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Electrophysiological signatures of semantic and syntactic processing in Primary Progressive Aphasia: integration and re-analysis processes during auditory sentence comprehension

Elena Barbieri1*, Matthew Walenski1, Chien-Ju Hsu1, Katrin Bovbjerg1, Brianne Dougherty1, Marek-Marsel Mesulam1, 2, 3 and Cynthia K. Thompson1, 2, 3
  • 1 Northwestern University, Communication Sciences and Disorders, United States
  • 2 Northwestern University, Feinberg School of Medicine, United States
  • 3 Northwestern University, Department of Neurology, United States

Introduction Investigations of the electrophysiological correlates of language processing in Primary Progressive Aphasia (PPA) have focused on the N400, an event-related potential (ERP) component associated with semantic processing. Studies report distinct patterns for patients with semantic PPA (PPA-S), who do not exhibit an N400 to semantic violations, and for patients with agrammatic or logopenic PPA (PPA-G, PPA-L), who show normal-like responses (Hurley et al., 2009, 2012). No previous study has investigated syntactic processing in PPA using ERP. Patients with stroke-induced agrammatic aphasia (whose language deficits are similar to those in PPA-G; Thompson et al., 2012) exhibit abnormal P600 effects to subject-verb agreement and to verb argument structure (VAS) violations (Wassenaar et al., 2004, Kielar et al., 2012), suggesting abnormal revision/repair processes to these violations. The present study investigates the electrophysiological correlates of semantic and verb argument structure violations in individuals with PPA, with (PPA-G) and without (non-PPA-G) grammatical impairments. Materials and Methods Two groups of healthy participants (younger: 18-28 years (n=17); older: 45-78 years (n=10)) and a group of PPA patients (age 51-73 years; PPA-G (n=5), non-PPA-G n=8) performed an auditory sentence acceptability judgment task while EEG was recorded from 32 scalp electrodes. The study included two conditions: (a) a semantic condition, with verb-object incongruencies (e.g. *Albert was poking [vs. wearing] sandals in the restaurant), and (b) a verb argument structure (VAS) condition, with violations created by deleting obligatory direct objects of the verb (e.g. *Mary was devouring [vs. eating] in the kitchen). Participants also performed a visual oddball task, as a non-language control task. Results Results from the oddball task indicate that all participant groups, including patients with PPA-G, showed normal-like P300 responses to rare target (vs. frequent non-target) shapes. Similarly, both healthy groups exhibited an N400 (Figure 1) (of similar amplitude in both groups) in the semantic condition, though the effect was later for the older (500-800 ms) than the younger (400-700 ms) participants, and shifted rightwards in younger but leftwards in older participants. The two healthy groups also showed similar bilateral P600 responses (Figure 1) with posterior distribution in the VAS condition. For the PPA participant groups, no N400 was found for either PPA-G or non-PPA-G patients. In addition, the PPA-G showed no significant P600 in VAS violations, whereas non-PPA-G patients exhibited a P600 of similar amplitude as in healthy participants, but with a more anterior and right-shifted distribution. Discussion These findings indicate that semantic integration, as reflected by the N400, may be impaired across PPA subtypes, including patients with PPA-G. In contrast, the P600 response, which reflects processes of syntactic re-analysis, was abnormal only in patients with grammatical impairments (PPA-G), although the P600 scalp distribution was irregular in the non-PPA-G group as well. Given the intact P300 response in the oddball task, the lack of a P600 response in the VAS condition for PPA-G participants reflects a language deficit, rather than a general attenuation of ERP components.

Figure 1
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Acknowledgements

The study was supported by the R01 DC008552 NIH grant to Dr. Cynthia K. Thompson and Dr. Marek-Marsel Mesulam.

References

Hurley, R.S., Paller, K.A., Wieneke, C.A., Weintraub, S., Thompson, K., Federmeier, K., & Mesulam, M-M. (2009). Electrophysiology of object naming in Primary Progressive Aphasia. The Journal of Neuroscience, 29: 15762-15769.

Hurley, R.S., Paller, K.A., Rogalski, E.J., & Mesulam, M-M. (2012). Neural mechanisms of object naming and word comprehension in Primary Progressive Aphasia. The Journal of Neuroscience, 32: 4848-4855.

Thompson, C.K., Cho, S., Hsu, C-J., Wieneke, C., Rademaker, A., Weitner, B.B., Mesulam, M-M, & Weintraub, S. (2012). Dissociations between fluency and agrammatism in Primary Progressive Aphasia. Aphasiology, 26: 20-43.

Wassenaar, M., Brown, C.M., & Hagoort, P. (2004). Verb agreement violations in patients with Broca’s aphasia. Journal of Cognitive Neuroscience, 16: 553-576.

Kielar, A., Meltzer-Asscher, A., & Thompson, C.K. (2012). Electrophysiological responses to argument structure violations in healthy adults and individuals with agrammatic aphasia. Neuropsychologia, 50: 3320-3337.

Keywords: primary progressive aphasia, event-related potentials (ERPs), P600, N400, semantics, syntax

Conference: 54th Annual Academy of Aphasia Meeting, Llandudno, United Kingdom, 16 Oct - 18 Oct, 2016.

Presentation Type: Platform Sessions

Topic: Academy of Aphasia

Citation: Barbieri E, Walenski M, Hsu C, Bovbjerg K, Dougherty B, Mesulam M and Thompson CK (2016). Electrophysiological signatures of semantic and syntactic processing in Primary Progressive Aphasia: integration and re-analysis processes during auditory sentence comprehension. Front. Psychol. Conference Abstract: 54th Annual Academy of Aphasia Meeting. doi: 10.3389/conf.fpsyg.2016.68.00089

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Received: 29 Apr 2016; Published Online: 15 Aug 2016.

* Correspondence: Dr. Elena Barbieri, Northwestern University, Communication Sciences and Disorders, Evanston, ILLINOIS, 60208, United States, elena.barbieri@northwestern.edu