Abstract
Right hemisphere recruitment of areas homotopical to affected left-sided language areas has classically been described in aphasia following stroke or brain tumors. It may also be a clinically significant mechanism in frontotemporal lobar degeneration (FTLD) and Alzheimer’s disease (AD). In a pooled analysis of previous functional magnetic resonance imaging studies of a modified version of the Pyramids and Palm Trees test, we probed the language network in 19 patients with primary progressive aphasia (nine semantic (SV) and ten agrammatic variant; neuropathologically confirmed FTLD in three cases to date), 15 patients with AD (14 clinically probable and one neuropathologically definite AD to date), and 37 healthy controls. The upper and lower bank of the left posterior superior temporal sulcus (STS) was affected in AD and the left anterior temporal pole (ATP) in primary progressive aphasia (PPA; mainly driven by SV). In the right hemisphere, the posterior STS showed an activity increase in both patient groups compared with controls. In AD, this activity increase correlated positively with naming accuracy. Both in AD and in PPA, the connection strength between right STS and right ATP was decreased compared with controls and this correlated with naming and comprehension scores, respectively. Only in PPA did the right anterior temporal pole show an activity increase, which correlated negatively with comprehension. Right-hemispheric recruitment and disconnections within the right temporal lobe may affect the degree of aphasia in cortical neurodegenerative disease.
Similar content being viewed by others
References
Agosta F, Henry RG, Migliaccio R, Neuhaus J, Miller BL, Dronkers NF, Brambati SM, Filippi M, Ogar JM, Wilson SM, Gorno-Tempini ML (2010) Language networks in semantic dementia. Brain 133:286–299
American Psychiatric Association (1994) Diagnostic and statistical manual of mental disorders 4th ed. American Psychiatric Association, Washington
Bastiaanse R, Bosje M, Visch-Brink E (1995) Psycholinguïstische testbatterij voor de taalverwerking van Afasiepatiënten (PALPA). Lawrence Erlbaum Associates, Hove
Blank S, Bird H, Turkheimer F, Wise R (2003) Speech production after stroke: the role of the right pars opercularis. Ann Neurol 54:310–320
Cotelli M, Manenti R, Cappa S, Geroldi C, Zanetti O, Rossini P, Miniussi C (2006) Effects of transcranial magnetic stimulation on action naming in patients with Alzheimer’s disease. Arch Neurol 63:1523–1524
Crinion J, Price CJ (2005) Right anterior superior temporal activation predicts auditory sentence comprehension following aphasic stroke. Brain 128:2858–2871
Dressel K, Huber W, Frings L, Kümmerer D, Saur D, Mader I, Hüll M, Weiller C, Abel S (2010) Model-oriented naming therapy in semantic dementia: a single case fMRI study. Aphasiology 12:1537–1558
Fletcher P, Happe F, Frith U, Baker S, Dolan R, Frackowiak R, Frith C (1995) Other minds in the brain: a functional imaging study of “theory of mind” in story comprehension. Cognition 57:109–128
Gorno-Tempini M, Dronkers N, Rankin K, Ogar J, Phengrasamy L, Rosen H, Johnson J, Weinner M, Miller B (2004) Cognition and anatomy in three variants of primary progressive aphasia. Ann Neurol 55:335–346
Gorno-Tempini ML, Hillis AE, Weintraub S, Kertesz A, Mendez M, Cappa SF, Ogar JM, Rohrer JD, Black S, Boeve BF, Manes F, Dronkers NF, Vandenberghe R, Rascovsky K, Patterson K, Miller BL, Knopman DS, Hodges JR, Mesulam MM, Grossman M (2011) Classification of primary progressive aphasia and its variants. Neurology 76:1006–1014
Graets P, DeBleser R, Willmes K (1992) Akense afasie test. Swets and Zeitlinger, Lisse
Griswold M, Jakob P, Heidemann R, Nittka M, Jellus V, Wang J, Kiefer B, Haase A (2002) Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med 47:1202–1210
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 126:292–311
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 127:628–649
Hodges J, Patterson K, Oxbury S, Funnell E (1992) Semantic dementia: progressive fluent aphasia with temporal lobe atrophy. Brain 115:1783–1806
Kaplan E, Goodglass H, Weintraub S (1983) The Boston naming test. Lea and Febiger, Philadelphia
Kay J, Lesser R, Coltheart M (1992) Psycholinguistic assessment of language processing in aphasia. Lawrence Erlbaum Associates, Hove
Marien P, Mampaey E, Vervaet A, Saerens J, De Deyn PP (1998) Normative data for the Boston Naming test in native Dutch-speaking Belgian elderly. Brain Lang 65:447–467
McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan E (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 34:939–994
Mesulam M (1999) Neuroplasticity failure in Alzheimer’s disease: bridging the gap between plaques and tangles. Neuron 24:521–529
Mesulam M (2001) Primary progressive aphasia. Ann Neurol 49:425–432
Mesulam M, Grossman M, Hillis A, Kertesz A, Weintraub S (2003) The core and halo of primary progressive aphasia and semantic dementia. Ann Neurol 54S5:S11–S14
Mummery C, Patterson K, Wise R, Vandenberghe R, Price C, Hodges J (1999) Disrupted temporal lobe connections in semantic dementia. Brain 122:61–73
Musso M, Weiller C, Kiebel S, Müller S, Bülau P, Rijntjens M (1999) Training-induced brain plasticity in aphasia. Brain 122:1781–1790
Nelissen N, Pazzaglia M, Vandenbulcke M, Sunaert S, Fannes K, Dupont P, Aglioti S, Vandenberghe R (2010) Gesture discrimination in primary progressive aphasia: the intersection between gesture and language processing pathways. J Neurosci 30:6334–6341
Nelissen N, Vandenbulcke M, Fannes K, Verbruggen A, Peeters R, Dupont P, Laere KV, Bormans G, Vandenberghe R (2007) Aβ amyloid deposition in the language system and how the brain responds. Brain 130:2055–2069
Peters F, Majerus S, Collette F, Degueldre C, Fiore GD, Laureys S, Moonen G, Salmon E (2009) Neural substrates of phonological and lexicosemantic representations in alzheimer’s disease. Hum Brain Mapp 30:185–199
Poline J, Worsley K, Evans A, Friston K (1997) Combining spatial extent and peak intensity to test for activations in functional imaging. NeuroImage 5:83–96
Rolls E (1996) A theory of hippocampal function in memory. Hippocampus 6:601–620
Snodgrass J, Vanderwart M (1980) A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity and visual complexity. J Exp Psychol Hum Learn Mem 6:174–215
Sonty S, Mesulam M, Thompson C, Johnson N, Weintraub S, Parrish T, Gitelman D (2003) Primary progressive aphasia: PPA and the language network. Ann Neurol 53:35–49
Sonty S, Mesulam M, Weintraub S, Johnson N, Parrish T, Gitelman D (2007) Altered effective connectivity within the language network in primary progressive aphasia. J Neurosci 27:1334–1345
Thiel A, Habedank B, Winhuisen L, Herholz K, Kessler J, Haupt W, Heiss W (2005) Essential language function of the right hemisphere in brain tumor patients. Ann Neurol 57:128–131
Thiel A, Herholz K, Koyuncu A, Ghaemi M, Kracht L, Habedank B, Heiss W (2001) Plasticity of language networks in patients with brain tumors: a positron emission tomography study. Ann Neurol 50:620–629
Thulborn K, Carpenter P, Just M (1999) Plasticity of language-related brain function during recovery from stroke. Stroke 30:749–754
Vandenberghe R, Price C, Wise R, Josephs O, Frackowiak R (1996) Functional anatomy of a common semantic system for words and pictures. Nature 383:254–256
Vandenberghe R, Nobre A, Price C (2002) The response of left temporal cortex to sentences. J Cogn Neurosci 14:550–560
Vandenbulcke M, Peeters R, Hecke PV, Vandenberghe R (2005) Anterior temporal laterality in primary progressive aphasia shifts to the right. Ann Neurol 58:362–370
Vandenbulcke M, Peeters R, Fannes K, Vandenberghe R (2006) Knowledge of visual attributes in the right hemisphere. Nat Neurosci 9:964–970
Vandenbulcke M, Peeters R, Dupont P, Van Hecke P, Vandenberghe R (2007) Word reading and posterior temporal dysfunction in amnestic mild cognitive impairment. Cereb Cortex 17:542–551
Warren JE, Crinion JT, Ralph MAL, Wise RJS (2009) Anterior temporal lobe connectivity correlates with functional outcome after aphasic stroke. Brain 132:3428–3442
Weiller C, Isensee C, Rijntjes M, Huber W, Muller S, Bier D, Dutschka K, Woods R, Noth J, Diener H (1995) Recovery from Wernicke’s aphasia: a positron emission tomography study. Ann Neurol 37:723–732
Wilson SM, Dronkers NF, Ogar JM, Jang J, Growdon ME, Agosta F, Henry ML, Miller BL, Gorno-Tempini ML (2010) Neural correlates of syntactic processing in the nonfluent variant of primary progressive aphasia. J Neurosci 30:16845–16854
Woodard JL, Seidenberg M, Nielson KA, Antuono P, Guidotti L, Durgerian S, Zhang Q, Lancaster M, Hantke N, Butts A, Rao SM (2009) Semantic memory activation in amnestic mild cognitive impairment. Brain 132:2068–2078
Acknowledgements
This work was supported by Research Foundation Flanders (FWO) (G.0076.02, G0668.07 to R.V.), K.U.Leuven (OT/04/41, OT/08/056, EF/05/014 to R.V.), and Federaal Wetenschapsbeleid belspo (IUAP P6/29). R.V. is a senior clinical investigator of the FWO and N.N. a postdoctoral fellow of the FWO.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Nelissen, N., Dupont, P., Vandenbulcke, M. et al. Right Hemisphere Recruitment During Language Processing in Frontotemporal Lobar Degeneration and Alzheimer’s Disease. J Mol Neurosci 45, 637–647 (2011). https://doi.org/10.1007/s12031-011-9603-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12031-011-9603-6