Generic placeholder image

Current Alzheimer Research

Editor-in-Chief

ISSN (Print): 1567-2050
ISSN (Online): 1875-5828

Research Article

Connected Speech Deficit as an Early Hallmark of CSF-defined Alzheimer’s Disease and Correlation with Cerebral Hypoperfusion Pattern

Author(s): Giulia Mazzon*, Miloš Ajčević, Tatiana Cattaruzza, Alina Menichelli, Michele Guerriero, Selene Capitanio, Valentina Pesavento, Franca Dore, Sandro Sorbi, Paolo Manganotti and Andrea Marini

Volume 16, Issue 6, 2019

Page: [483 - 494] Pages: 12

DOI: 10.2174/1567205016666190506141733

Price: $65

Abstract

Background: Diagnosis of prodromal Alzheimer's disease (AD) still represents a hot topic and there is a growing interest for the detection of early and non-invasive biomarkers. Although progressive episodic memory impairment is the typical predominant feature of AD, communicative difficulties can be already present at the early stages of the disease.

Objective: This study investigated the narrative discourse production deficit as a hallmark of CSFdefined prodromal AD and its correlation with cerebral hypoperfusion pattern.

Methods: Narrative assessment with a multilevel procedure for discourse analysis was conducted on 28 subjects with Mild Cognitive Impairment (15 MCI due to AD; 13 MCI non-AD) and 28 healthy controls. The diagnostic workup included CSF AD biomarkers. Cerebral hypoperfusion pattern was identified by SPECT image processing.

Results: The results showed that the discourse analysis of global coherence and lexical informativeness indexes allowed to identify MCI due to AD from MCI non-AD and healthy subjects. These findings allow to hypothesize that the loss of narrative efficacy could be a possible early clinical hallmark of Alzheimer’s disease. Furthermore, a significant correlation of global coherence and lexical informativeness reduction with the SPECT hypoperfusion was found in the dorsal aspect of the anterior part of the left inferior frontal gyrus, supporting the hypothesis that this area has a significant role in communicative efficacy, and in particular, in semantic selection executive control.

Conclusion: This study contributes to the understanding of the neural networks for language processing and their involvement in prodromal Alzheimer's disease. It also suggests an easy and sensitive tool for clinical practice that can help identifying individuals with prodromal Alzheimer’s disease.

Keywords: Mild cognitive impairment, Alzheimer’s disease, connected speech, language disorders, functional neuroimaging, lexical impairments.

[1]
Toepper M. Dissociating normal aging from Alzheimer’s disease: a view from cognitive neuroscience. J Alzheimers Dis 57(2): 331-52. (2017)
[2]
Kirshner HS. Primary progressive aphasia and Alzheimer’s disease: brief history, recent evidence. Curr Neurol Neurosci Rep 12(6): 709-14. (2012)
[3]
Dubois B, Feldman HH, Jacova C, Cummings JL, Dekosky ST, Barberger-Gateau P, et al. Revising the definition of Alzheimer's disease: a new lexicon, in Lancet Neurol. 2010, Copyright (c) 2010 Elsevier Ltd. All rights reserved.: England 1118-27.
[4]
Fraser KC, Meltzer JA, Rudzicz F. Linguistic features identify Alzheimer’s disease in narrative speech. J Alzheimers Dis 49(2): 407-22. (2016)
[5]
Faber-Langendoen K, Morris JC, Knesevich JW, LaBarge E, Miller JP, Berg L, et al. Aphasia in senile dementia of the Alzheimer type. Ann Neurol 23(4): 365-70. (1988)
[6]
Weiner MF. Language in Alzheimer’s disease. J Clin Psychiatry 69(8): 1223-7. (2008)
[7]
Forbes-McKay KE, Venneri A. Detecting subtle spontaneous language decline in early Alzheimer’s disease with a picture description task. Neurol Sci 26(4): 243-54. (2005)
[8]
Oulhaj A, Wilcock GK, Smith AD, de Jager CA. Predicting the time of conversion to MCI in the elderly: role of verbal expression and learning. Neurology 73(18): 1436-42. (2009)
[9]
Lemos R, Afonso A, Martins C, Waters JH, Blanco FS, Simões MR, et al. Selective reminding and free and cued selective reminding in mild cognitive impairment and Alzheimer disease. Appl Neuropsychol Adult 23(2): 85-93. (2016)
[10]
Reilly JJ. Troche, Grossman, M. Language processing in dementia. The handbook of Alzheimer’s disease and other dementias, (2011); pp. p. 336-368.
[11]
Goedert M. NEURODEGENERATION. Alzheimer’s and Parkinson’s diseases: the prion concept in relation to assembled Abeta, tau, and alpha-synuclein. Science 349(6248)1255555 (2015)
[12]
Hane FT, Lee BY, Leonenko Z. Recent progress in Alzheimer’s disease research, Part 1: Pathology. J Alzheimers Dis 57(1): 1-28. (2017)
[13]
Taler V, Phillips NA. Language performance in Alzheimer’s disease and mild cognitive impairment: a comparative review. J Clin Exp Neuropsychol 30(5): 501-56. (2008)
[14]
Adlam A-LR, Bozeat S, Arnold R, Watson P, Hodges JR. Semantic knowledge in mild cognitive impairment and mild Alzheimer’s disease. Cortex 42(5): 675-84. (2006)
[15]
Salmon DP, Butters N, Chan AS. The deterioration of semantic memory in Alzheimer’s disease. Can J Exp Psychol 53(1): 108. (1999)
[16]
Marini A, Boewe A, Caltagirone C, Carlomagno S. Age-related differences in the production of textual descriptions. J Psycholinguist Res 34(5): 439-63. (2005)
[17]
Kavé G, Levy Y. Morphology in picture descriptions provided by persons with Alzheimer’s disease. J Speech Lang Hear Res 46(2): 341-52. (2003)
[18]
Nicholas M, Obler LK, Albert ML, Helm-Estabrooks N. Empty speech in Alzheimer’s disease and fluent aphasia. J Speech Hear Res 28(3): 405-10. (1985)
[19]
Marini A, Martelli S, Gagliardi C, Fabbro F. Narrative language in Williams Syndrome and its neuropsychological correlates. J Neurolinguist 23(2): 97-11. (2010)
[20]
Marini A, Andreetta S, del Tin S. Carlomagno Sergio. A multi-level approach to the analysis of narrative language in aphasia. Aphasiology 25(11): 1372-92. (2011)
[21]
Marini A, Galetto V, Zampieri E, Vorano L, Zettin M, Carlomagno S. Narrative language in traumatic brain injury. Neuropsychologia 49(10): 2904-10. (2011)
[22]
Carlomagno S, Santoro A, Menditti A, Pandolfi M, Marini A. Referential communication in Alzheimer’s type dementia. Cortex 41(4): 520-34. (2005)
[23]
Boschi V, Catricalà E, Consonni M, Chesi C, Moro A, Cappa SF. Connected speech in neurodegenerative language disorders: a review. Front Psychol 8: 269. (2017)
[24]
Drummond C, Coutinho G, Fonseca RP, Assunção N, Teldeschi A, de Oliveira-Souza R, et al. Deficits in narrative discourse elicited by visual stimuli are already present in patients with mild cognitive impairment. Front Aging Neurosci 7: 96. (2015)
[25]
Ahmed S, Haigh AM, de Jager CA, Garrard P. Connected speech as a marker of disease progression in autopsy-proven Alzheimer’s disease. Brain 136(Pt 12): 3727-37. (2013)
[26]
Cuetos F, Arango-Lasprilla JC, Uribe C, Valencia C, Lopera F. Linguistic changes in verbal expression: a preclinical marker of Alzheimer’s disease. J Int Neuropsychol Soc 13(3): 433-9. (2007)
[27]
Spalletta G, Spoletini I, Cherubini A, Rubino IA, Siracusano A, Piras F, et al. Cortico-subcortical underpinnings of narrative processing impairment in schizophrenia. Psychiatry Res 182(1): 77-80. (2010)
[28]
Blank SC, Scott SK, Murphy K, Warburton E, Wise RJ. Speech production: wernicke, Broca and beyond. Brain 125(Pt 8): 1829-38. (2002)
[29]
Blank SC, Bird H, Turkheimer F, Wise RJ. Speech production after stroke: the role of the right pars opercularis. Ann Neurol 54(3): 310-20. (2003)
[30]
Marini A, Urgesi C. Please get to the point! A cortical correlate of linguistic informativeness. J Cogn Neurosci 24(11): 2211-22. (2012)
[31]
Vigneau M, Beaucousin V, Hervé PY, Duffau H, Crivello F, Houdé O, et al. Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. Neuroimage 30(4): 1414-32. (2006)
[32]
Wagner AD, Paré-Blagoev EJ, Clark J, Poldrack RA. Recovering meaning: left prefrontal cortex guides controlled semantic retrieval. Neuron 31(2): 329-38. (2001)
[33]
Whitney C, Kirk M, O’Sullivan J, Lambon Ralph MA, Jefferies E. The neural organization of semantic control: TMS evidence for a distributed network in left inferior frontal and posterior middle temporal gyrus. Cereb Cortex 21(5): 1066-75. (2011)
[34]
Whitney C, Kirk M, O’Sullivan J, Lambon Ralph MA, Jefferies E. Executive semantic processing is underpinned by a large-scale neural network: revealing the contribution of left prefrontal, posterior temporal, and parietal cortex to controlled retrieval and selection using TMS. J Cogn Neurosci 24(1): 133-47. (2012)
[35]
Badre D, Poldrack RA, Paré-Blagoev EJ, Insler RZ, Wagner AD. Dissociable controlled retrieval and generalized selection mechanisms in ventrolateral prefrontal cortex. Neuron 47(6): 907-18. (2005)
[36]
Badre D, Wagner AD. Left ventrolateral prefrontal cortex and the cognitive control of memory. Neuropsychologia 45(13): 2883-901. (2007)
[37]
Mueller KD, Koscik RL, Turkstra LS, Riedeman SK, LaRue A, Clark LR, et al. Connected language in late middle-aged adults at risk for Alzheimer’s disease. J Alzheimers Dis 54(4): 1539-50. (2016)
[38]
Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12(3): 189-98. (1975)
[39]
Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, et al. The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53(4): 695-9. (2005)
[40]
Petersen RC. Mild cognitive impairment as a diagnostic entity. J Intern Med 256(3): 183-94. (2004)
[41]
Petersen RC, Caracciolo B, Brayne C, Gauthier S, Jelic V, Fratiglioni L. Mild cognitive impairment: a concept in evolution. J Intern Med 275(3): 214-28. (2014)
[42]
Matthews FE. Two Year Progression from mild cognitive impairment to dementia: to what extent do different definitions agree? J Am Geriatr Soc 56(8): 1424-33. (2008)
[43]
Morris JC. The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology 43(11): 2412-4. (1993)
[44]
Hamilton M. A rating scale for depression. J Neurol Neurosurg Psychiatry 23: 56-62. (1960)
[45]
McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR Jr, Kawas CH, et al. 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. Alzheimers Dement 7(3): 263-9. (2011)
[46]
Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, et al. The diagnosis of mild cognitive impairment due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 7(3): 270-9. (2011)
[47]
Dubois B, Dubois B, Feldman HH, Jacova C, Hampel H, Molinuevo JL, et al. Advancing research diagnostic criteria for Alzheimer’s disease: the IWG-2 criteria. Lancet Neurol 13(6): 614-29. (2014)
[48]
Blennow K, Hampel H, Weiner M, Zetterberg H. Cerebrospinal fluid and plasma biomarkers in Alzheimer disease. Nat Rev Neurol 6(3): 131-44. (2010)
[49]
Mulder C, Verwey NA, van der Flier WM, Bouwman FH, Kok A, van Elk EJ, et al. Amyloid-beta(1-42), total tau, and phosphorylated tau as cerebrospinal fluid biomarkers for the diagnosis of Alzheimer disease. Clin Chem 56(2): 248-53. (2010)
[50]
van Harten AC, Visser PJ, Pijnenburg YA, Teunissen CE, Blankenstein MA, Scheltens P, et al. Cerebrospinal fluid Abeta42 is the best predictor of clinical progression in patients with subjective complaints. Alzheimers Dement 9(5): 481-7. (2013)
[51]
Hansson O, Zetterberg H, Buchhave P, Londos E, Blennow K, Minthon L. Association between CSF biomarkers and incipient Alzheimer’s disease in patients with mild cognitive impairment: a follow-up study. Lancet Neurol 5(3): 228-34. (2006)
[52]
Duits FH, Teunissen CE, Bouwman FH, Visser PJ, Mattsson N, Zetterberg H, et al. The cerebrospinal fluid “Alzheimer profile”: easily said, but what does it mean? Alzheimers Dement 10(6): 713-723.e2. (2014)
[53]
Monaco M, Costa A, Caltagirone C, Carlesimo GA. Forward and backward span for verbal and visuo-spatial data: standardization and normative data from an Italian adult population. Neurol Sci 34(5): 749-54. (2013)
[54]
Mauri M. Standardizzazione di due nuovi test di memoria: apprendimento di liste di parole correlate e non correlate semanticamente. Arch Psicol Neurol Psichiatr 5-6: 621-45. (1997)
[55]
Spinnler H, Tognoni G. Standardizzazione e taratura italiana di test neuropsicologici 1987 Masson Italia Periodici.
[56]
Caffarra P, Vezzadini G, Dieci F, Zonato F, Venneri A. Rey-Osterrieth complex figure: normative values in an Italian population sample. Neurol Sci 22(6): 443-7. (2002)
[57]
Giovagnoli AR, Del Pesce M, Mascheroni S, Simoncelli M, Laiacona M, Capitani E, et al. Trail making test: normative values from 287 normal adult controls. Ital J Neurol Sci 17(4): 305-9. (1996)
[58]
Brugnolo A, De Carli F, Accardo J, Amore M, Bosia LE, Bruzzaniti C, et al. An updated Italian normative dataset for the Stroop color word test (SCWT). Neurol Sci 37(3): 365-72. (2016)
[59]
Caffarra P, Vezzadini G, Dieci F, Zonato F, Venneri A. Modified card sorting test: normative data. J Clin Exp Neuropsychol 26(2): 246-50. (2004)
[60]
Della Sala S, MacPherson SE, Phillips LH, Sacco L, Spinnler H. How many camels are there in Italy? Cognitive estimates standardised on the Italian population. Neurol Sci 24(1): 10-5. (2003)
[61]
Scarpina F, D’Aniello GE, Mauro A, Castelnuovo G, MacPherson SE. How many segments are there in an orange: normative data for the new Cognitive Estimation Task in an Italian population. Neurol Sci 36(10): 1889-95. (2015)
[62]
Novelli G, Papagno C, Capitani E, Laiacona M. Tre test clinici di memoria verbale a lungo termine: taratura su soggetti normali. / Three clinical tests for the assessment of verbal long-term memory function: norms from 320 normal subjects. Arch Psicol Neurol Psichiatr 47(2): 278-96. (1986)
[63]
Costa A, Bagoj E, Monaco M, Zabberoni S, De Rosa S, Papantonio AM, et al. Standardization and normative data obtained in the Italian population for a new verbal fluency instrument, the phonemic/semantic alternate fluency test. Neurol Sci 35(3): 365-72. (2014)
[64]
Luzzatti C, Willmes K, De Bleser R. Aachener aphasie test: versione italiana. (1996) Organizzazioni Speciali: Firenze
[65]
Catricala E, Della Rosa PA, Ginex V, Mussetti Z, Plebani V, Cappa SF. An Italian battery for the assessment of semantic memory disorders. Neurol Sci 34(6): 985-93. (2013)
[66]
Goodglass H, Kaplan E. The Boston Diagnostic Aphasia Examination. (1972) Philadelphia Lea & Febiger
[67]
Kertesz A. Western aphasia battery test manual. (1982) Psychological Corp.
[68]
Huber W, Gleber J. Linguistic and nonlinguistic processing of narratives in aphasia. Brain Lang 16(1): 1-18. (1982)
[69]
Andreetta S, Marini A. The effect of lexical deficits on narrative disturbances in fluent aphasia. Aphasiology 29(6): 705-23. (2015)
[70]
Matsuda H, Mizumura S, Nagao T, Ota T, Iizuka T, Nemoto K, et al. Automated discrimination between very early Alzheimer disease and controls using an easy Z-score imaging system for multicenter brain perfusion single-photon emission tomography. Am J Neuroradiol 28(4): 731-6. (2007)
[71]
Waragai M, Yamada T, Matsuda H. Evaluation of brain perfusion SPECT using an easy Z-score imaging system (eZIS) as an adjunct to early-diagnosis of neurodegenerative diseases. J Neurol Sci 260(1-2): 57-64. (2007)
[72]
de Lira JO, Ortiz KZ, Campanha AC, Bertolucci PH, Minett TS. Microlinguistic aspects of the oral narrative in patients with Alzheimer’s disease. Int Psychogeriatr 23(03): 404-12. (2011)
[73]
Hoffmann I, Nemeth D, Dye CD, Pákáski M, Irinyi T, Kálmán J. Temporal parameters of spontaneous speech in Alzheimer’s disease. Int J Speech Lang Pathol 12(1): 29-34. (2010)
[74]
Sajjadi SA, Patterson K, Tomek M, Nestor PJ. Abnormalities of connected speech in semantic dementia vs Alzheimer’s disease. Aphasiology 26(6): 847-66. (2012)
[75]
Lai Y-H. Discourse features of chinese-speaking seniors with and without Alzheimer’s disease. Lang Linguis 15(3): 411-34. (2014)
[76]
Cannizzaro MS, Dumas J, Prelock P, Newhouse P. Organizational structure reduces processing load in the prefrontal cortex during discourse processing of written text: implications for high-level reading issues after TBI. Perspect Neurophysiol Neurogenic Speech Lang Disord 22(2): 67-78. (2012)
[77]
Laws KR, Duncan A, Gale TM. ‘Normal’ semantic-phonemic fluency discrepancy in Alzheimer’s disease? A meta-analytic study. Cortex 46(5): 595-601. (2010)
[78]
Hodges JR, Salmon DP, Butters N. Semantic memory impairment in Alzheimer’s disease: failure of access or degraded knowledge? Neuropsychologia 30(4): 301-14. (1992)
[79]
Caselli RJ, Locke DE, Dueck AC, Knopman DS, Woodruff BK, Hoffman-Snyder C, et al. The neuropsychology of normal aging and preclinical Alzheimer's disease. Alzheimers Dement 2014; 10(1): 84-92. (2014)
[80]
Indefrey P, Levelt WJM. The neural correlates of language production. inThe new cognitive neurosciences 2nd ed 2000, MIT press p. 845-65.
[81]
Jefferies E, Ralph L, Matthew A. Semantic impairment in stroke aphasia versus semantic dementia: a case-series comparison. Brain 129(8): 2132-47. (2006)
[82]
Jefferies E, Patterson K, Ralph MA. Deficits of knowledge versus executive control in semantic cognition: insights from cued naming. Neuropsychologia 46(2): 649-58. (2008)
[83]
Novick JM, Kan IP, Trueswell JC, Thompson-Schill SL. A case for conflict across multiple domains: memory and language impairments following damage to ventrolateral prefrontal cortex. Cogn Neuropsychol 26(6): 527-67. (2009)
[84]
Thompson-Schill SL, D’Esposito M, Aguirre GK, Farah MJ. Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. Proc Natl Acad Sci USA 94(26): 14792-7. (1997)
[85]
Hoffman P, Jefferies E, Lambon Ralph MA. Ventrolateral prefrontal cortex plays an executive regulation role in comprehension of abstract words: convergent neuropsychological and repetitive TMS evidence. J Neurosci 30(46): 15450-6. (2010)

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy