Distinguishing Among Variants of Primary Progressive Aphasia with a Brief Multimodal Test of Nouns and Verbs
Abstract
1. Introduction
1.1. Verb Naming
1.2. Noun Naming
1.3. Verbal and Written Modalities
2. Materials and Methods
2.1. Procedures
2.2. Participants
2.3. Experimental Test
2.4. Statistical Analysis
3. Results
3.1. Analysis of Performance by Variant
3.2. Analysis of Performance Within Individuals
4. Discussion
4.1. Limitations
4.2. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Mesulam, M.M. Slowly Progressive Aphasia without Generalized Dementia. Ann. Neurol. 1982, 11, 592–598. [Google Scholar] [CrossRef] [PubMed]
- Léger, G.C.; Johnson, N. A Review on Primary Progressive Aphasia. Neuropsychiatr. Dis. Treat. 2007, 3, 745–752. [Google Scholar] [CrossRef] [PubMed]
- Gorno-Tempini, M.L.; Hillis, A.E.; Weintraub, S.; Kertesz, A.; Mendez, M.; Cappa, S.F.; Ogar, J.M.; Rohrer, J.D.; Black, S.; Boeve, B.F. Classification of Primary Progressive Aphasia and Its Variants. Neurology 2011, 76, 1006–1014. [Google Scholar] [CrossRef]
- Mesulam, M. Primary Progressive Aphasia. Ann. Neurol. 2001, 49, 425–432. [Google Scholar] [CrossRef]
- Damasio, H.; Grabowski, T.; Tranel, D. A Neural Basis for Lexical Retrieval. Nature 1996, 380, 499–505. [Google Scholar] [CrossRef]
- Silveri, M.C.; Pravatà, E.; Brita, A.C. Primary Progressive Aphasia: Linguistic Patterns and Clinical Variants. Brain Lang. 2014, 135, 57–65. [Google Scholar] [CrossRef]
- Hunston, S.; Herbst, T.; Schmid, H.J.; Faulhaber, S. Pattern Grammar in Context. In Constructions, Collocations, Patterns; De Gruyter Mouton: Berlin, Germany, 2014; pp. 99–119. [Google Scholar]
- Themistocleous, C.; Webster, K.; Afthinos, A.; Tsapkini, K. Part of Speech Production in Patients with Primary Progressive Aphasia: An Analysis Based on Natural Language Processing. Am. J. Speech Lang. Pathol. 2021, 30, 466–480. [Google Scholar] [CrossRef]
- Munro, P.; Siyambalapitiya, S. Improved Word Comprehension in Global Aphasia Using a Modified Semantic Feature Analysis Treatment. Clin. Linguist. Phon. 2017, 31, 119–136. [Google Scholar] [CrossRef]
- Hillis, A.E.; Oh, S.; Ken, L. Deterioration of Naming Nouns versus Verbs in Primary Progressive Aphasia. Ann. Neurol. 2004, 55, 268–275. [Google Scholar] [CrossRef] [PubMed]
- Ikejiri, Y.; Tanabe, H.; Nakagawa, Y.; Kashiwagi, A.; Okuda, J.; Shirashi, J.; Nishimura, T. Two Cases of Primary Progressive Non-Fluent Aphasia. Brain Nerve 1993, 45, 370–376. [Google Scholar]
- Wilson, S.M.; Henry, M.L.; Besbris, M.; Ogar, J.M.; Dronkers, N.F.; Jarrold, W.; Miller, B.L.; Gorno-Tempini, M.L. Connected Speech Production in Three Variants of Primary Progressive Aphasia. Brain 2010, 133, 2069–2088. [Google Scholar] [CrossRef]
- Plaut, D.C.; Shallice, T. Perseverative and Semantic Influences on Visual Object Naming Errors in Optic Aphasia: A Connectionist Account. J. Cogn. Neurosci. 1993, 5, 89–117. [Google Scholar] [CrossRef]
- Dell, G.S.; Schwartz, M.F.; Martin, N.; Saffran, E.M.; Gagnon, D.A. Lexical Access in Aphasic and Nonaphasic Speakers. Psychol. Rev. 1997, 104, 801–838. [Google Scholar] [CrossRef]
- Rapp, B.; Goldrick, M. Speaking words: Contributions of cognitive neuropsychological research. Cogn. Neuropsychol. 2006, 23, 39–73. [Google Scholar] [CrossRef] [PubMed]
- Lorca-Puls, D.L.; Gajardo-Vidal, A.; Mandelli, M.L. Neural Basis of Speech and Grammar Symptoms in Non-Fluent Variant Primary Progressive Aphasia Spectrum. Brain 2024, 147, 607–626. [Google Scholar] [CrossRef] [PubMed]
- Zingeser, L.B.; Berndt, R.S. Retrieval of Nouns and Verbs in Agrammatism and Anomia. Brain Lang. 1990, 39, 14–32. [Google Scholar] [CrossRef]
- McCarthy, R.; Warrington, E.K. Category Specificity in an Agrammatic Patient: The Relative Impairment of Verb Retrieval and Comprehension. Neuropsychologia 1985, 23, 709–727. [Google Scholar] [CrossRef] [PubMed]
- Miceli, G.; Silveri, M.C.; Villa, G.; Caramazza, A. On the Basis for the Agrammatic’s Difficulty in Producing Main Verbs. Cortex 1984, 20, 207–220. [Google Scholar] [CrossRef]
- Thompson, C.K.; Mack, J.E. Grammatical Impairments in PPA. Aphasiology 2014, 28, 1018–1037. [Google Scholar] [CrossRef]
- Deleon, J.; Gesierich, B.; Besbris, M. Elicitation of Specific Syntactic Structures in Primary Progressive Aphasia. Brain Lang. 2012, 123, 183–190. [Google Scholar] [CrossRef]
- Marcotte, K.; Graham, N.L.; Black, S.E. Verb Production in the Nonfluent and Semantic Variants of Primary Progressive Aphasia: The Influence of Lexical and Semantic Factors. Cogn. Neuropsychol. 2014, 31, 565–583. [Google Scholar] [CrossRef] [PubMed]
- Faroqi-Shah, Y.; Thompson, C.K. Verb Inflections in Agrammatic Aphasia: Encoding of Tense Features. J. Mem. Lang. 2007, 56, 129–151. [Google Scholar] [CrossRef]
- Cupit, J.; Leonard, C.; Graham, N.L. Analysing Syntactic Productions in Semantic Variant PPA and Non-Fluent Variant PPA: How Different Are They? Aphasiology 2017, 31, 282–307. [Google Scholar] [CrossRef]
- Mummery, C.J.; Patterson, K.; Price, C.J.; Ashburner, J.; Frackowiak, R.S.J.; Hodges, J.R. A Voxel-Based Morphometry Study of Semantic Dementia: Relationship between Temporal Lobe Atrophy and Semantic Memory. Ann. Neurol. 2000, 47, 36–45. [Google Scholar] [CrossRef]
- Migliaccio, R.; Boutet, C.; Valabregue, R.; Ferrieux, S.; Nogues, M. The Brain Network of Naming: A Lesson from Primary Progressive Aphasia. PLoS ONE 2016, 11, e0148707. [Google Scholar] [CrossRef]
- Mesulam, M.; Rogalski, E.; Wieneke, C. Neurology of Anomia in the Semantic Variant of Primary Progressive Aphasia. Brain 2009, 132, 2553–2565. [Google Scholar] [CrossRef]
- Race, D.S.; Tsapkini, K.; Crinion, J. An Area Essential for Linking Word Meanings to Word Forms: Evidence from Primary Progressive Aphasia. Brain Lang. 2013, 127, 167–176. [Google Scholar] [CrossRef] [PubMed]
- Gorno-Tempini, M.L.; Brambati, S.M.; Ginex, V. The Logopenic/Phonological Variant of Primary Progressive Aphasia. Neurology 2008, 71, 1227–1234. [Google Scholar] [CrossRef] [PubMed]
- Migliaccio, R.; Agosta, F.; Rascovsky, K. Clinical Syndromes Associated with Posterior Atrophy. Neurology 2009, 73, 1571–1578. [Google Scholar] [CrossRef]
- Lukic, S.; Borghesani, V.; Weis, E. Dissociating Nouns and Verbs in Temporal and Perisylvian Networks: Evidence from Neurodegenerative Diseases. Cortex 2021, 142, 47–61. [Google Scholar] [CrossRef]
- Thompson, C.K.; Lukic, S.; King, M.C.; Mesulam, M.M.; Weintraub, S. Verb and Noun Deficits in Strokeinduced and Primary Progressive Aphasia: The Northwestern Naming Battery. Aphasiology 2012, 26, 632–655. [Google Scholar] [CrossRef] [PubMed]
- Damasio, A.R.; Tranel, D. Nouns and Verbs Are Retrieved with Differently Distributed Neural Systems. Proc. Natl. Acad. Sci. USA 1993, 90, 4957–4960. [Google Scholar] [CrossRef]
- Pagnoni, I.; Gobbi, E.; Premi, E. Language Training for Oral and Written Naming Impairment in Primary Progressive Aphasia: A Review. Transl. Neurodegener. 2021, 10, 24. [Google Scholar] [CrossRef]
- Hillis, A.E.; Tuffiash, E.; Caramazza, A. Modality-Specific Deterioration in Naming Verbs in Nonfluent Primary Progressive Aphasia. J. Cogn. Neurosci. 2002, 14, 1099–1108. [Google Scholar] [CrossRef]
- Hillis, A.E.; Heidlergary, J.; Newhart, M.; Chang, S.; Ken, L.; Bak, T.H. Naming and Comprehension in Primary Progressive Aphasia: The Influence of Grammatical Word Class. Aphasiology 2006, 20, 246–256. [Google Scholar] [CrossRef]
- Leys, C.; Schumann, S. A nonparametric method to analyze interactions: The adjusted rank transform test. J. Exp. Soc. Psychol. 2010, 46, 684–688. [Google Scholar] [CrossRef]
- Sonty, S.P.; Mesulam, M.M.; Thompson, C.K.; Johnson, N.A.; Weintraub, S.; Parrish, T.B.; Gitelman, D.R. Primary Progressive Aphasia: PPA and the Language Network. Ann. Neurol. 2003, 53, 35–49. [Google Scholar] [CrossRef]
- Croisile, B.; Ska, B.; Brabant, M. Comparative Study of Oral and Written Picture Description in Patients with Alzheimer’s Disease. Brain Lang. 1996, 53, 1–19. [Google Scholar] [CrossRef] [PubMed]
- Groves-Wright, K.; Neils-Strunjas, J.; Burnett, R.; O’neill, M.J. A Comparison of Verbal and Written Language in Alzheimer’s Disease. J. Commun. Disord. 2004, 37, 109–130. [Google Scholar] [CrossRef] [PubMed]
- Druks, J.; Masterson, J.; Kopelman, M.; Clare, L.; Rose, A.; Rai, G. Is Action Naming Better Preserved (than Object Naming) in Alzheimer’s Disease and Why Should We Ask? Brain Lang. 2006, 98, 332–340. [Google Scholar] [CrossRef]
- Kemmerer, D. Word Classes in the Brain: Implications of Linguistic Typology for Cognitive Neuroscience. Cortex 2014, 58, 27–51. [Google Scholar] [CrossRef] [PubMed]
- Vigliocco, G.; Vinson, D.P.; Druks, J.; Barber, H.; Cappa, S.F. Nouns and Verbs in the Brain: A Review of Behavioural, Electrophysiological, Neuropsychological and Imaging Studies. Neurosci. Biobehav. Rev. 2011, 35, 407–426. [Google Scholar] [CrossRef]
- De Simone, F.; Collina, S. The Picture–Word Interference Paradigm: Grammatical Class Effects in Lexical Production. J. Psycholinguist. Res. 2016, 45, 1003–1019. [Google Scholar] [CrossRef]
- Sepelyak, K.; Crinion, J.; Molitoris, J.; Epstein-Peterson, Z.; Bann, M.; Davis, C.; Newhart, M.; Heidler-Gary, J.; Tsapkini, K.; Hillis, A.E. Patterns of Breakdown in Spelling in Primary Progressive Aphasia. Cortex 2011, 47, 342–352. [Google Scholar] [CrossRef] [PubMed]
- Webster, J.; Whitworth, A. Treating Verbs in Aphasia: Exploring the Impact of Therapy at the Single Word and Sentence Levels. Int. J. Lang. Commun. Disord. 2012, 47, 619–636. [Google Scholar] [CrossRef]
- Edmonds, L.A.; Mammino, K.; Ojeda, J. Effect of Verb Network Strengthening Treatment (VNeST) in Persons with Aphasia: Extension and Replication of Previous Findings. Am. J. Speech Lang. Pathol. 2014, 23, S312–S329. [Google Scholar] [CrossRef]
- Taylor-Rubin, C.; Nickels, L.; Croot, K. Exploring the Effects of Verb and Noun Treatment on Verb Phrase Production in Primary Progressive Aphasia: A Series of Single Case Experimental Design Studies. Neuropsychol. Rehabil. 2022, 32, 1121–1163. [Google Scholar] [CrossRef]
- Raymer, A.M.; Ciampitti, M.; Holliway, B.; Singletary, F.; Blonder, L.X.; Ketterson, T.; Anderson, S.; Lehnen, J.; Heilman, K.M.; Rothi, L.J.G. Semantic-Phonologic Treatment for Noun and Verb Retrieval Impairments in Aphasia. Neuropsychol. Rehabil. 2007, 17, 244–270. [Google Scholar] [CrossRef]
- Papanikolaou, K.; Nasios, G.; Nousia, A.; Siokas, V.; Messinis, L.; Dardiotis, E. Noninvasive Brain Stimulation in Primary Progressive Aphasia: A Literature Review. Adv. Exp. Med. Biol. 2023, 1425, 567–574. [Google Scholar] [PubMed]
- Rapp, B.; Glucroft, B. The Benefits and Protective Effects of Behavioural Treatment for Dysgraphia in a Case of Primary Progressive Aphasia. Aphasiology 2009, 23, 236–265. [Google Scholar] [CrossRef]
Criterion | Count |
---|---|
Previous history of stroke | 16 |
Speech impediment, apraxia of speech, or dysarthria that interfered with intelligibility | 6 |
Previous history of learning disabilities | 2 |
Diagnosis did not include PPA | 18 |
PPA too progressed for task | 2 |
PPA identified but deemed unclassifiable into three classic variants | 44 |
Evaluation data were missing | 1 |
Records excluded | 89 |
Semantic | Non-Fluent | Logopenic | |
---|---|---|---|
Count | 82 | 67 | 151 |
Age * | 67 (8) | 70 (9) | 71 (8) |
Sex (Female:Male) | 51:31 | 30:37 | 89:62 |
Education (N = 141) | 16 (2) | 16 (3) | 16 (3) |
Handedness (Right:Left; N = 168) | 42:4 | 41:6 | 70:5 |
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Lambert, M.A.; Stockbridge, M.D.; Kelly, L.; Diaz-Carr, I.; Neal, V.; Hillis, A.E. Distinguishing Among Variants of Primary Progressive Aphasia with a Brief Multimodal Test of Nouns and Verbs. Brain Sci. 2025, 15, 1108. https://doi.org/10.3390/brainsci15101108
Lambert MA, Stockbridge MD, Kelly L, Diaz-Carr I, Neal V, Hillis AE. Distinguishing Among Variants of Primary Progressive Aphasia with a Brief Multimodal Test of Nouns and Verbs. Brain Sciences. 2025; 15(10):1108. https://doi.org/10.3390/brainsci15101108
Chicago/Turabian StyleLambert, Marco A., Melissa D. Stockbridge, Lindsey Kelly, Isidora Diaz-Carr, Voss Neal, and Argye E. Hillis. 2025. "Distinguishing Among Variants of Primary Progressive Aphasia with a Brief Multimodal Test of Nouns and Verbs" Brain Sciences 15, no. 10: 1108. https://doi.org/10.3390/brainsci15101108
APA StyleLambert, M. A., Stockbridge, M. D., Kelly, L., Diaz-Carr, I., Neal, V., & Hillis, A. E. (2025). Distinguishing Among Variants of Primary Progressive Aphasia with a Brief Multimodal Test of Nouns and Verbs. Brain Sciences, 15(10), 1108. https://doi.org/10.3390/brainsci15101108