Neural substrates of phonological and lexicosemantic representations in Alzheimer's disease.

Alzheimer; Language; PET; Articulation Disorders/etiology/physiopathology/radionuclide imaging; Brain Mapping; Cerebral Cortex/pathology/physiopathology/radionuclide imaging; Female; Frontal Lobe/pathology/physiopathology/radionuclide imaging; Humans; Language Disorders/etiology/physiopathology/radionuclide imaging; Language Tests; Male; Middle Aged; Nerve Net/pathology/physiopathology/radionuclide imaging; Phonetics; Positron-Emission Tomography; Predictive Value of Tests; Semantics; Speech/physiology; Speech Perception/physiology; Temporal Lobe/pathology/physiopathology/radionuclide imaging

Abstract :

[en] The language profile of patients suffering from Alzheimer's disease (AD) is characterized not only by lexicosemantic impairments but also by phonological deficits, as shown by an increasing number of neuropsychological studies. This study explored the functional neural correlates underlying phonological and lexicosemantic processing in AD. Using H(215)O PET functional brain imaging, a group of mild to moderate AD patients and a group of age-matched controls were asked to repeat four types of verbal stimuli: words, wordlike nonwords (WL+), non-wordlike nonwords (WL-) and simple vowels. The comparison between the different conditions allowed us to determine brain activation preferentially associated with lexicosemantic or phonological levels of language representations. When repeating words, AD patients showed decreased activity in the left temporo-parietal and inferior frontal regions relative to controls, consistent with distorted lexicosemantic representations. Brain activity was abnormally increased in the right superior temporal area during word repetition, a region more commonly associated with perceptual-phonological processing. During repetition of WL+ and WL- nonwords, AD patients showed decreased activity in the middle part of the superior temporal gyrus, presumably associated with sublexical phonological information; at the same time, AD patients showed larger activation than controls in the inferior temporal gyrus, typically associated with lexicosemantic levels of representation. Overall, the results suggest that AD patients use altered pathways to process phonological and lexicosemantic information, possibly related to a progressive loss of specialization of phonological and lexicosemantic neural networks.

Research Center/Unit :

GIGA CRC (Cyclotron Research Center) In vivo Imaging-Aging & Memory - ULiège
Centre de Neurosciences Cognitives et Comportementales - ULiège

Disciplines :

Neurosciences & behavior

Author, co-author :

Peters, Frederic; Université de Liège - ULiège > Centre de Recherches du Cyclotron

Majerus, Steve ; Université de Liège - ULiège > Département des sciences cognitives > Psychopathologie cognitive

Collette, Fabienne ; Université de Liège - ULiège > Département des sciences cognitives > Neuropsychologie - Département des sciences cognitives

Degueldre, Christian ; Université de Liège - ULiège > Centre de recherches du cyclotron

Del Fiore, Guy; Université de Liège - ULiège > Centre de Recherches du Cyclotron

Laureys, Steven ; Centre Hospitalier Universitaire de Liège - CHU > Neurologie Sart Tilman

Moonen, Gustave ; Centre Hospitalier Universitaire de Liège - CHU > Neurologie Sart Tilman

Salmon, Eric ; Université de Liège - ULiège > Département des sciences cliniques > Neuroimagerie des troubles de la mémoire et révalid. cogn.

Language :

English

Title :

Neural substrates of phonological and lexicosemantic representations in Alzheimer's disease.

Publication date :

2009

Journal title :

Human Brain Mapping

ISSN :

1065-9471

eISSN :

1097-0193

Publisher :

Wiley Liss, Inc., New York, United States - New York

Volume :

Issue :

Pages :

185-99

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

http://www3.interscience.wiley.com/journal/117868149/abstract

Name of the research project :

EC-FP6 project DiMI; IUAP P6/29

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique

Available on ORBi :

since 15 March 2011

Statistics

Number of views

233 (25 by ULiège)

Number of downloads

2 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Belin P, Zatorre RJ, Ahad P (2002): Human temporal-lobe response to vocal sounds. Brain Res Cogn Brain Res 13:17-26.
Binder J (2000): The new neuroanatomy of speech perception. Brain 123(Part 12):2371-2372.
Binder J, Price C (2001): Functional neuroimaging of language. In: Cabeza R, Kingstone A, editors. Handbook of Functional Neuroimaging of Cognition. Cambridge: MIT Press, pp 187-252.
Binder JR, Frost JA, Hammeke TA, Rao SM, Cox RW (1996): Function of the left planum temporale in auditory and linguistic processing. Brain 119(Part 4):1239-1247.
Binder JR, Frost JA, Hammeke TA, Cox RW, Rao SM, Prieto T (1997): Human brain language areas identified by functional magnetic resonance imaging. J Neurosci 17:353-362.
Binder JR, Frost JA, Hammeke TA, Bellgowan PS, Rao SM, Cox RW (1999): Conceptual processing during the conscious resting state. A functional MRI study. J Cogn Neurosci 11:80-95.
Binder JR, Frost JA, Hammeke TA, Bellgowan PS, Springer JA, Kaufman JN, Possing ET (2000): Human temporal lobe activation by speech and nonspeech sounds. Cereb Cortex 10:512-528.
Binder JR, Medler DA, Desai R, Conant LL, Lieberthal E. (2005): Some neurophysiological constraints on models of word naming. Neuroimage 27(3):677-693.
Burton M, Small S, Blumstein S (2000): The role of segmentation in phonological processing: An fMRI investigation. J Cogn Neurosci 12:679-690.
Burton MW, Locasto PC, Krebs-Noble D, Gullapalli RP (2005): A systematic investigation of the functional neuroanatomy of auditory and visual phonological processing. Neuroimage 26: 647-661.
Cabeza R (2002): Hemispheric asymmetry reduction in older adults: The HAROLD model. Psychol Aging 17:85-100.
Croot K, Hodges JR, Xuereb J, Patterson K (2000): Phonological and articulatory impairment in Alzheimer's disease: A case series. Brain Lang 75:277-309.
Damasio H, Kuljis RO, Yuh W, van Hoesen GW, Ehrhardt J (1991): Magnetic resonance imaging of human intracortical structure in vivo. Cereb Cortex 1:374-379.
Damasio H, Grabowski TJ, Tranel D, Hichwa RD, Damasio AR (1996): A neural basis for lexical retrieval. Nature 380:499-505.
Davis MH, Meunier F, Marslen-Wilson WD (2004): Neural responses to morphological, syntactic, and semantic properties of single words: An fMRI study. Brain Lang 89:439-449.
Demonet JF, Chollet F, Ramsay S, Cardebat D, Nespoulous JL, Wise R, Rascol A, Frackowiak R (1992): The anatomy of phonological and semantic processing in normal subjects. Brain 115(Part6):1753-1768.
Demonet JF, Price C, Wise R, Frackowiak RS (1994): Differential activation of right and left posterior sylvian regions by semantic and phonological tasks: A positron-emission tomography study in normal human subjects. Neurosci Lett 182:25-28.
Desgranges B, Baron JC, de la Sayette V, Petit-Taboue MC, Benali K, Landeau B, Lechevalier B, Eustache F (1998): The neural substrates of memory systems impairment in Alzheimer's disease. A PET study of resting brain glucose utilization. Brain 121(Part 4):611-631.
Dräger B, Jansen A, Bruchmann S, Förster AF, Pleger B, Zwitserlood P, Knecht S (2004): How does the brain accommodate to increased task difficulty in word finding? A functional MRI study. Neuroimage 23:1152-1160.
Dronkers NF (1996): A new brain region for coordinating speech articulation. Nature 384:159-161.
Fiebach CJ, Friederici AD, Müller K, von Cramon DY (2002): fMRI evidence for dual routes to the mental lexicon in visual word recognition. J Cogn Neurosci 14:11-23.
Fox RJ, Kasner SE, Chatterjee A, Chalela JA (2000): Aphemia: An isolated disorder of articulation. Clin Neurol Neurosurg 103:123-126.
Friston KJ, Ashburner J, Frith CD, Poline JB, Heather JD, Frackowiak RSJ (1995): Spatial registration and normalisation of images. Hum Brain Mapp 3:165-189.
Frison L, Pocock SJ (1992): Repeated measures in clinical trials: analysis using mean summary statistics and its implications for design. Stat Med 11(13):1685-1704.
Garrard P, Lambon Ralph MA, Watson PC, Powis J, Patterson K, Hodges JR (2001): Longitudinal profiles of semantic impairment for living and nonliving concepts in dementia of Alzheimer's type. J Cogn Neurosci 13:892-909.
Gathercole SE, Frankish CR, Pickering SJ, Peaker S (1999): Phonotactic influences on short-term memory. J Exp Psychol Learn Mem Cogn 25:84-95.
Giffard B, Desgranges B, Nore-Mary F, Lalevee C, Beaunieux H, de la Sayette V, Pasquier F, Eustache F (2002): The dynamic time course of semantic memory impairment in Alzheimer's disease: Clues from hyperpriming and hypopriming effects. Brain 125(Part 9):2044-2057.
Glosser G, Kohn SE, Friedman RB, Sands L, Grugan P (1997): Repetition of single words and nonwords in Alzheimer's disease. Cortex 33:653-666.
Glosser G, Friedman RB, Kohn SE, Sands L, Grugan P (1998): Cognitive mechanisms for processing nonwords: Evidence from Alzheimer's disease. Brain Lang 63:32-49.
Graff-Radford NR, Damasio AR, Hyman BT, Hart MN, Tranel D, Damasio H, Van Hoesen GW, Rezai K (1990): Progressive aphasia in a patient with Pick's disease: A neuropsychological, radiologic, and anatomic study. Neurology 40:620-626.
Grossman M, Payer F, Onishi K, White-Devine T, Morrison D, D'Esposito M, Robinson K, Alavi A (1997): Constraints on the cerebral basis for semantic processing from neuroimaging studies of Alzheimer's disease. J Neurol Neurosurg Psychiatry 63:152-158.
Grossman M, Payer F, Onishi K, D'Esposito M, Morrison D, Sadek A, Alavi A (1998): Language comprehension and regional cerebral defects in frontotemporal degeneration and Alzheimer's disease. Neurology 50:157-163.
Grossman M, Koenig P, Glosser G, DeVita C, Moore P, Rhee J, Detre J, Alsop D, Gee J (2003): Neural basis for semantic memory difficulty in Alzheimer's disease: An fMRI study. Brain 126(Part 2):292-311.
Grossman M, McMillan C, Moore P, Ding L, Glosser G, Work M, Gee J (2004): What's in a name: Voxel-based morphometric analyses of MRI and naming difficulty in Alzheimer's disease, frontotemporal dementia and corticobasal degeneration. Brain 127(Part 3):628-649.
Harasty JA, Halliday GM, Kril JJ, Code C. (1999): Specific temporoparietal gyral atrophy reflects the pattern of language dissolution in Alzheimer's disease. Brain 122(Pt4):675-686.
Harasty JA, Halliday GM, Xuereb J, Croot K, Bennett H, Hodges JR (2001): Cortical degeneration associated with phonologic and semantic language impairments in AD. Neurology 56:944-950.
Hickok G, Poeppel D (2000): Towards a functional neuroanatomy of speech perception. Trends Cogn Sci 4:131-138.
Hirono N, Mori E, Ishii K, Imamura T, Tanimukai S, Kazui H, Hashimoto M, Takatsuki Y, Kitagaki H, Sasaki M (2001): Neuronal substrates for semantic memory: A positron emission tomography study in Alzheimer's disease. Dement Geriatr Cogn Disord 12:15-21.
Holmes AP, Friston KJ (1998): Generalisability, random effects and population inference. Neuroimage 7:754-754.
Howard D, Patterson K, Wise R, Brown WD, Friston K, Weiller C, Frackowiak R (1992): The cortical localization of the lexicons. Positron emission tomography evidence. Brain 115(Part 6): 1769-1782.
Hulme C, Maughan S, Brown GDA (1991): Memory for familiar and unfamiliar words: Evidence for a long term memory contribution to short term memory span. J Mem Lang 30:685-701.
Jacquemot C, Pallier C, LeBihan D, Dehaene S, Dupoux E (2003): Phonological grammar shapes the auditory cortex: A functional magnetic resonance imaging study. J Neurosci 23:9541-9546.
Jancke L, Wustenberg T, Scheieh H, Heinze HJ (2002): Phonetic perception and the temporal cortex. Neuroimage 15:733-746.
Johnsrude IS, Penhune VB, Zatorre RJ (2000): Functional specificity in the right human auditory cortex for perceiving pitch direction. Brain 123:155-163.
Jueptner M, Weiller C (1995): Review: Does measurement of regional cerebral blood flow reflect synaptic activity? Implications for PET and fMRI. Neuroimage 2:148-156.
Just MA, Carpenter PA, Keller TA, Eddy WF, Thulborn KR (1996): Brain activation modulated by sentence comprehension. Science 274:114-116.
Lattner S, Meyer EM, Friederici AD (2005). Voice perception: Sex, pitch, and the right hemisphere. Hum Brain Mapp 24:11-20.
Li SC, Lindenberger U (1999): Cross-level unification: A computational exploration of the link between deterioration of neuro-transmitter systems and dedifferentiation of cognitive abilities in old age. In: Nilsson LG, Markowitsch HJ, editors. Cognitive Neuroscience of Memory. Toronto: Hogrefe and Huber. pp 104-146.
Majerus S, Collette F, Van der Linden M, Peigneux P, Laureys S, Delfiore G, Degueldre C, Luxen A, Salmon E (2002): A PET investigation of lexicality and phonotactic frequency in oral language processing. Cogn Neuropsychol 19:343-360.
Majerus S, Van der Linden M, Mulder L, Meulemans T, Peters F (2004): Verbal short-term memory reflects the sublexical organization of the phonological language network: Evidence from an incidental phonotactic learning paradigm. J Mem Lang 51:297-306.
Majerus S, Van der Linden M, Collette F, Laureys S, Poncelet M, Degueldre C, Delfiore G, Luxen A, Salmon E (2005): Modulation of brain activity during phonological familiarization. Brain Lang 92:320-331.
Mattis S (1973): Dementia Rating Scale. Windsor: NFER-Nelson.
Mazoyer BM, Tzourio N, Frak V, Syrota A, Murayama N, Levrier O, Salamon G, Dehaene S, Cohen L, Mehler J (1993): The cortical representation of speech. J Cogn Neurosci 5:467-479.
McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984): Clinical diagnosis of Alzheimer's disease: Report of the NINCDS-ADRDA Work Group under the auspices of Department of health and human services task force on Alzheimer's Disease. Neurology 34:939-944.
Mummery CJ, Ashburner J, Scott SK, Wise RJ (1999): Functional neuroimaging of speech perception in six normal and two aphasic subjects. J Acoust Soc Am 106:449-457.
New B, Pallier C, Brysbaert M, Ferrand L: Lexique 2: A new French lexical database. Behav Res Method Instrument Comput 36:516-524.
Nicholas M, Obler LK, Albert ML, Helm-Estabrooks N (1985): Empty speech in Alzheimier's disease and fluent aphasia. J Speech Hearing Res 28:405-410.
Okada G, Hickok H (2006): Left posterior auditory-related cortices participate both in speech perception and speech production: Neural overlap revealed by fMRI. Brain Lang 98:112-117.
Perani D, Dehaene S, Grassi F, Cohen L, Cappa SF, Dupoux E, Fazio F, Mehler J (1996): Brain processing of native and foreign languages. Neuroreport 7:2439-2444.
Peters F, Majerus S, Olivier L, Van der Linden M, Salmon E, Collette F (2007): A multi-component exploration of verbal short-term storage deficits in normal aging and Alzheimer's disease. J Clin Exp Neuropsychol 29:405-417.
Petersen SE, Fox PT, Posner MI, Mintun M, Raichle ME (1988): Positron emission tomographic studies of the cortical anatomy of singleword processing. Nature 331:585-589.
Poeppel D, Guillemin A, Thompson J, Fritz J, Bavelier D, Braun AR (2004): Auditory lexical decision, categorical perception, and FM direction discrimination differentially engage left and right auditory cortex. Neuropsychologia 42:183-200.
Poldrack RA, Temple E, Protopapas A, Nagarajan S, Tallal P, Merzenich M, Gabrieli JD (2001): Relations between the neural bases of dynamic auditory processing and phonological processing: Evidence from fMRI. J Cogn Neurosci 13:687-697.
Price CJ, Wise RJ, Warburton EA, Moore CJ, Howard D, Patterson K, Frackowiak RS, Friston KJ (1996): Hearing and saying. The functional neuro-anatomy of auditory word processing. Brain 119(Part 3):919-931.
Price CJ, Winterburn D, Giraud AL, Moore CJ, Noppeney U (2003): Cortical localisation of the visual and auditory word form areas: A reconsideration of the evidence. Brain Lang 86:272-286.
Pugh KR, Shaywitz BA, Shaywitz SE, Constable RT, Skudlarski P, Fulbright RK, Bronen RA, Shankweiler DP, Katz L, Fletcher JM, Gore JC. (1996): Cerebral organization of component processes in reading. Brain 119(Part 4):1221-1238.
Scott SK, Blank CC, Rosen S, Wise RJ (2000): Identification of a pathway for intelligible speech in the left temporal lobe. Brain 123(Part 12):2400-2406.
Sekiguchi T, Koyama S, Kakigi R (2001): The effect of phonological repetition on cortical magnetic responses evoked by visually presented words. J Cogn Neurosci 16:1250-1261.
Semenza C, Zettin M (1989): Evidence from aphasia for the role of proper names as pure referring expressions. Nature 342:678-679.
Simos PG, Breier JI, Fletcher JM, Foorman BR, Castillo EM, Papanicolaou AC (2002): Brain mechanisms for reading words and pseudowords: An integrated approach. Cereb Cortex 12:297-305.
Specht K, Reul J (2003): Functional segregation of the temporal lobes into highly differentiated subsystems for auditory perception: An auditory rapid event-related fMRI-task. Neuroimage 20:1944-1954.
St George M, Kutas M, Martinez A, Sereno MI (1999): Semantic integration in reading: Engagement of the right hemisphere during discourse processing. Brain 122:1317-1325.
Talairach J, Tournoux P (1988): Co-planar Stereotaxic Atlas of the Human Brain. Stuttgart, Germany: Thieme Medical Publishers.
Tanji K, Suzuki K, Yamadori A, Tabuchi M, Endo K, Fujii T, Itoyama Y (2001): Pure anarthria with predominantly sequencing errors in phoneme articulation: A case report. Cortex 37:671-678.
Thioux M, Pesenti M, Costes N, De Volder A, Seron X (2005): Task-independent semantic activation for numbers and animals. Brain Res Cogn Brain Res 24:284-290.
Tubach JP, Boë LJ (1990): Un corpus de transcription phonétique. Constitution et exploitation statistique. Ecoles nationales supérieur des télécommunication.
Uppenkamp S, Johnsrude IS, Norris D, Marslen-Wilson W, Patterson RD (2006): Locating the initial stages of speech-sound processing in human temporal cortex. Neuroimage 31:1284-1296.
Vandenberghe R, Price C, Wise R, Josephs O, Frackowiak RS (1996): Functional anatomy of a common semantic system for words and pictures. Nature 383:254-256.
Vigneau M, Beaucousin V, Herve PY, Duffau H, Crivello F, Houde O, Mazoyer B, Tzourio-Mazoyer N (2006): Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing. Neuroimage 30:1414-1432.
Vitevitch MS, Luce PA (1998): When words compete: Levels of processing in perception of spoken words. Psychol Sci 9:325-329.
Vitevitch MS, Luce PA, Pisoni DB, Auer ET (1999): Phonotactics, neighborhood activation, and lexical access for spoken words. Brain Lang 68:306-311.
Zahn R, Juengling F, Bubrowski P, Jost E, Dykierek P, Talazko J, Huell M (2004): Hemispheric asymmetries of hypometabolism associated with semantic memory impairment in Alzheimer's disease: A study using positron emission tomography with flu-orodeoxyglucose-F18. Psychiatry Res 132:159-172.
Zatorre RJ, Belin P (2001): Spectral and temporal processing in human auditory cortex. Cereb Cortex 11:946-953.