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Differential impairment in semantic, phonemic, and action fluency performance in Friedreich's ataxia: Possible evidence of prefrontal dysfunction

Published online by Cambridge University Press:  18 October 2007

ÉRIKA DE NÓBREGA ,
ANTONIETA NIETO ,
JOSÉ BARROSO  and
FERNANDO MONTÓN
ÉRIKA DE NÓBREGA
Affiliation:
Faculty of Psychology, University of La Laguna, La Laguna, Tenerife, Canary Islands, Spain.
ANTONIETA NIETO
Affiliation:
Faculty of Psychology, University of La Laguna, La Laguna, Tenerife, Canary Islands, Spain.
JOSÉ BARROSO
Affiliation:
Faculty of Psychology, University of La Laguna, La Laguna, Tenerife, Canary Islands, Spain.
FERNANDO MONTÓN
Affiliation:
Department of Neurology, N.S.C. University Hospital, Santa Cruz de Tenerife, Canary Islands, Spain.
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Abstract

This study examined phonemic (letters), semantic (animals) and action verbal fluency cues in twenty-four patients with FRDA, and twenty matched healthy control subjects. The Action Fluency Test (AFT) is a newly-developed verbal fluency cue that consists in asking the subject to rapidly generate verbs. Given the high presence of dysarthria and cognitive slowness in FRDA patients, control tasks were administered in order to dissociate motor/articulatory impairment and cognitive slowness from verbal fluency deficit. Results showed that patients and control subjects performed similarly on the semantic fluency task. In contrast, patients performed significantly poorer on phonemic and action fluency tests. Correlational analyses showed that the deficits cannot be attributed to dysarthria or cognitive slowness. Although executive processes are necessary for initiating and monitoring all verbal fluency tasks, phonemic and action fluency may place a greater burden on strategic processes, given that they require a more unusual type of lexicon search. Thus, the deficits found occur in tasks that require greater executive/prefrontal control. This impairment might be the result of an affectation of cerebellum-prefrontal cortex connections, although the possibility of a primary prefrontal dysfunction remains to be investigated. (JINS, 2007, 13, 944–952.)

Keywords

CerebellumCognitionExecutive functionsCerebellar ataxiaVerb generationLanguage
Type
Research Article
Information
Journal of the International Neuropsychological Society , Volume 13 , Issue 6 , November 2007 , pp. 944 - 952
Copyright
© 2007 The International Neuropsychological Society

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References

REFERENCES

Allen, G., McColl, R., Barnard, H., Ringe, W.K., Fleckenstein, J., & Cullum, C.M. (2005). Magnetic resonance imaging of cerebellar-prefrontal and cerebellar-parietal functional connectivity. Neuroimage, 28, 39–48.Google Scholar
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, 586–596.CrossRefGoogle Scholar
Beatty, W.W. & Goodkin, D.E. (1990). Screening for cognitive impairment in multiple sclerosis. An evaluation of the Mini-Mental State Examination. Archives of Neurology, 47, 297–301.CrossRefGoogle Scholar
Benton, A.L. & Hamsher, K. (1989). Multilingual Aphasia Examination. (2nd ed). Iowa City, IA: The University of Iowa.
Berciano, J., Infante, J., Mateo, I., & Combarros, O. (2002). Hereditary ataxias and paraplegias: A clinicogenetic review. Neurologia, 17, 40–51.Google Scholar
Berent, S., Giordani, B., Gilman, S., Junck, L., Lehtinen, S., Markel, D.S., Boivin, M., Kluin, K.J., Parks, R., & Koeppe, R.A. (1990). Neuropsychological changes in olivopontocerebellar atrophy. Archives of Neurology, 47, 997–1001.Google Scholar
Bidichandani, S.I., Ashizawa, T., & Patel, P.I. (1998). The GAA triplet-repeat expansion in Friedreich Ataxia interferes with transcription and may be associated with an unusual DNA structure. The American Journal of Human Genetics, 62, 111–121.CrossRefGoogle Scholar
Billingsley, R.L., Simos, P.G., Castillo, E.M., Sarkari, S., Breier, J.I., Pataraia, E., & Papanicolau, A.C. (2004). Spatio-temporal cortical dynamics of phonemic and semantic fluency. Journal of Clinical and Experimental Neuropsychology, 26, 1031–1043.CrossRefGoogle Scholar
Boivin, M.J., Giordani, B., Berent, S., Amato, D.A., Lehtinen, S., Koeppe, R.A., Buchtel, H.A., Foster, N.L., & Kuhl, D.E. (1992). Verbal fluency and positron emission tomographic mapping of regional cerebral glucose metabolism. Cortex, 28, 231–239.Google Scholar
Botez, M.I., Pedraza, O.L., Botez-Marquard, T., Vezina, J.L., & Elie, R. (1993). Radiologic correlates of reaction time measurements in olivopontocerebellar atrophy. European Neurology, 33, 304–309.Google Scholar
Botez-Marquard, T. & Botez, M.I. (1993). Cognitive behavior in heredodegenerative ataxias. European Neurology, 33, 351–357.CrossRefGoogle Scholar
Botez-Marquard, T. & Botez, M.I. (1997). Olivopontocerebellar atrophy and Friedreich's ataxia: Neuropsychological consequences of bilateral versus unilateral cerebellar lesions. International Review of Neurobiology, 41, 387–410.CrossRefGoogle Scholar
Brickman, A.M., Paul, R.H., Cohen, R.A., Williams, L.M., MacGregor, K.L., Jefferson, A.L., Tate, D.F., Gunstad, J., & Gordon, E. (2005). Category and letter verbal fluency across the adult lifespan: Relationship to EEG theta power. Archives of Clinical Neuropsychology, 20, 561–573.CrossRefGoogle Scholar
Bürk, K., Globas, C., Bosch, S., Graber, S., Abele, M., Brice, A., Dichgans, J., Daum, I., & Klockgether, T. (1999). Cognitive deficits in spinocerebellar ataxia 2. Brain, 122 (Pt 4), 769–777.CrossRefGoogle Scholar
Campuzano, V., Montermini, L., Moltó, M.D., Pianese, L., Cossee, M., & Cavalcanti, F. (1996). Friedreich's Ataxia: Autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science, 271, 1243–1247.Google Scholar
Cuenod, C.A., Bookheimer, S.Y., Hertz-Pannier, L., Zeffiro, T.A., Theodore, W.H., & Le Bihan, D. (1995). Functional MRI during word generation, using conventional equipment: A potential tool for language localization in the clinical environment. Neurology, 45, 1821–1827.Google Scholar
Damasio, A.R. & Tranel, D. (1993). Nouns and verbs are retrieved with differently distributed neural systems. Proceedings of the National Academy of Sciences USA, 90, 4957–4960.CrossRefGoogle Scholar
Daniele, A., Giustolisi, L., Silveri, M.C., Colosimo, C., & Gainotti, G. (1994). Evidence for a possible neuroanatomical basis for lexical processing of nouns and verbs. Neuropsychologia, 32, 1325–1341.CrossRefGoogle Scholar
De Michele, G., Di Salle, F., Filla, A., D'Alessio, G., Ambrosio, G., Viscardi, L., Scala, R., & Campanella, G. (1995). Magnetic resonance imaging in “typical” and “late onset” Friedreich's disease and early onset cerebellar ataxia with retained tendon reflexes. Italian Journal of Neurological Sciences, 16, 303–308.CrossRefGoogle Scholar
Dürr, A., Cossee, M., Agid, Y., Campuzano, V., Mignard, C., Penet, C., Mandel, J.L., Brice, A., & Koening, M. (1996). Clinical and genetic abnormalities in patients with Friedreich's Ataxia. The New England Journal of Medicine, 335, 1169–1175.CrossRefGoogle Scholar
Elfgren, C.I. & Risberg, J. (1998). Lateralized frontal blood flow increases during fluency tasks: Influence of cognitive strategy. Neuropsychologia, 36, 505–512.CrossRefGoogle Scholar
Fehrenbach, R.A., Wallesch, C.W., & Claus, D. (1984). Neuropsychologic findings in Friedreich's Ataxia. Archives of Neurology, 41, 306–308.CrossRefGoogle Scholar
Frith, C.D., Friston, K.J., Liddle, P.F., & Frackowiak, R.S. (1991). A PET study of word finding. Neuropsychologia, 29, 1137–1148.CrossRefGoogle Scholar
Fu, C.H., McIntosh, A.R., Kim, J., Chau, W., Bullmore, E.T., Williams, S.C., Honey, G.D., & McGuire, P.K. (2006). Modulation of effective connectivity by cognitive demand in phonological verbal fluency. Neuroimage, 30, 266–271.CrossRefGoogle Scholar
García-Albea, J.E., Sánchez Bernardos, M.L., & del Viso, S. (1986). Boston Diagnostic Aphasia Examination: Spanish Adaptation. [Original version: (Goddglass & Kaplan, 1983)].
Gourovitch, M.L., Kirkby, B.S., Goldberg, T.E., Weinberger, D.R., Gold, J.M., Esposito, G., Van Horn, J.D., & Berman, K.F. (2000). A comparison of rCBF patterns during letter and semantic fluency. Neuropsychology, 14, 353–360.CrossRefGoogle Scholar
Harding, A.E. (1981). Friedreich's Ataxia: A clinical and genetic study of 90 families with an analysis of early diagnostic criteria and intrafamilial clustering of clinical features. Brain, 104, 589–620.CrossRefGoogle Scholar
Hart, R.P., Kwentus, J.A., Leshner, R.T., & Frazier, R. (1985). Information processing speed in Friedreich's Ataxia. Annals of Neurology, 17, 612–614.CrossRefGoogle Scholar
Helmuth, L.L., Ivry, R.B., & Shimizu, N. (1997). Preserved performance by cerebellar patients on tests of word generation, discrimination learning, and attention. Learning & Memory, 3, 456–474.CrossRefGoogle Scholar
Hirono, N., Yamadori, A., Kameyama, M., Mezaki, T., & Abe, K. (1991). Spinocerebellar degeneration (SCD): Cognitive disturbances. Acta Neurologica Scandinavica, 84, 226–230.CrossRefGoogle Scholar
Hubrich-Ungureanu, P., Kaemmerer, N., Henn, F.A., & Braus, D.F. (2002). Lateralized organization of the cerebellum in a silent verbal fluency task: A functional magnetic resonance imaging study in healthy volunteers. Neuroscience Letter, 319, 91–94.CrossRefGoogle Scholar
Ivry, R.B. & Fiez, J.A. (2000). Cerebellar Contributions to Cognition and Imagery. In M.S. Gazzaniga (Ed.), The New Cognitive Neurosciences. (2nd ed.). Cambridge, MA: The MIT Press.
Junck, L., Gilman, S., Gebarski, S., Koeppe, R., Kluin, K., & Markel, D. (1994). Structural and functional brain imaging in Friedreich's ataxia. Archives of Neurology, 51, 349–355.CrossRefGoogle Scholar
Lamarche, J.B., Lemieux, B., & Lieu, H.B. (1984). The neuropathology of “typical” Friedreich's ataxia in Quebec. Canadian Journal of Neurological Sciences, 11, 592–600.CrossRefGoogle Scholar
Leggio, M.G., Silveri, M.C., Petrosini, L., & Molinari, M. (2000). Phonological grouping is specifically affected in cerebellar patients: A verbal fluency study. Journal of Neurology, Neurosurgery & Psychiatry, 69, 102–106.CrossRefGoogle Scholar
Leiner, H.C., Leiner, A.L., & Dow, R.S. (1986). Does the cerebellum contribute to mental skills? Behavioural Neuroscience, 100, 443–454.Google Scholar
Leiner, H.C., Leiner, A.L., & Dow, R.S. (1993). Cognitive and language functions of the human cerebellum. Trends in Neurosciences, 16, 444–447.CrossRefGoogle Scholar
Lezak, M.D. (1995). Neuropsychological Assessment. (3rd ed.). New York: Oxford University Press.
Mantovan, M.C., Martinuzzi, A., Squarzanti, F., Bolla, A., Silvestri, I., Liessi, G., Macchi, C., Ruzza, G., Trevisan, C.P., & Angelini, C. (2006). Exploring mental status in Friedreich's Ataxia: A combined neuropsychological, behavioral and neuroimaging study. European Journal of Neurology, 13, 827–35.CrossRefGoogle Scholar
Martin, A., Haxby, J.V., Lalonde, F.M., Wiggs, C.L., & Ungerleider, L.G. (1995). Discrete cortical regions associated with knowledge of color and knowledge of action. Science, 270, 102–105.CrossRefGoogle Scholar
Martin, A., Wiggs, C.L., Lalonde, F., & Mack, C. (1994). Word retrieval to letter and semantic cues: A double dissociation in normal subjects using interference tasks. Neuropsychologia, 32, 1487–1494.CrossRefGoogle Scholar
Middleton, F.A. & Strick, P.L. (1994). Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. Science, 266, 458–461.CrossRefGoogle Scholar
Middleton, F.A. & Strick, P.L. (1997). Dentate output channels: Motor and cognitive components. Progress in Brain Research, 114, 553–66.CrossRefGoogle Scholar
Nieto Barco, A., Wollmann Engeby, T., & Barroso Ribal, J. (2004). Cerebellum and cognitive processes. Anales de Psicología, 20, 205–221.Google Scholar
Nobile-Orazio, E., Baldini, L., & Barbieri, S. (1988). Treatment of patients with neuropathy and anti-MAG IgM M-proteins. Annals of Neurology, 24, 93–97.CrossRefGoogle Scholar
Oppenheimer, D.R. (1979). Brain lesions in Friedreich's ataxia. Canadian Journal of Neurological Sciences, 6, 173–176.CrossRefGoogle Scholar
Oppenheimer, D.R. & Esiri, M.M. (1992). Diseases of the basal ganglia, cerebellum and motor neurons. In J.H. Adams & L.W. Duchen (Ed.), Greenfield's Neuropathology. London: Edward Arnold.
Pandolfo, M. (2002). Frataxin deficiency and mitochondrial dysfunction. Mitochondrion, 2, 87–93.CrossRefGoogle Scholar
Papathanassiou, D., Etard, O., Mellet, E., Zago, L., Mazoyer, B., & Tzourio-Mazoyer, N. (2000). A common language network for comprehension and production: A contribution to the definition of language epicenters with PET. Neuroimage, 11, 347–357.CrossRefGoogle Scholar
Parks, R.W., Loewenstein, D.A., Dodrill, K.L., Barker, W.W., Yoshii, F., Chang, J.Y., Emran, A., Apicella, A., Sheramata, W.A., & Duara, R. (1988). Cerebral metabolic effects of a verbal fluency test: A PET scan study. Journal of Clinical and Experimental Neuropsychology, 10, 565–575.CrossRefGoogle Scholar
Perani, D., Cappa, S.F., Schnur, T., Tettamanti, M., Collina, S., Rosa, M.M., & Fazio, R. (1999). The neural correlates of verb and noun processing. A PET study. Brain, 122, 2337–2344.CrossRefGoogle Scholar
Petersen, S.E., Fox, P.T., Posner, M., Mintun, M., & Raichle, M.E. (1989). Positron emission tomographic studies of the processing of single words. The Journal of Cognitive Neuroscience, 1, 53–170.Google Scholar
Petersen, S.E., van Mier, H., Fiez, J.A., & Raichle, M.E. (1998). The effects of practice on the functional anatomy of task performance. Proceedings of the National Academy of Sciences USA, 95, 853–860.CrossRefGoogle Scholar
Piatt, A.L., Fields, J.A., Paolo, A.M., Koller, W.C., & Troster, A.I. (1999a). Lexical, semantic, and action verbal fluency in Parkinson's disease with and without dementia. Journal of Clinical and Experimental Neuropsychology, 21, 435–443.Google Scholar
Piatt, A.L., Fields, J.A., Paolo, A.M., & Troster, A.I. (1999b). Action (verb naming) fluency as an executive function measure: Convergent and divergent evidence of validity. Neuropsychologia, 37, 1499–1503.Google Scholar
Pihlajamäki, M., Tanila, H., Hanninen, T., Kononen, M., Laakso, M., Partanen, K., Soininen, H., & Aronen, H.J. (2000). Verbal fluency activates the left medial temporal lobe: A functional magnetic resonance imaging study. Annals of Neurology, 47, 470–476.3.0.CO;2-M>CrossRefGoogle Scholar
Raichle, M.E., Fiez, J.A., Videen, T.O., MacLeod, A.M., Pardo, J.V., Fox, P.T., & Petersen, S.E. (1994). Practice-related changes in human brain functional anatomy during nonmotor learning. Cerebral Cortex, 4, 8–26.CrossRefGoogle Scholar
Richter, S., Kaiser, O., Hein-Kropp, C., Dimitrova, A., Gizewski, E., Beck, A., Aurich, V., Ziegler, W., & Timmann, D. (2004). Preserved verb generation in patients with cerebellar atrophy. Neuropsychologia, 42, 1235–1246.CrossRefGoogle Scholar
Schlösser, R., Hutchinson, M., Joseffer, S., Rusinek, H., Saarimaki, A., Stevenson, J., Dewey, S.L., & Brodie, J.D. (1998). Functional magnetic resonance imaging of human brain activity in a verbal fluency task. Journal of Neurology, Neurosurgery & Psychiatry, 64, 492–498.CrossRefGoogle Scholar
Schmahmann, J.D. (1991). An emerging concept. The cerebellar contribution to higher function. Archives of Neurology, 48, 1178–1187.CrossRefGoogle Scholar
Schmahmann, J.D. & Pandya, D.N. (1995). Prefrontal cortex projections to the basilar pons in rhesus monkey: Implications for the cerebellar contribution to higher function. Neuroscience Letter, 199, 175–178.CrossRefGoogle Scholar
Schmahmann, J.D. & Sherman, J.C. (1998). The cerebellar cognitive affective syndrome. Brain, 121, 561–579.CrossRefGoogle Scholar
Schuhfried, G. (1992). Vienna Reaction Unit (manual). Austria: Schuhfried Ges.m.b.H.
Seger, C.A., Desmond, J.E., Glover, G.H., & Gabrieli, J.D. (2000). Functional magnetic resonance imaging evidence for right-hemisphere involvement in processing unusual semantic relationships. Neuropsychology, 14, 361–369.CrossRefGoogle Scholar
Shedlack, K.J., Hunter, R., Wyper, D., McLuskie, R., Fink, G., & Goodwin, G.M. (1991). The pattern of cerebral activity underlying verbal fluency shown by split-dose single photon emission tomography (SPET or SPECT) in normal volunteers. Psychological Medicine, 21, 687–696.CrossRefGoogle Scholar
Storey, E., Forrest, S.M., Shaw, J.H., Mitchell, P., & Gardner, R.J. (1999). Spinocerebellar ataxia type 2: Clinical features of a pedigree displaying prominent frontal-executive dysfunction. Archives of Neurology, 56, 43–50.CrossRefGoogle Scholar
Stuss, D.T., Alexander, M.P., Hamer, L., Palumbo, C., Dempster, R., Binns, M., Levine, B., & Izukawa, D. (1998). The effects of focal anterior and posterior brain lesions on verbal fluency. Journal of the International Neuropsychological Society, 4, 265–278.Google Scholar
Van Swieten, J.C., Koudstaal, P.K., Visser, M.C., Schouten, H.J.A., & van Gijn, J. (1988). Interobserver agreement for the assessment of handicap in stroke patients. Stroke, 19, 604–607.CrossRefGoogle Scholar
Waldvogel, D., Van Gelderen, P., & Hallett, M. (1999). Increased iron in the dentate nucleus of patients with Friedreich Ataxia. Annals of Neurology, 46, 123–125.3.0.CO;2-H>CrossRefGoogle Scholar
Wechsler, D. (1997). Wechsler Adult Intelligence Scale (3rd ed.). Administration and Scoring Manual. San Antonio, TX, USA: The Psychological Corporation.
White, M., Lalonde, R., & Botez-Marquard, T. (2000). Neuropsychologic and neuropsychiatric characteristics of patients with Friedreich's Ataxia. Acta Neurologica Scandinavica, 102, 222–226.CrossRefGoogle Scholar
Wollmann, T., Barroso, J., Montón, F., & Nieto, A. (2002). Neuropsychological test performance of patients with Friedreich's Ataxia. Journal of Clinical and Experimental Neuropsychology, 24, 677–686.CrossRefGoogle Scholar
Wollmann, T., Nieto-Barco, A., Montón-Alvarez, F., & Barroso-Ribal, J. (2004). [Friedreich's Ataxia: Analysis of magnetic resonance imaging parameters and their correlates with cognitive and motor slowing]. Revista de Neurología, 38, 217–222.Google Scholar
Woods, S.P., Carey, C.L., Troster, A.I., & Grant, I. (2005a). Action (verb) generation in HIV-1 infection. Neuropsychologia, 43, 1144–1151.Google Scholar
Woods, S., Morgan, E.E., Dawson, M., Cobb, S.J., & Grant, I. (2006). Action (verb) fluency predicts dependence in instrumental activities of daily living in persons infected with HIV-1. Journal of Clinical and Experimental Neuropsychology, 28, 1030–1042.CrossRefGoogle Scholar
Woods, S.P., Scott, J.C., Sires, D.A., Grant, I., Heaton, R.K., & Troster, A.I. (2005b). Action (verb) fluency: Test-retest reliability, normative standards, and construct validity. Journal of the International Neuropsychological Society, 11, 408–415.Google Scholar