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Paragrammatism and agrammatism: a cortical double dissociation revealed by lesion-symptom mapping

William Matchin1*, Alexandra Basilakos1, Brielle C. Stark2, Dirk Den Ouden1*, Julius Fridriksson1 and Greg Hickok3
  • 1 Department of Communication Sciences and Disorders, Arnold School of Public Health, University of South Carolina, United States
  • 2 Department of Speech and Hearing Sciences, College of Arts and Sciences, Indiana University Bloomington, United States
  • 3 Department of Cognitive Sciences, School of Social Sciences, University of California, Irvine, United States

Introduction. The cortical organization of syntax has been difficult to determine, in part because similar syntactic effects in functional neuroimaging studies are elicited in the inferior frontal gyrus (IFG) and the posterior middle temporal gyrus (pMTG). Agrammatic speech is associated with damage to frontal structures including the pars triangularis of the IFG (Wilson et al., 2010; den Ouden et al., 2019). However, unlike the pMTG, damage to the IFG does not reliably impair basic sentence and syntactic comprehension abilities (Dronkers et al., 2004; Wilson & Saygin, 2004; Pillay et al., 2017; Rogalsky et al., 2018). Kleist (1914) originally proposed two kinds of syntactic disturbances in the speech of people with aphasia: agrammatism (simplification of grammatical structure, omission of function words/morphemes), and paragrammatism (error-filled misuse of grammatical elements and structures, leading to “sentence monsters”, e.g. “two women is ugly”, “…wanted to make a trick her”). Matchin & Hickok (in press) suggest that agrammatism results from damage to a morpho-syntactic sequencing system in the pars triangularis and paragrammatism results from damage to a hierarchical syntactic system in the pMTG. Alternatively, it has been suggested that agrammatism and paragrammatism reflect the same underlying grammatical deficit (with presumably the same etiology), modulated by speech fluency (Heeschen & Kolk, 1988; Bates & Goodman, 1997; Dick et al., 2001). However, as the cortical locus of paragrammatism is largely unknown, we performed a voxel-based lesion-symptom mapping (VLSM) study in 53 patients with chronic aphasia secondary to a single-event left hemisphere stroke. Methods. Four expert raters classified subjects’ spoken narrative discourse samples as agrammatic, paragrammatic, or no grammatical deficit, with consensus obtained through discussion. Subjects’ lesion maps were manually drawn and warped to MNI space, and VLSM analyses were performed. Lesion volume was always included as a covariate. Results. Region of interest analyses (Figure 1, right) identified a clear double dissociation: damage to the left pars triangularis of IFG was significantly associated with agrammatism, t(51) = 2.959, p = 0.002, but not paragrammatism, t(51) = -1.542, p = 0.935, while damage to the left pMTG was significantly associated with paragrammatism, t(51) = 3.087, p = 0.002, but not agrammatism, t(51) = -1.429, p = 0.920. Whole brain analyses (Figure 1, left) revealed non-overlapping effects of agrammatism in inferior and middle frontal brain regions and paragrammatism in posterior temporal and parietal brain regions. Secondary analyses adding speech fluency (words per minute) as an additional covariate revealed the same significant double dissociation, albeit weaker, with the same spatial distribution. Discussion. We showed that these qualitatively distinct grammatical deficits, agrammatism and paragrammatism, correspond to inferior frontal and posterior temporal damage (respectively) as proposed by Matchin & Hickok (in press). While both brain regions appear to support syntactic processing, broadly construed, their patterns strongly diverge with respect to grammatical deficits in aphasia, consistent with distinct roles in linear morpho-syntactic processing in IFG and hierarchical lexical-syntactic processing in pMTG. Our results suggest that agrammatism and paragrammatism in fact reflect distinct underlying deficits that cannot be accounted for purely by appeal to speech fluency.

Figure 1
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Acknowledgements

We would like to thank Stephen Wilson for advice during development of this work.

References

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Keywords: agrammatism, Paragrammatism, syntax, lesion-symptom mapping, Speech fluency

Conference: Academy of Aphasia 57th Annual Meeting, Macau, Macao, SAR China, 27 Oct - 29 Oct, 2019.

Presentation Type: Poster presentation

Topic: Not eligible for student award

Citation: Matchin W, Basilakos A, Stark BC, Den Ouden D, Fridriksson J and Hickok G (2019). Paragrammatism and agrammatism: a cortical double dissociation revealed by lesion-symptom mapping. Front. Hum. Neurosci. Conference Abstract: Academy of Aphasia 57th Annual Meeting. doi: 10.3389/conf.fnhum.2019.01.00063

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Received: 06 May 2019; Published Online: 09 Oct 2019.

* Correspondence:
Prof. William Matchin, Department of Communication Sciences and Disorders, Arnold School of Public Health, University of South Carolina, Columbia, South Carolina, 29208, United States, matchin@mailbox.sc.edu
Prof. Dirk Den Ouden, Department of Communication Sciences and Disorders, Arnold School of Public Health, University of South Carolina, Columbia, South Carolina, 29208, United States, OUDEN@mailbox.sc.edu