Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-25T07:07:56.391Z Has data issue: false hasContentIssue false

Design and Verbal Fluency in Alzheimer’s Disease and Frontotemporal Dementia: Clinical and Metabolic Correlates

Published online by Cambridge University Press:  27 September 2021

Alfonso Delgado-Álvarez
Affiliation:
Department of Neurology, Hospital Clinico San Carlos, San Carlos Institute for Health Research (IdiSSC), Universidad Complutense, Madrid, Spain
María Nieves Cabrera-Martín
Affiliation:
Department of Nuclear Medicine, Hospital Clinico San Carlos, San Carlos Institute for Health Research (IdiSSC), Universidad Complutense, Madrid, Spain
Vanesa Pytel
Affiliation:
Department of Neurology, Hospital Clinico San Carlos, San Carlos Institute for Health Research (IdiSSC), Universidad Complutense, Madrid, Spain
Cristina Delgado-Alonso
Affiliation:
Department of Neurology, Hospital Clinico San Carlos, San Carlos Institute for Health Research (IdiSSC), Universidad Complutense, Madrid, Spain
Jorge Matías-Guiu
Affiliation:
Department of Neurology, Hospital Clinico San Carlos, San Carlos Institute for Health Research (IdiSSC), Universidad Complutense, Madrid, Spain
Jordi A. Matias-Guiu*
Affiliation:
Department of Neurology, Hospital Clinico San Carlos, San Carlos Institute for Health Research (IdiSSC), Universidad Complutense, Madrid, Spain
*
Correspondence and reprint requests to: Jordi A. Matias-Guiu, Department of Neurology, Hospital Clinico San Carlos, Profesor Martin Lagos St., ES-28040, Spain. Emails: [email protected]; [email protected]

Abstract

Objective:

Cognitive processes underlying verbal and design fluency, and their neural correlates in patients with Alzheimer’s disease (AD) and behavioural variant Frontotemporal Dementia (bvFTD) remain unclear. We hypothesised that verbal and design fluency may be associated with distinct neuropsychological processes in AD and FTD, showing different patterns of impairment and neural basis.

Methods:

We enrolled 142 participants including patients with AD (n = 80, mean age = 74.71), bvFTD (n = 34, mean age = 68.18), and healthy controls (HCs) (n = 28, mean age = 71.14), that underwent cognitive assessment and 18F-fluorodeoxyglucose positron emission tomography imaging.

Results:

Semantic and phonemic fluency showed the largest effect sizes between groups, showing lower scores in bvFTD than AD and HCs, and lower scores in AD than HC. Both AD and bvFTD showed a lower number of unique designs in design fluency in comparison to HC. Semantic fluency was correlated with left frontotemporal lobe in AD, and with left frontal, caudate, and thalamus in bvFTD. Percentage of unique designs in design fluency was associated with the metabolism of the bilateral fronto-temporo-parietal cortex in AD, and the bilateral frontal cortex with right predominance in bvFTD. Repetitions in AD were correlated with bilateral frontal, temporal, and parietal lobes, and with left prefrontal cortex in bvFTD.

Conclusions:

Our findings demonstrate differential underlying cognitive processes in verbal and design fluency in AD and bvFTD. While memory and executive functioning associated with fronto-temporo-parietal regions were key in AD, attention and executive functions correlated with the frontal cortex and played a more significant role in bvFTD during fluency tasks.

Type
Research Article
Copyright
Copyright © INS. Published by Cambridge University Press, 2021

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alvarez, J. A., & Emory, E. (2006). Executive function and the frontal lobes: a meta-analytic review. Neuropsychology Review, 16(1), 1742.CrossRefGoogle ScholarPubMed
Alzheimer’s Association. (2019). 2019 Alzheimer’s disease facts and figures. Alzheimer’s & Dementia, 15(3), 321387.CrossRefGoogle Scholar
Amunts, J., Camilleri, J.A., Eickhoff, S.B., Heim, S., & Weis, S. (2020). Executive functions predict verbal fluency scores in healthy participants. Scientific Reports, 10, 11141.CrossRefGoogle ScholarPubMed
Baddeley, A. (2000). The episodic buffer: a new component of working memory? Trends in Cognitive Sciences, 4(11), 417423.CrossRefGoogle ScholarPubMed
Baldo, J. V., Shimamura, A. P., Delis, D. C., Kramer, J., & Kaplan, E. (2001). Verbal and design fluency in patients with frontal lobe lesions. Journal of the International Neuropsychological Society, 7(5), 586596.CrossRefGoogle ScholarPubMed
Bettcher, B.M., Mungas, D., Patel, N., Elofson, J., Dutt, S., Wynn, M., … Kramer, J.H. (2016). Neuroanatomical substrates of executive functions: beyond prefrontal structures. Neuropsychologia, 85, 100109.CrossRefGoogle ScholarPubMed
Birn, R.M., Kenworthy, L., Case, L., Caravella, R., Jones, T.B., Bandettini, P.A., & Martin, A. (2010). Neural systems supporting lexical search guided by letter and semantic category cues: a self-paced overt response fMRI study of verbal fluency. NeuroImage, 49, 10991107.CrossRefGoogle ScholarPubMed
Borroni, B., Agosti, C., Premi, E., Cerini, C., Cosseddu, M., Paghera, B., … Padovani, A. (2010). The FTLD-modified Clinical Dementia Rating is a reliable tool for defining disease severity in frontotemporal lobar degeneration: evidence from a brain SPECT study. European Journal of Neurology, 17, 703707.CrossRefGoogle ScholarPubMed
Cipolotti, L., Molenberghs, P., Dominguez, J., Smith, N., Smirni, D., Xu, T., … Chan, E. (2020). Fluency and rule breaking behaviour in the frontal cortex. Neuropsychologia, 137, 107308.CrossRefGoogle ScholarPubMed
Cole, M.W., Reynolds, J.R., Power, J.D., Repovs, G., Anticevic, A., & Braver, T.S. (2013). Multi-task connectivity reveals flexible hubs for adaptive task control. Nature Neuroscience, 16, 13481355.CrossRefGoogle ScholarPubMed
Collette, F., Hogge, M., Salmon, E., & Van der Linden, M. (2006). Exploration of the neural substrates of executive functioning by functional neuroimaging. Neuroscience, 139(1), 209221.CrossRefGoogle ScholarPubMed
Copland, D. A., Brownsett, S., Iyer, K., & Angwin, A. J. (2021). Corticostriatal Regulation of Language Functions. Neuropsychology Review, 123.Google ScholarPubMed
Coyle-Gilchrist, I.T., Dick, K.M., Patterson, K., Rodríquez, P.V., Wehmann, E., Wilcox, A., …. Rowe, J.B. (2016). Prevalence, characteristics, and survival of frontotemporal lobar degeneration syndromes. Neurology, 86(18), 17361743.CrossRefGoogle ScholarPubMed
Cristofori, I., Cohen-Zimerman, S., & Grafman, J. (2019). Executive functions. Handbook of Clinical Neurology, 163, 197219.CrossRefGoogle ScholarPubMed
Delis, D.C., Kaplan, E., Kramer, J.H., Delis, D., & Kramer, J. (2001). Delis-Kaplan executive function system (D-KEFS). Examiner’s manual.Google Scholar
Della Rosa, P.A., Cerami, C., Gallivanone, F., Prestia, A., Caroli, A., Castiglioni, I., Gilardi, M.C., Frisoni, G., Friston, K., Ashburner, J, Perani, D., & the EADC-PET Consortium (2014). A standardized [18F]-FDG-PET template for spatial normalization in statistical parametric mapping of dementia. Neuroinformatics, 12, 575593.CrossRefGoogle ScholarPubMed
Fernández-Matarrubia, M., Matías-Guiu, J.A., Cabrera-Martín, M.N., Moreno-Ramos, T., Valles-Salgado, M., Carreras, J.L., & Matias-Guiu, J. (2017). Episodic memory dysfunction in behavioral variant frontotemporal dementia: a clinical and FDG-PET study. Journal of Alzheimer’s Disease, 57, 12511264.CrossRefGoogle ScholarPubMed
Fernández-Matarrubia, M., Matías-Guiu, J.A., Moreno-Ramos, T., & Matías-Guiu, J. (2014). Behavioural variant frontotemporal dementia: clinical and therapeutic approaches. Neurologia, 29, 464472.CrossRefGoogle ScholarPubMed
Folstein, M.F., Folstein, S.E., & McHugh, P. R. (1975). Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189198.Google Scholar
Friedman, N.P., & Miyake, A. (2017). Unity and diversity of executive functions: individual differences as a window on cognitive structure. Cortex, 86, 186204.CrossRefGoogle ScholarPubMed
Garavan, H., Ross, T.J., Murphy, K., Roche, R.A.P., & Stein, E.A (2002). Dissociable executive function in the dynamic control of behavior: inhibition, error detection, and correction. Neuroimage, 17, 18201829.CrossRefGoogle Scholar
Giovagnoli, A.R., Erbetta, A., Reati, F., & Bugiani, O (2008). Differential neuropsychological patterns of frontal variant frontotemporal dementia and Alzheimer's disease in a study of diagnostic concordance. Neuropsychologia, 46(5), 14951504.CrossRefGoogle Scholar
Glikmann-Johnston, Y., Oren, N., Hendler, T., & Shapira-Lichter, I. (2015). Distinct functional connectivity of the hippocampus during semantic and phonemic fluency. Neuropsychologia, 69, 3949.CrossRefGoogle ScholarPubMed
Hansen, S., Muenssinger, J., Kronhofmann, S., Lautenbacher, S., Oschmann, P., & Keune, P. M. (2017). Cognitive screening in multiple sclerosis: the five-point test as a substitute for the PASAT in measuring executive function. The Clinical Neuropsychologist, 31(1), 179192.CrossRefGoogle ScholarPubMed
Henry, J. D., & Crawford, J. R. (2004). A meta-analytic review of verbal fluency performance following focal cortical lesions. Neuropsychology, 18(2), 284.CrossRefGoogle ScholarPubMed
Henry, J. D., Crawford, J. R., & Phillips, L. H. (2004). Verbal fluency performance in dementia of the Alzheimer’s type: a meta-analysis. Neuropsychologia, 42(9), 12121222.CrossRefGoogle ScholarPubMed
Hutchinson, A. D., & Mathias, J. L. (2007). Neuropsychological deficits in frontotemporal dementia and Alzheimer’s disease: a meta-analytic review. Journal of Neurology, Neurosurgery & Psychiatry, 78(9), 917928.CrossRefGoogle ScholarPubMed
Jones-Gotman, M., & Milner, B. (1977). Design fluency: The invention of nonsense drawings after focal cortical lesions. Neuropsychologia, 15(4–5), 653674.CrossRefGoogle ScholarPubMed
Jurado, M.B., & Rosselli, M. (2007). The elusive nature of executive functions: a review of our current understanding. Neuropsychology Review, 17(3), 213233.CrossRefGoogle ScholarPubMed
Karr, J.E., Areshenkoff, C.N., Rast, P., Hofer, S.M., Iverson, G.L., & Garcia-Barrera, M.A. (2018). The unity and diversity of executive functions: a systematic review and re-analysis of latent variable studies. Psychology Bulletin, 144, 11471185.CrossRefGoogle ScholarPubMed
Knight, H.C., Smith, D.T., & Ellison, A. (2020). The role of the left dorsolateral prefrontal cortex in attentional bias. Neuropsychologia, 148, 107631.CrossRefGoogle ScholarPubMed
Kramer, J.H., Quitania, L., Dean, D., Neuhaus, J., Rosen, H.J., Halabi, C., Weiner, M.W., Magnotta, V.A., Delis, D.C., & Miller, B.L. (2007). Magnetic resonance imaging correlates of set shifting. Journal of the International Neuropsychological Society, 13(3), 386392.CrossRefGoogle ScholarPubMed
Laisney, M., Matuszewski, V., Mézenge, F., Belliard, S., de la Sayette, V., Eustache, F., & Desgrandes, B. (2009). The underlying mechanisms of verbal fluency deficit in frontotemporal dementia and semantic dementia. Journal of Neurology, 256, 10831094.CrossRefGoogle ScholarPubMed
Lee, G. P., Strauss, E., Loring, D. W., McCloskey, L., Haworth, J. M., & Lehman, R. A. (1997). Sensitivity of figural fluency on the five-point test to focal neurological dysfunction. The Clinical Neuropsychologist, 11(1), 5968.CrossRefGoogle Scholar
Lezak, M. D., Howieson, D. B., Loring, D. W., & Fischer, J. S. (2004). Neuropsychological assessment. Oxford, USA: Oxford University Press.Google Scholar
Libon, D.J., McMillan, C., Gunawardena, D., Powers, C., Massimo, L., Khan, A., Morgan, B., Farag, C., Richmond, L., Weinstein, J., Moore, P., Coslett, H.B., Chatterjee, A., Aguirre, G., & Grossman, M. (2009). Neurocognitive contributions to verbal fluency deficits in frontotemporal lobar degeneration. Neurology, 73(7), 535542.CrossRefGoogle ScholarPubMed
Matias-Guiu, J.A., Cabrera-Martín, M.N., Valles-Salgado, M., Pérez-Pérez, A., Rognoni, T., Moreno-Ramos, T., … Matias-Guiu, J. (2017). Neural basis of cognitive assessment in Alzheimer Disease, Amnestic Mild Cognitive Impairment, and Subjective Memory Complaints. American Journal of Geriatric Psychiatry, 25, 730740.CrossRefGoogle ScholarPubMed
Matias-Guiu, J.A., Cabrera-Martín, M.N., Valles-Salgado, M., Rognoni, T., Galán, L., Moreno-Ramos, T., … Matias-Guiu, J. (2019). Inhibition impairment in frontotemporal dementia, amyotrophic lateral sclerosis, and Alzheimer’s disease: clinical assessment and metabolic correlates. Brain Imaging and Behavior, 13, 651659.CrossRefGoogle ScholarPubMed
Matias-Guiu, J.A., Fernández de Bobadilla, R., Escudero, G., Pérez-Pérez, J., Cortés, A., Morenas-Rodríguez, E., … Matias-Guiu, J. (2015). Validation of the Spanish version of Addenbrooke’s Cognitive Examination III for diagnosing dementia. Neurologia, 30, 545551.CrossRefGoogle ScholarPubMed
Matias-Guiu, J.A., Fernández-Bobadilla, R., Fernández-Oliveira, A., Valles-Salgado, M., Rognoni, T., Cortés-Martínez, A., … Matias-Guiu, J. (2016). Normative data for the Spanish version of the Addenbrooke’s Cognitive Examination III. Dementia and Geriatric Cognitive Disorders, 41, 243250.CrossRefGoogle ScholarPubMed
Matias-Guiu, J.A., Pytel, V., Delgado-Álvarez, A., Delgado-Alonso, A., Cortés-Martínez, A., Fernández-Oliveira, A., … Matias-Guiu, J. (2021). The Five-Point Test: normative data for middle-aged and elderly Spaniards. Applied Neuropsychology: Adult 2020.Google Scholar
McKhann, G. M., Knopman, D. S., Chertkow, H., Hyman, B. T., Jack, C. R. Jr, Kawas, C. H., … Mohs, R. C. (2011). The diagnosis of dementia due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s & Dementia, 7(3), 263269.CrossRefGoogle Scholar
Menon, V. (2011). Large-scale brain networks and psychopathology: a unifying triple network model. Trends in Cognitive Sciences, 15(10), 483506.CrossRefGoogle ScholarPubMed
Metzger, F.G., Schopp, B., Hauessinger, F.B., Dehnen, K., Synofzik, M., Fallgatter, A.J., & Ehlhis, A.C. (2016). Brain activation in frontotmporal and Alzheimer’s dementia: a functional near-infrared spectroscopy study. Alzheimer’s Research & Therapy, 8(1), 56.CrossRefGoogle ScholarPubMed
Migliaccio, R., Tanguy, D., Bouzigues, A., Sezer, I., Dubois, B., Le Ber, I., … Levy, R. (2020). Cognitive and behavioural inhibition deficits in neurodegenerative dementias. Cortex, 131, 265283.CrossRefGoogle ScholarPubMed
Miyake, A., Friedman, N. P., Emerson, M. J., Witzki, A. H., Howerter, A., & Wager, T. D. (2000). The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: A latent variable analysis. Cognitive Psychology, 41(1), 49100.CrossRefGoogle ScholarPubMed
Morris, J.C. (1993). The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology, 43, 24122414.CrossRefGoogle ScholarPubMed
Olazarán, J., Hoyos-Alonso, M.C., del Ser, T., Garrido Barral, A., Conde-Sala, J.L., Bermejo-Pareja, F., … Carnero-Pardo, C. (2016). Practical application of brief cognitive tests. Neurologia, 31(3), 183194.CrossRefGoogle ScholarPubMed
Olazarán, J., Mouronte, P., & Bermejo, F. (2005). Clinical validity of two scales of instrumental activities in Alzheimer’s disease. Neurología, 20, 395401.Google ScholarPubMed
Olney, N. T., Spina, S., & Miller, B. L. (2017). Frontotemporal dementia. Neurologic Clinics, 35(2), 339374.CrossRefGoogle ScholarPubMed
Pa, J., Possin, K.L., Wilson, S.M., Quitania, L.C., Kramer, J.H., Boxer, A.L., …, Johnson, J. K. (2010). Gray matter correlates of set-shifting among neurodegenerative disease, mild cognitive impairment, and healthy older adults. Journal of the International Neuropsychological Society, 16, 640650.CrossRefGoogle ScholarPubMed
Peña-Casanova, J., Blesa, R., Aguilar, M., Gramunt-Fombuena, N., Gómez-Ansón, B., Oliva, R., … Sol, J. M. (2009). Spanish multicenter normative studies (NEURONORMA project): Methods and sample characteristics. Archives of Clinical Neuropsychology, 24(4), 307319.CrossRefGoogle ScholarPubMed
Peña-Casanova, J., Gramunt Fombuena, N., & Gich Fullà, J. (2004). Test neuropsicológicos. Fundamentos para una neurología clínica basada en la evidencia. Masson, Spain.Google Scholar
Peter, J., Kaiser, J., Landerer, V., Köstering, L., Kaller, C. P., Heimbach, B., … Klöppel, S. (2016). Category and design fluency in mild cognitive impairment: Performance, strategy use, and neural correlates. Neuropsychologia, 93, 2129.CrossRefGoogle ScholarPubMed
Poos, J.M., Jiskoot, L.C., Papma, J.M., van Swieten, J.C., & van den Berg, E. (2018). Meta-analytic review of memory impairment in behavioral variant frontotemporal dementia. Journal of the International Neuropsychological Society, 24, 593605.CrossRefGoogle ScholarPubMed
Possin, K. L., Chester, S. K., Laluz, V., Bostrom, A., Rosen, H. J., Miller, B. L., & Kramer, J.H. (2012). The frontal-anatomic specificity of design fluency repetitions and their diagnostic relevance for behavioral variant frontotemporal dementia. Journal of the International Neuropsychological Society, 18(5), 834844.CrossRefGoogle ScholarPubMed
Rascovsky, K., Hodges, J. R., Knopman, D., Mendez, M. F., Kramer, J. H., Neuhaus, J., … Hillis, A. E. (2011). Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain, 134(9), 24562477.CrossRefGoogle ScholarPubMed
Rascovsky, K., Salmon, D.P., Hansen, L.A., Thal, L.J, & Galasko, D. (2007). Disparate letter and semantic category fluency deficits in autopsy-confirmed frontotemporal dementia and Alzhiemer’s disease. Neuropsychology, 21, 2030.CrossRefGoogle Scholar
Regard, M., Strauss, E., & Knapp, P. (1982). Children’s production on verbal and non-verbal fluency tasks. Perceptual and motor skills, 55(3), 839844.CrossRefGoogle ScholarPubMed
Robinson, G., Shallice, T., Bozzali, M., & Cipolotti, L. (2012). The differing roles of the frontal cortex in fluency tests. Brain, 135(7), 22022214.CrossRefGoogle ScholarPubMed
Rodríguez-Aranda, C., Waterloo, K., Johnsen, S.H., Eldevik, P., Sparr, S., Wikran, G.C., Herder, M., & Vangberg, T.R. (2016). Neuroanatomical correlates of verbal fluency in early Alzheimer’s disease and normal aging. Brain and Language, 155–156, 2435.CrossRefGoogle ScholarPubMed
Ruff, R. M., Allen, C. C., Farrow, C. E., Niemann, H., & Wylie, T. (1994). Figural fluency: differential impairment in patients with left versus right frontal lobe lesions. Archives of Clinical Neuropsychology, 9(1), 4155.CrossRefGoogle ScholarPubMed
Ruff, R. M., Light, R. H., & Evans, R. W. (1987). The Ruff Figural Fluency Test: a normative study with adults. Developmental neuropsychology, 3(1), 3751.CrossRefGoogle Scholar
Schurgin, M.W. (2018). Visual memory, the long and the sort of it: a review of visual working memory and long-term memory. Attention, Perception, & Psychophysics, 80(5): 10351056.CrossRefGoogle Scholar
So, M., Foxe, D., Kumfor, F., Murray, C., Hsieh, S., Savage, G., … Piguet, O. (2018). Addenbrooke’s Cognitive Examination: psychometric characteristics and relations to functional ability in dementia. Journal of the International Neuropsychological Society, 24(8), 854863.CrossRefGoogle ScholarPubMed
Stopford, C. L., Thompson, J. C., Neary, D., Richardson, A. M., & Snowden, J. S. (2012). Working memory, attention, and executive function in Alzheimer’s disease and frontotemporal dementia. Cortex, 48(4), 429446.CrossRefGoogle ScholarPubMed
Strauss, E., Sherman, E.M.S., & Spreen, O. (2006). A compendium of neuropsychological tests: administration, norms, and commentary (3rd ed.). Oxford University Press.Google Scholar
Suchy, Y., Kraybill, M.L., & Gidley Larson, J.C. (2010). Understanding design fluency: motor and executive contributions. Journal of the International Neuropsychological Society, 16(1) 2637.CrossRefGoogle ScholarPubMed
Sutin, A. R., Stephan, Y., & Terracciano, A. (2019). Verbal fluency and risk of dementia. International Journal of Geriatric Psychiatry, 34(6), 863867.CrossRefGoogle ScholarPubMed
van den Berg, E., Jiskoot, L.C., Grosveld, M.J.H., van Switen, J.C., & Papma, J.M. (2017). Qualitative Assessment of verbal fluency performance in frontotemporal dementia. Dementia and Geriatrics Cognitive Disorders, 44(1–2), 3544.CrossRefGoogle ScholarPubMed
Varrone, A., Asenbaum, S., Vander Borght, T., Booij, J., Nobili, F., Någren, K., Darcourt, J., Kapucu, Ö.L., Tatsch, K., Bartenstein, P., & Van Laere, K. (2009). EANM procedure guidelines for PET brain imaging using [18 F] FDG, version 2. European Journal of Nuclear Medicine and Molecular Imaging, 36, 21032110.CrossRefGoogle Scholar
Vaughan, R. M., Coen, R. F., Kenny, R., & Lawlor, B. A. (2018). Semantic and Phonemic Verbal Fluency Discrepancy in Mild Cognitive Impairment: Potential Predictor of Progression to Alzheimer’s Disease. Journal of the American Geriatric Society, 66(4), 755759.CrossRefGoogle ScholarPubMed
Wagner, S., Sebastian, A., Lieb, K., Tüscher, O., & Tadic, A. (2014). A coordinate-based ALE functional MRI meta-analysis of brain activation during verbal fluency tasks in healthy control subjects. BMC Neuroscience, 15, 19.CrossRefGoogle ScholarPubMed
Whiteside, D.M., Kealey, T., Semla, M., Luu, H., Rice, L., … Roper, B. (2016). Verbal fluency: language or executive function measure? Applied Neuropsychology Adult, 23, 2934.CrossRefGoogle ScholarPubMed
Whitwell, J.L., & Jack, C.R. Jr (2005). Comparison between Alzheimer’s disease, frontotemporal lobar degeneration, and normal aging with brain mapping. Topics in Magnetic Resonance Imaging, 16(6), 409425.CrossRefGoogle Scholar
Witt, S.T., van Ettinger-Veenstra, H., Salo, T., Riedel, M.C., & Laird, A.R. (2021). What executive function network is that? An image-based meta-analysis of network labels. Brain Topography. doi: 10.1007/s10548-021-00847-z.CrossRefGoogle ScholarPubMed
Wittenberg, D., Possin, K.L., Rascovsky, K., Rankin, K.P., Miller, B.L., & Kramer, J.H. (2008). The early neuropsychological and behavioral characteristics of frontotemporal dementia. Neuropsychology Review, 18, 91102.CrossRefGoogle ScholarPubMed
Woods, D. L., Wyma, J. M., Herron, T. J., & Yund, E. W. (2016). A computerized test of design fluency. PLoS One, 11(5).CrossRefGoogle ScholarPubMed
Yeo, B.T.T., Krienen, F.M., Sepulcre, J., Sabuncu, M.R., Lashkari, D., Hollinshead, M., … Buckner, R.L. (2011). The organization of the human cerebral cortex estimated by intrinsic functional connectivity. Journal of Neurophysiology, 106, 11251165.Google ScholarPubMed
Zukotynksi, K., Gaudet, V., Kuo, P.H., Adamo, S., Goubran, M., Scott, C.J.M., … Black, S.E. (2020). The use of random forests to identify brain regions on amyloid and FDG PET associated with MoCA score. Clinical Nuclear Medicine, 45, 427433.CrossRefGoogle Scholar
Supplementary material: File

Delgado-Álvarez et al. supplementary material

Delgado-Álvarez et al. supplementary material

Download Delgado-Álvarez et al. supplementary material(File)
File 1.1 MB