Neural Connectivity in Syntactic Movement Processing

Eduardo Europa, Darren R Gitelman, Swathi Kiran, Cynthia K Thompson, Eduardo Europa, Darren R Gitelman, Swathi Kiran, Cynthia K Thompson

Abstract

Linguistic theory suggests non-canonical sentences subvert the dominant agent-verb-theme order in English via displacement of sentence constituents to argument (NP-movement) or non-argument positions (wh-movement). Both processes have been associated with the left inferior frontal gyrus and posterior superior temporal gyrus, but differences in neural activity and connectivity between movement types have not been investigated. In the current study, functional magnetic resonance imaging data were acquired from 21 adult participants during an auditory sentence-picture verification task using passive and active sentences contrasted to isolate NP-movement, and object- and subject-cleft sentences contrasted to isolate wh-movement. Then, functional magnetic resonance imaging data from regions common to both movement types were entered into a dynamic causal modeling analysis to examine effective connectivity for wh-movement and NP-movement. Results showed greater left inferior frontal gyrus activation for Wh > NP-movement, but no activation for NP > Wh-movement. Both types of movement elicited activity in the opercular part of the left inferior frontal gyrus, left posterior superior temporal gyrus, and left medial superior frontal gyrus. The dynamic causal modeling analyses indicated that neither movement type significantly modulated the connection from the left inferior frontal gyrus to the left posterior superior temporal gyrus, nor vice-versa, suggesting no connectivity differences between wh- and NP-movement. These findings support the idea that increased complexity of wh-structures, compared to sentences with NP-movement, requires greater engagement of cognitive resources via increased neural activity in the left inferior frontal gyrus, but both movement types engage similar neural networks.

Keywords: dynamic causal modeling; functional magnetic resonance imaging; non-canonical sentences; sentence comprehension; syntactic movement.

Figures

Figure 1
Figure 1
Example trial from the auditory sentence-picture verification task.
Figure 2
Figure 2
Base dynamic causal model of network of regions involved in non-canonical sentence processing for sentence-picture verification task. LSFGm, Left superior frontal gyrus, medial part. LIFGop, left inferior frontal gyrus, opercular part. LSTGp, Left superior temporal gyrus, posterior part.
Figure 3
Figure 3
Significant fMRI activation (uncorrected voxelwise p < 0.001) of the contrasts Sentences > Baseline and vice-versa (corrected cluster-defining threshold k > 61), Non-canonical > Canonical (k > 43.4), and Wh > NP-movement (k > 42.1) from healthy adult participants.
Figure 4
Figure 4
Significant fMRI activation (uncorrected voxelwise p < 0.001) of Non-canonical > Canonical (corrected cluster-defining threshold k > 61) masked by Sentences > Baseline (k > 61) from healthy adult participants.
Figure 5
Figure 5
Results for wh-movement models (**p < 0.05, FDR-corrected; *p < 0.05, uncorrected; ∧p < 0.08, uncorrected).
Figure 6
Figure 6
Results for NP-movement models (**p < 0.05, FDR-corrected; *p < 0.05, uncorrected; ∧p < 0.08, uncorrected).

References

    1. Adank P. (2012a). Design choices in imaging speech comprehension: an activation likelihood estimation (ALE) meta-analysis. Neuroimage 63, 1601–1613. 10.1016/j.neuroimage.2012.07.027
    1. Adank P. (2012b). The neural bases of difficult speech comprehension and speech production: two activation likelihood estimation (ALE) meta-analyses. Brain Lang. 122, 42–54. 10.1016/j.bandl.2012.04.014
    1. Alario F. X., Chainay H., Lehericy S., Cohen L. (2006). The role of the supplementary motor area (SMA) in word production. Brain Res. 1076, 129–143. 10.1016/j.brainres.2005.11.104
    1. Alpert K., Kogan A., Parrish T., Marcus D., Wang L. (2016). The northwestern university neuroimaging data archive (NUNDA). Neuroimage 124, 1131–1136. 10.1016/j.neuroimage.2015.05.060
    1. Ben-Shachar M., Hendler T., Kahn I., Ben-Bashat D., Grodzinsky Y. (2003). The neural reality of syntactic transformations: evidence from functional magnetic resonance imaging. Psychol. Sci. 14, 433–440. 10.1111/1467-9280.01459
    1. Ben-Shachar M., Palti D., Grodzinsky Y. (2004). Neural correlates of syntactic movement: converging evidence from two fMRI experiments. Neuroimage 21, 1320–1336. 10.1016/j.neuroimage.2003.11.027
    1. Bornkessel I., Zysset S., Friederici A. D., Yves von Cramon D., Schlesewsky M. (2005). Who did what to whom? The neural basis of argument hierarchies during language comprehension. NeuroImage 26, 221–233. 10.1016/j.neuroimage.2005.01.032
    1. Bornkessel-Schlesewsky I., Grewe T., Schlesewsky M. (2012). Prominence vs. aboutness in sequencing: A functional distinction within the left inferior frontal gyrus. Brain Lang. 120, 96–107. 10.1016/j.bandl.2010.06.004
    1. Bornkessel-Schlesewsky I., Schlesewsky M. (2013). Reconciling time, space and function: a new dorsal–ventral stream model of sentence comprehension. Brain Lang. 125, 60–76. 10.1016/j.bandl.2013.01.010
    1. Boylan C., Trueswell J. C., Thompson-Schill S. L. (2015). Compositionality and the angular gyrus: a multi-voxel similarity analysis of the semantic composition of nouns and verbs. Neuropsychologia 78, 130–141. 10.1016/j.neuropsychologia.2015.10.007
    1. Boylan C., Trueswell J. C., Thompson-Schill S. L. (2017). Relational vs. attributive interpretation of nominal compounds differentially engages angular gyrus and anterior temporal lobe. Brain Lang. 169, 8–21. 10.1016/j.bandl.2017.01.008
    1. Campbell K. L., Samu D., Davis S. W., Geerligs L., Mustafa A., Tyler L. K. (2016). Robust resilience of the frontotemporal syntax system to aging. J. Neurosci. 36, 5214–5227. 10.1523/JNEUROSCI.4561-15.2016
    1. Campbell K. L., Tyler L. K. (2018). Language-related domain-specific and domain-general systems in the human brain. Curr. Opin. Behav. Sci. 21, 132–137. 10.1016/j.cobeha.2018.04.008
    1. Caplan D., Alpert N., Waters G. (1999). PET studies of syntactic processing with auditory sentence presentation. Neuroimage 9, 343–351. 10.1006/nimg.1998.0412
    1. Caplan D., Stanczak L., Waters G. (2008). Syntactic and thematic constraint effects on blood oxygenation level dependent signal correlates of comprehension of relative clauses. J. Cogn. Neurosci. 20, 643–656. 10.1162/jocn.2008.20044
    1. Catani M., Mesulam M.-M., Jakobsen E., Malik F., Martersteck A., Wieneke C., et al. . (2013). A novel frontal pathway underlies verbal fluency in primary progressive aphasia. Brain 136, 2619–2628. 10.1093/brain/awt163
    1. Chomsky N. (1986). Barriers, Vol. 13. Cambridge, MA: The MIT Press.
    1. Chomsky N. (1995). The Minimalist Program. Cambridge, MA: The MIT Press.
    1. Corbetta M., Shulman G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201–215. 10.1038/nrn755
    1. Costafreda S. G., Fu C. H., Lee L., Everitt B., Brammer M. J., David A. S. (2006). A systematic review and quantitative appraisal of fMRI studies of verbal fluency: role of the left inferior frontal gyrus. Hum. Brain Mapp. 27, 799–810. 10.1002/hbm.20221
    1. Crozier S., Sirigu A., Lehéricy S., van de Moortele P.-F., Pillon B., Grafman J., et al. . (1999). Distinct prefrontal activations in processing sequence at the sentence and script level: an fMRI study. Neuropsychologia 37, 1469–1476. 10.1016/S0028-3932(99)00054-8
    1. den Ouden D. B., Saur D., Mader W., Schelter B., Lukic S., Wali E., et al. . (2012). Network modulation during complex syntactic processing. Neuroimage 59, 815–823. 10.1016/j.neuroimage.2011.07.057
    1. Dick A. S., Bernal B., Tremblay P. (2014). The language connectome: new pathways, new concepts. Neuroscientist 20, 453–467. 10.1177/1073858413513502
    1. Dickey M. W., Choy J. J., Thompson C. K. (2007). Real-time comprehension of wh- movement in aphasia: evidence from eyetracking while listening. Brain Lang. 100, 1–22. 10.1016/j.bandl.2006.06.004
    1. Dickey M. W., Thompson C. K. (2004). The resolution and recovery of filler-gap dependencies in aphasia: evidence from on-line anomaly detection. Brain Lang. 88, 108–127. 10.1016/S0093-934X(03)00283-9
    1. Dickey M. W., Thompson C. K. (2009). Automatic processing of wh- and NP- movement in agrammatic aphasia: evidence from eye-tracking. J. Neurolinguistics 22, 563–583. 10.1016/j.jneuroling.2009.06.004
    1. Dosenbach N. U., Visscher K. M., Palmer E. D., Miezin F. M., Wenger K. K., Kang H. C., et al. . (2006). A core system for the implementation of task sets. Neuron 50, 799–812. 10.1016/j.neuron.2006.04.031
    1. Dreher J.-C., Grafman J. (2003). Dissociating the roles of the rostral anterior cingulate and the lateral prefrontal cortices in performing two tasks simultaneously or successively. Cerebral Cortex 13, 329–339. 10.1093/cercor/13.4.329
    1. Eklund A., Nichols T. E., Knutsson H. (2016). Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proc. Natl. Acad. Sci. U.S.A. 113:7900–5. 10.1073/pnas.1602413113
    1. Feng S., Legault J., Yang L., Zhu J., Shao K., Yang Y. (2015). Differences in grammatical processing strategies for active and passive sentences: an fMRI study. J. Neurolinguistics 33, 104–117. 10.1016/j.jneuroling.2014.09.002
    1. Finocchiaro C., Capasso R., Cattaneo L., Zuanazzi A., Miceli G. (2015). Thematic role assignment in the posterior parietal cortex: a TMS study. Neuropsychologia 77, 223–232. 10.1016/j.neuropsychologia.2015.08.025
    1. Friederici A. D. (2011). The brain basis of language processing: From structure to function. Physiol. Rev. 91, 1357–1392. 10.1152/physrev.00006.2011
    1. Friederici A. D. (2012). The cortical language circuit: from auditory perception to sentence comprehension. Trends Cogn. Sci. 16, 262–268. 10.1016/j.tics.2012.04.001
    1. Friston K. J., Harrison L., Penny W. (2003). Dynamic causal modelling. Neuroimage 19, 1273–1302. 10.1016/S1053-8119(03)00202-7
    1. Grodzinsky Y., Santi A. (2008). The battle for Broca's region. Trends Cogn. Sci. 12, 474–480. 10.1016/j.tics.2008.09.001
    1. Hagoort P. (2005). On Broca, brain, and binding: a new framework. Trends Cogn. Sci. 9, 416–423. 10.1016/j.tics.2005.07.004
    1. Henry R. G., Berman J. I., Nagarajan S. S., Mukherjee P., Berger M. S. (2004). Subcortical pathways serving cortical language sites: initial experience with diffusion tensor imaging fiber tracking combined with intraoperative language mapping. Neuroimage 21, 616–622. 10.1016/j.neuroimage.2003.09.047
    1. Hirotani M., Makuuchi M., Ruschemeyer S., Friederici A. D. (2011). Who was the agent? The neural correlates of reanalysis processes during sentence comprehension. Hum. Brain Mapp. 32, 1775–1787. 10.1002/hbm.21146
    1. Kalénine S., Peyrin C., Pichat C., Segebarth C., Bonthoux F., Baciu M. (2009). The sensory-motor specificity of taxonomic and thematic conceptual relations: A behavioral and fMRI study. Neuroimage 44, 1152–1162. 10.1016/j.neuroimage.2008.09.043
    1. Kinno R., Kawamura M., Shioda S., Sakai K. L. (2008). Neural correlates of noncanonical syntactic processing revealed by picture-sentence matching task. Hum. Brain Mapp. 29, 1015–1027. 10.1002/hbm.20441
    1. Kristensen L. B., Wang L., Petersson K. M., Hagoort P. (2013). The interface between language and attention: prosodic focus marking recruits a general attention network in spoken language comprehension. Cerebral Cortex 23, 1836–1848. 10.1093/cercor/bhs164
    1. Lee M.-W. (2004). Another look at the role of empty categories in sentence processing (and grammar). J. Psycholinguist. Res. 33, 51–73. 10.1023/B:JOPR.0000010514.50468.30
    1. Lewis G. A., Poeppel D., Murphy G. L. (2015). The neural bases of taxonomic and thematic conceptual relations: an MEG study. Neuropsychologia 68, 176–189. 10.1016/j.neuropsychologia.2015.01.011
    1. Mack J. E., Meltzer-Asscher A., Barbieri E., Thompson C. K. (2013). Neural correlates of processing passive sentences. Brain Sci. 3, 1198–1214. 10.3390/brainsci3031198
    1. Makuuchi M., Friederici A. D. (2013). Hierarchical functional connectivity between the core language system and the working memory system. Cortex 49, 2416–2423. 10.1016/j.cortex.2013.01.007
    1. Makuuchi M., Grodzinsky Y., Amunts K., Santi A., Friederici A. D. (2012). Processing noncanonical sentences in Broca's region: reflections of movement distance and type. Cereb. Cortex 23, 694–702. 10.1093/cercor/bhs058
    1. Marreiros A. C., Kiebel S. J., Friston K. J. (2008). Dynamic causal modelling for fMRI: a two-state model. Neuroimage 39, 269–278. 10.1016/j.neuroimage.2007.08.019
    1. Martino J., Lucas E. M. (2014). Subcortical anatomy of the lateral association fascicles of the brain: a review. Clin. Anat. 27, 563–569. 10.1002/ca.22321
    1. Matchin W., Hickok G. (2016). ‘Syntactic Perturbation’during production activates the right IFG, but not broca's area or the ATL. Front. Psychol. 7:241 10.3389/fpsyg.2016.00241
    1. Mauner G., Fromkin V. A., Cornell T. L. (1993). Comprehension and acceptability judgments in agrammatism: disruptions in the syntax of referential dependency. Brain Lang. 45, 340–370. 10.1006/brln.1993.1050
    1. Mizuno K., Tanaka M., Tanabe H. C., Sadato N., Watanabe Y. (2012). The neural substrates associated with attentional resources and difficulty of concurrent processing of the two verbal tasks. Neuropsychologia 50, 1998–2009. 10.1016/j.neuropsychologia.2012.04.025
    1. Nagel H. N., Shapiro L. P., Nawy R. (1994). Prosody and the processing of filler-gap sentences. J. Psycholinguist. Res. 23, 473–485. 10.1007/BF02146686
    1. Raichle M. E., Snyder A. Z. (2007). A default mode of brain function: a brief history of an evolving idea. Neuroimage 37, 1083–1090. 10.1016/j.neuroimage.2007.02.041
    1. Rogalsky C., Hickok G. (2011). The role of Broca's area in sentence comprehension. J. Cogn. Neurosci. 23, 1664–1680. 10.1162/jocn.2010.21530
    1. Salis C., Edwards S. (2005). Comprehension of wh-questions in agrammatism: a single-case study. Read. Work. Pap. Linguist. 8, 219–233. Available online at:
    1. Schlesewsky M., Bornkessel-Schlesewsky I. (2013). Computational primitives in syntax and possible brain correlates, in The Cambridge Handbook of Biolinguistics, eds Boeckx C., Grohmann K. (Cambridge: Cambridge University Press; ), 257–282. 10.1017/CBO9780511980435.016
    1. Segaert K., Kempen G., Petersson K. M., Hagoort P. (2013). Syntactic priming and the lexical boost effect during sentence production and sentence comprehension: an fMRI study. Brain Lang. 124, 174–183. 10.1016/j.bandl.2012.12.003
    1. Seghier M. L., Zeidman P., Neufeld N. H., Leff A. P., Price C. J. (2010). Identifying abnormal connectivity in patients using dynamic causal modeling of FMRI responses. Front. Syst. Neurosci. 4:142. 10.3389/fnsys.2010.00142
    1. Shetreet E., Friedmann N. (2014). The processing of different syntactic structures: fMRI investigation of the linguistic distinction between wh-movement and verb movement. J. Neurolinguistics 27, 1–17. 10.1016/j.jneuroling.2013.06.003
    1. Skipper J. I. (2014). Echoes of the spoken past: how auditory cortex hears context during speech perception. Phil. Trans. R. Soc. B 369:20130297. 10.1098/rstb.2013.0297
    1. Stephan K. E., Penny W. D., Moran R. J., den Ouden H. E., Daunizeau J., Friston K. J. (2010). Ten simple rules for dynamic causal modeling. Neuroimage 49, 3099–3109. 10.1016/j.neuroimage.2009.11.015
    1. Swick D., Ashley V., Turken U. (2008). Left inferior frontal gyrus is critical for response inhibition. BMC Neurosci. 9:102. 10.1186/1471-2202-9-102
    1. Thompson C. K., Bonakdarpour B., Fix S. F. (2010a). Neural mechanisms of verb argument structure processing in agrammatic aphasic and healthy age-matched listeners. J. Cogn. Neurosci. 22, 1993–2011. 10.1162/jocn.2009.21334
    1. Thompson C. K., den Ouden D.-B., Bonakdarpour B., Garibaldi K., Parrish T. B. (2010b). Neural plasticity and treatment-induced recovery of sentence processing in agrammatism. Neuropsychologia 48, 3211–3227. 10.1016/j.neuropsychologia.2010.06.036
    1. Thompson C. K., Meltzer-Asscher A. (2014). Neurocognitive mechanisms of verb argument structure processing, in Structuring the Argument: Multidisciplinary Research on Verb Argument Structure, eds Bachrach A., Roy I., Stockall L. (Amsterdam: John Benjamins; ), 141–168. 10.1075/lfab.10.07tho
    1. Van Essen D. C., Maunsell J. H. (1983). Hierarchical organization and functional streams in the visual cortex. Trends Neurosci. 6, 370–375. 10.1016/0166-2236(83)90167-4
    1. Wang X., Song X., Mack J., Thompson C. K., Parrish T. B. (2015). Reliability of language network BOLD activation, in Paper presented at the Society for the Neurobiology of Language (Chicago, IL: ).
    1. Ye Z., Zhou X. (2009). Conflict control during sentence comprehension: fMRI evidence. Neuroimage 48, 280–290. 10.1016/j.neuroimage.2009.06.032
    1. Yokoyama S., Okamoto H., Miyamoto T., Yoshimoto K., Kim J., Iwata K., et al. . (2006). Cortical activation in the processing of passive sentences in L1 and L2: an fMRI study. Neuroimage 30, 570–579. 10.1016/j.neuroimage.2005.09.066
    1. Yokoyama S., Watanabe J., Iwata K., Ikuta N., Haji T., Usui N., et al. . (2007). Is Broca's area involved in the processing of passive sentences? An event-related fMRI study. Neuropsychologia 45, 989–996. 10.1016/j.neuropsychologia.2006.09.003

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