaliação de componentes das funções executivas. Avaliação psicológica e neuropsicológica de crianças e adolescentes 2010:337-364.
⁴⁶
Burke DM, MacKay DG, James LE. Theoretical approaches to language and aging. In: Perfect T, Maylor E, editors. Models of cognitive aging. Oxford: Oxford University Press; 2000:204-237.
⁴⁷
Abrams L, Farrel MT. Language processing in normal aging. In: Guendouzi J, Loncke F, Williams MJ, editors. The Handbook of Psycholinguistic and Cognitive Processes: Perspectives in Communication disorders. New York: Psychology Press; 2011:603-624.
⁴⁸
Fleming VB. Early Detection of Cognitive-Linguistic Change Associated With Mild Cognitive Impairment. Communication Disorders Quarterly 2014;35:146-157.
⁴⁹
Boone KB, Ghaffarian S, Lesser IM, Hill-Gutierrez E, G Berman N. Wisconsin Card Sorting Test performance in healthy, older adults: Relationship to age, sex, education, and {IQ}. J Clin Psychol 1993;49:54-60.

Publication Dates

Publication in this collection
Apr-Jun 2014

History

Received
05 Jan 2014
Accepted
16 Mar 2014

This is an open-access article distributed under the terms of the Creative Commons Attribution License

[1] ¹
Ardila R. The nature of psychology: the great dilemmas. Am Psychol 2007;62:904-912.

[2] ²
Sánchez JL, Torrellas C, Martín J, Barrera I. Study of sociodemographic variables linked to lifestyle and their possible influence on cognitive reserve. J Clin Exp Neuropsychol. 2011;33:874-891.

[3] ³
Ska B, Joanette Y. Normal aging and cognition. Med Sci (Paris). 2006;22:284-287

[4] ⁴
Wasylyshyn C, Verhaeghen P, Sliwinski MJ. Aging and task switching: a meta-analysis. Psychol Aging. 2011;26:15-20.

[5] ⁵
Wong CEI, Cotrena C, Cardoso C, Fonseca RP. Memoria visual: relación con factores sociodemográficos. Rev Mex Neuropsicol 2010;5:10-18.

[6] ⁶
Peña-Casanova J, Gramunt-Fombuena N, Quiñones-Úbeda S, et al. Spanish Multicenter Normative Studies (NEURONORMA Project): norms for the Rey-Osterrieth complex figure (copy and memory), and free and cued selective reminding test. Arch Clin Neuropsychol 2009;24:371-393.

[7] ⁷
Jang SN, Choi YJ, Kim DH. Association of socioeconomic status with successful ageing: differences in the components of successful ageing. J Biosoc Sci 2009;41:207-219.

[8] ⁸
Varnava A, Halligan PW. Influence of age and sex on line bisection: A study of normal performance with implications for visuospatial neglect. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn 2007;14:571-585.

[9] ⁹
Jefferson AL, Gibbons LE, Rentz DM, et al. A life course model of cognitive activities, socioeconomic status, education, reading ability, and cognition. J Am Geriatr Soc 2011;59:1403-1411.

[10] ¹⁰
Pawlowski J, Remor E, Parente MAMP, de Salles JF, Fonseca RP, Bandeira DR. The influence of reading and writing habits associated with education on the neuropsychological performance of Brazilian adults. Read Writ 2012;25:2275-2289.

[11] ¹¹
Parente MAMP, Scherer LC, Zimmermann N, Fonseca RP. Evidências do papel da escolaridade na organização cerebral. Neuropsicol Latinoam 2009;1:72-80.

[12] ¹²
Ardila A, Rosselli M. Illiterates and cognition: The impact of education. In: Uzzell BP, Ponton MO, Ardila A, editors. International handbook of cross-cultural neuropsychology. New Jersey: Lawrence Erlbaum Associates, Inc.; 2007:181-98.

[13] ¹³
Ardila A, Ostrosky-Solis F, Rosselli M, Gómez C. Age-related cognitive decline during normal aging: the complex effect of education. Arch Clin Neuropsychol 2000;15:495-513.

[14] ¹⁴
Byrd DA, Jacobs DM, Hilton HJ, Stern Y, Manly JJ. Sources of errors on visuoperceptual tasks: Role of education, literacy, and search strategy. Brain Cogn 2005;58:251-7.

[15] ¹⁵
Seo EH, Lee DY, Choo IH, et al. Performance on the Benton Visual Retention Test in an educationally diverse elderly population. J Gerontol Ser B Psychol Sci Soc Sci 2007;62:191-193.

[16] ¹⁶
Valenzuela MJ, Sachdev P. Brain reserve and dementia: a systematic review. Psychol Med 2006;36:441-454.

[17] ¹⁷
Cabeza R. Hemispheric asymmetry reduction in older adults: the {HAROLD} model. Psychol Aging 2002;17:85.

[18] ¹⁸
Stern Y. Cognitive Reserve. Neuropsychologia 2009;47:2015-2028.

[19] ¹⁹
Lezak MD, Howieson DB, Bigler ED, Tranel D. Neuropsychological Assessment. 5th ed. New York: Oxford University Press; 2012.

[20] ²⁰
Gee GC, Walsemann KM, Takeuchi DT. English proficiency and language preference: testing the equivalence of two measures. Am J Public Health 2010;100:563.

[21] ²¹
Dotson VM, Kitner-Triolo MH, Evans MK, Zonderman AB. Effects of race and socioeconomic status on the relative influence of education and literacy on cognitive functioning. J Int Neuropsychol Soc 2009; 15:580-589.

[22] ²²
Chan RC, Shum D, Toulopoulou T, Chen EY. Assessment of executive functions: Review of instruments and identification of critical issues. Arch Clin Neuropsychol 2008;23:201-216.

[23] ²³
Matsuoka K, Kotani I, Yamasato M. Correct information unit analysis for determining the characteristics of narrative discourse in individuals with chronic traumatic brain injury. Brain Inj 2012;26:1723-1730.

[24] ²⁴
Coelho CA, Grela B, Corso M, Gamble A, Feinn R. Microlinguistic deficits in the narrative discourse of adults with traumatic brain injury. Brain Inj 2005;19:1139-1145.

[25] ²⁵
Head D, Kennedy KM, Rodrigue KM, Raz N. Age differences in perseveration: Cognitive and neuroanatomical mediators of performance on the Wisconsin Card Sorting Test. Neuropsychologia 2009;47:1200-1203.

[26] ²⁶
Bielak AA, Mansueti L, Strauss E, Dixon RA. Performance on the Hayling and Brixton tests in older adults: norms and correlates. Arch Clin Neuropsychol 2006;21:141-149.

[27] ²⁷
Burgess PW, Shallice T. The Hayling and Brixton Tests: Thames Valley Test Company Bury St. Edmonds, England. 1997.

[28] ²⁸
Nelson HE. A modified card sorting test sensitive to frontal lobe defects. Cortex 1976;12:313-324.

[29] ²⁹
Ashendorf L, McCaffrey RJ. Exploring age-related decline on the Wisconsin Card Sorting Test. Clin Neuropsychol 2008;22:262-272.

[30] ³⁰
Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD. The Unity and Diversity of Executive Functions and Their Contributions to Complex "' Frontal Lobe '" Tasks: A Latent Variable Analysis. Cogn Psychol 2000;41:49-100.

[31] ³¹
Marton K. Visuo-spatial processing and executive functions in children with specific language impairment. Int J Lang Commun Disord 2008;43:181-200.

[32] ³²
Borella E, Ghisletta P, De Ribaupierre A. Age differences in text processing: The role of working memory, inhibition, and processing speed. J Gerontol Ser B Psychol Sci Soc Sci 2011;66:311-320.

[33] ³³
Persad CC, Abeles N, Zacks RT, Denburg NL. Inhibitory changes after age 60 and their relationship to measures of attention and memory. J Gerontol Ser B Psychol Sci Soc Sci 2002;57:P223-P232.

[34] ³⁴
Anderson MC, Reinholz J, Kuhl BA, Mayr U. Intentional suppression of unwanted memories grows more difficult as we age. Psychol Aging 2011;26:397-405.

[35] ³⁵
Friedman NP, Miyake A, Corley RP, Young SE, Defries JC, Hewitt JK. Not all executive functions are related to intelligence. Psychol Sci 2006;17:172-179.

[36] ³⁶
Tombaugh TN. Trail Making Test A and B: normative data stratified by age and education. Arch Clin Neuropsychol 2004;19:203-214.

[37] ³⁷
Drag LL, Bieliauskas LA. Contemporary review 2009: cognitive aging. J Geriatr Psychiatry Neurol 2010;23:75-93.

[38] ³⁸
Steffener J, Barulli D, Habeck C, O'Shea D, Razlighi Q, Stern Y. The Role of Education and Verbal Abilities in Altering the Effect of Age-Related Gray Matter Differences on Cognition. PLoS One 2014;9:e91196.

[39] ³⁹
Soto-Añari M, Flores-Valdivia G, Fernández-Guinea S. Nivel de lectura como medida de reserva cognitiva en adultos mayores. Rev Neurol 2013;56:79-85.

[40] ⁴⁰
Chaves MLF, Izquierdo I. Differential diagnosis between dementia and depression: a study of efficiency increment. Acta Neurol Scand 1992; 85:378-82.

[41] ⁴¹
Kochhann R, Varela JS, Lisboa CSM, Chaves MLF. The Mini Mental State Examination Review of cutoff points adjusted for schooling in a large Southern Brazilian sample. Dement Neuropsychol 2010;4:35-41.

[42] ⁴²
Associação Brasileira de Empresas de Pesquisa (ABEP). Critério de classificação econômica Brasil/2008 [Internet]. 2008. Available from: http://www.abep.org/codigosguias/criterio_brasil_2008.pdf
» http://www.abep.org/codigosguias/criterio_brasil_2008.pdf

[43] ⁴³
Fonseca RP, Zimmermann N, Pawlowski J, Oliveira CR, Gindri G, Scherer LC, et al. Métodos em avaliação neuropsicológica: pressupostos gerais, neurocognitivos, neuropsicolingüísticos e psicométricos no uso e desenvolvimento de instrumentos. In: Landeira-Fernandez J, Fukusima SS, editors. Métodos de pesquisa em neurociência clínica e experimental. São Paulo: Manole; 2012. p. 266-96.

[44] ⁴⁴
Amaral RA, Malbergier A. Effectiveness of the {CAGE} questionnaire, gamma-glutamyltransferase and mean corpuscular volume of red blood cells as markers for alcohol-related problems in the workplace. Addict Behav 2008;33:772-781.

[45] ⁴⁵
Fonseca RP, Oliveira C, Gindri G, Zimmermann N, Reppold C, Parente M. Teste Hayling: um instrumento de avaliação de componentes das funções executivas. Avaliação psicológica e neuropsicológica de crianças e adolescentes 2010:337-364.

[46] ⁴⁶
Burke DM, MacKay DG, James LE. Theoretical approaches to language and aging. In: Perfect T, Maylor E, editors. Models of cognitive aging. Oxford: Oxford University Press; 2000:204-237.

[47] ⁴⁷
Abrams L, Farrel MT. Language processing in normal aging. In: Guendouzi J, Loncke F, Williams MJ, editors. The Handbook of Psycholinguistic and Cognitive Processes: Perspectives in Communication disorders. New York: Psychology Press; 2011:603-624.

[48] ⁴⁸
Fleming VB. Early Detection of Cognitive-Linguistic Change Associated With Mild Cognitive Impairment. Communication Disorders Quarterly 2014;35:146-157.

[49] ⁴⁹
Boone KB, Ghaffarian S, Lesser IM, Hill-Gutierrez E, G Berman N. Wisconsin Card Sorting Test performance in healthy, older adults: Relationship to age, sex, education, and {IQ}. J Clin Psychol 1993;49:54-60.

Brasil