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Distinct spatiotemporal patterns of syntactic and semantic processing in human inferior frontal gyrus

Abstract

Human languages are based on syntax, a set of rules which allow an infinite number of meaningful sentences to be constructed from a finite set of words. A theory associated with Chomsky and others holds that syntax is a mind-internal, universal structure independent of semantics. This theory, however, has been challenged by studies of the Chinese language showing that syntax is processed under the semantic umbrella, and is secondary and not independent. Here, using intracranial high-density electrocorticography, we find distinct spatiotemporal patterns of neural activity in the left inferior frontal gyrus that are specifically associated with syntactic and semantic processing of Chinese sentences. These results suggest that syntactic processing may occur before semantic processing. Our findings are consistent with the view that the human brain implements syntactic structures in a manner that is independent of semantics.

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Fig. 1: Study paradigm and different neural responsivity to semantic and syntactic violation tasks.
Fig. 2: Spatial representation of syntax and semantics.
Fig. 3: Temporal representation of syntax and semantics.

Data availability

Source data are provided with this paper. The data set generated during the current study will be made available from the authors upon reasonable request.

Code availability

The completely developed code that operates on the full data set will be made available from the authors upon reasonable request.

References

  1. Hauser, M. D., Chomsky, N.& Fitch, W. T. The faculty of language: what is it, who has it, and how did it evolve? Science 298, 1569–1579 (2002).

    CAS  PubMed  Article  Google Scholar 

  2. Chomsky, N. Rules and Representations (Columbia Univ. Press, 1980).

  3. Fodor, J. A. Modularity of Mind (MIT Press, 1983).

  4. Pinker, S. Rules of language. Science 253, 530–535 (1991).

    CAS  PubMed  Article  Google Scholar 

  5. Dapretto, M. & Bookheimer, S. Y. Form and content: dissociating syntax and semantics in sentence comprehension. Neuron 24, 427–432 (1999).

    CAS  PubMed  Article  Google Scholar 

  6. Friederici, A. D., Chomsky, N., Berwick, R. C. Moro, A. & Bolhuis, J. J. Language, mind and brain. Nat. Hum. Behav. 1, 713–722 (2017).

    PubMed  Article  Google Scholar 

  7. Pylkkänen, L. The neural basis of combinatory syntax and semantics. Science 366, 62–66 (2019).

    PubMed  Article  CAS  Google Scholar 

  8. Hagoort, P. The core and beyond in the language-ready brain. Neurosci. Biobehav. Rev. 81, 194–204 (2017).

    PubMed  Article  Google Scholar 

  9. Pallier, C., Devauchelle, A. & Dehaene, S. Cortical representation of the constituent structure of sentences. Proc. Natl Acad. Sci. USA 108, 2522–2527 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. Grodzinsky, Y. The neurology of syntax: language use without Broca’s area. Behav. Brain Sci. 23, 1–21 (2000).

    CAS  PubMed  Article  Google Scholar 

  11. Tyler, L. K. et al. Left inferior frontal cortex and syntax: function, structure and behaviour in patients with left hemisphere damage. Brain 134, 415–431 (2011).

    PubMed  PubMed Central  Article  Google Scholar 

  12. Dronkers, N. F. A new brain region for coordinating speech articulation. Nature 384, 159–161 (1996).

  13. Embick, D., Marantz, A., Miyashita, Y. Oneil, W. & Sakai, K. L. A syntactic specialization for Broca’s area. Proc. Natl Acad. Sci. USA 97, 6150–6154 (2000).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  14. Glaser, Y. G., Martin, R. C., Van Dyke, J. A., Hamilton, A. C. & Tan, Y. Neural basis of semantic and syntactic interference in sentence comprehension. Brain Lang. 126, 314–326 (2013).

    PubMed  Article  Google Scholar 

  15. Hagoort, P. & Indefrey, P. The neurobiology of language beyond single words. Annu. Rev. Neurosci. 37, 347–362 (2014).

    CAS  PubMed  Article  Google Scholar 

  16. Prat, C. S. & Just, M. A. Exploring the neural dynamics underpinning individual differences in sentence comprehension. Cereb. Cortex 21, 1747–1760 (2011).

    PubMed  Article  Google Scholar 

  17. Hashimoto, R. & Sakai, K. L. Specialization in the left prefrontal cortex for sentence comprehension. Neuron 35, 589–597 (2002).

    CAS  PubMed  Article  Google Scholar 

  18. Osterhout, L. & Holcomb, P. J. Event-related brain potentials elicited by syntactic anomaly. J. Mem. Lang. 31, 785–806 (1992).

    Article  Google Scholar 

  19. Friederici, A. D. The brain basis of language processing: from structure to function. Physiol. Rev. 91, 1357–1392 (2011).

    PubMed  Article  Google Scholar 

  20. Kutas, M. & Federmeier, K. D. Thirty years and counting: finding meaning in the N400 component of the event-related brain potential (ERP). Annu. Rev. Psychol. 62, 621–647 (2011).

    PubMed  PubMed Central  Article  Google Scholar 

  21. Blank, I., Balewski, Z., Mahowald, K. & Fedorenko, E. Syntactic processing is distributed across the language system. Neuroimage 127, 307–323 (2016).

    PubMed  Article  Google Scholar 

  22. Rogalsky, C. & Hickok, G. Selective attention to semantic and syntactic features modulates sentence processing networks in anterior temporal cortex. Cereb. Cortex 19, 786–796 (2009).

    PubMed  Article  Google Scholar 

  23. Luke, K., Liu, H., Wai, Y., Wan, Y. & Tan, L. Functional anatomy of syntactic and semantic processing in language comprehension. Hum. Brain Mapp. 16, 133–145 (2002).

    PubMed  PubMed Central  Article  Google Scholar 

  24. Bautista, A. & Wilson, S. M. Neural responses to grammatically and lexically degraded speech. Lang., Cognition Neurosci. 31, 567–574 (2016).

    Article  Google Scholar 

  25. Fedorenko, E. & Varley, R. Language and thought are not the same thing: evidence from neuroimaging and neurological patients. Ann. N. Y. Acad. Sci. 1369, 132–153 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  26. Heim, S., Eickhoff, S. B. & Amunts, K. Specialisation in Broca’s region for semantic, phonological, and syntactic fluency? Neuroimage 40, 1362–1368 (2008).

    PubMed  Article  Google Scholar 

  27. Rodd, J. M., Vitello, S., Woollams, A. M. & Adank, P. Localising semantic and syntactic processing in spoken and written language comprehension: an activation likelihood estimation meta-analysis. Brain Lang. 141, 89–102 (2015).

    PubMed  Article  Google Scholar 

  28. Dick, F. et al. Language deficits, localization, and grammar: evidence for a distributive model of language breakdown in aphasic patients and neurologically intact individuals. Psychol. Rev. 108, 759–788 (2001).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  29. Kaan, E. & Swaab, T. Y. The brain circuitry of syntactic comprehension. Trends Cogn. Sci. 6, 350–356 (2002).

    PubMed  Article  Google Scholar 

  30. Fedorenko, E., Nietocastanon, A. & Kanwisher, N. Lexical and syntactic representations in the brain: an fMRI investigation with multi-voxel pattern analyses. Neuropsychologia 50, 499–513 (2012).

    PubMed  Article  Google Scholar 

  31. Mesulam, M. M. et al. Primary progressive aphasia and the evolving neurology of the language network. Nat. Rev. Neurol. 10, 554–569 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  32. Wilson, S. M., Galantucci, S., Tartaglia, M. C. & Gornotempini, M. L. The neural basis of syntactic deficits in primary progressive aphasia. Brain Lang. 122, 190–198 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  33. Anumanchipalli, G. K., Chartier, J. & Chang, E. F. Speech synthesis from neural decoding of spoken sentences. Nature 568, 493–498 (2019).

    CAS  PubMed  Article  Google Scholar 

  34. Li, C. & Thompson, S. Mandarin Chinese: A Functional Reference Grammar (Univ. of California Press, 1989).

  35. Wang, W. S. Y. The Chinese language. Sci. Am. 228, 50–62 (1973).

    Article  Google Scholar 

  36. Li, P., Shu, H. & Liu, Y. in The Handbook of Chinese Linguistics (eds Huang, C.-T. J. et al.) (John Wiley & Sons, 2014).

  37. Zhang, Y., Yu, J. & Boland, J. E. Semantics does not need a processing license from syntax in reading Chinese.J. Exp. Psychol.: Learning Mem. Cognition 36, 765–781 (2010).

    Google Scholar 

  38. Scott, B. Translation, Brains and the Computer. Machine Translation: Technologies and Applications (Springer, 2018).

  39. Liu, Y., Li, P., Shu, H., Zhang, Q. & Chen, L. Structure and meaning in Chinese: an ERP study of idioms. J. Neurolinguist. 23, 615–630 (2010).

    Article  Google Scholar 

  40. Ye, Z., Luo, Y., Friederici, A. D. & Zhou, X. Semantic and syntactic processing in Chinese sentence comprehension: evidence from event-related potentials. Brain Res. 1071, 186–196 (2006).

    CAS  PubMed  Article  Google Scholar 

  41. Li, P., Jin, Z. & Tan, L. H. Neural representations of nouns and verbs in Chinese: an fMRI study. Neuroimage 21, 1533–1541 (2004).

    PubMed  Article  Google Scholar 

  42. Wu, C., Zaccarella, E. & Friederici, A. D. Universal neural basis of structure building evidenced by network modulations emerging from Broca’s area: the case of Chinese. Hum. Brain Mapp. 40, 1705–1717 (2019).

    PubMed  Article  Google Scholar 

  43. Leise, E. M. Modular construction of nervous systems: a basic principle of design for invertebrates and vertebrates. Brain Res. Rev. 15, 1–23 (1990).

    CAS  PubMed  Article  Google Scholar 

  44. Chomsky, N. Language and Mind 3rd edn (Cambridge Univ. Press, 2006).

  45. Frazier, L. & Fodor, J. D. The sausage machine: a new two-stage parsing model. Cognition 6, 291–325 (1978).

    Article  Google Scholar 

  46. Friederici, A. D. Towards a neural basis of auditory sentence processing. Trends Cogn. Sci. 6, 78–84 (2002).

    PubMed  Article  Google Scholar 

  47. Mukamel, R. et al. Coupling between neuronal firing, field potentials, and FMRI in human auditory cortex. Science 309, 951–954 (2005).

    CAS  PubMed  Article  Google Scholar 

  48. Nir, Y. et al. Coupling between neuronal firing rate, gamma LFP, and BOLD fMRI is related to interneuronal correlations. Curr. Biol. 17, 1275–1285 (2007).

    CAS  PubMed  Article  Google Scholar 

  49. Gregoriou, G. G., Gotts, S. J., Zhou, H. & Desimone, R. High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science 324, 1207–1210 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  50. Sahin, N. T., Pinker, S., Cash, S. S., Schomer, D. L. & Halgren, E. Sequential processing of lexical, grammatical, and phonological information within Broca’s area. Science 326, 445–449 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  51. Friston, K. J. & Price, C. J. Modules and brain mapping. Cogn. Neuropsychol. 28, 241–250 (2011).

    PubMed  PubMed Central  Article  Google Scholar 

  52. Kanwisher, N. Functional specificity in the human brain: a window into the functional architecture of the mind. Proc. Natl Acad. Sci. USA 107, 11163–11170 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  53. Goucha, T. & Friederici, A. D. The language skeleton after dissecting meaning: a functional segregation within Broca’s area. Neuroimage 114, 294–302 (2015).

    PubMed  Article  Google Scholar 

  54. Zaccarella, E. Meyer, L., Makuuchi, M. & Friederici, A. D. Building by syntax: the neural basis of minimal linguistic structures. Cereb. Cortex 27, 411–421 (2015).

    Google Scholar 

  55. Siok, W. T., Perfetti, C. A., Jin, Z. & Tan, L. H. Biological abnormality of impaired reading is constrained by culture. Nature 431, 71–76 (2004).

    CAS  PubMed  Article  Google Scholar 

  56. Perfetti, C. A., Cao, F. & Booth, J. Specialization and universals in the development of reading skill: how Chinese research informs a universal science of reading. Sci. Stud. Read. 17, 5–21 (2013).

    PubMed  Article  Google Scholar 

  57. Nakamura, K. et al. Universal brain systems for recognizing word shapes and handwriting gestures during reading. Proc. Natl Acad. Sci. USA 109, 20762–20767 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  58. Goldberg, A. E. A Construction Grammar Approach to Argument Structure (Univ. of Chicago Press, 1995).

  59. Lu, J. et al. Awake language mapping and 3-Tesla intraoperative MRI-guided volumetric resection for gliomas in language areas. J. Clin. Neurosci. 20, 1280–1287 (2013).

    PubMed  Article  Google Scholar 

  60. Wu, J. et al. Direct evidence from intraoperative electrocortical stimulation indicates shared and distinct speech production center between Chinese and English languages. Hum. Brain Mapp. 36, 4972–4985 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  61. Hamilton, L. S., Chang, D. L., Lee, M. B. & Chang, E. F. Semi-automated anatomical labeling and inter-subject warping of high-density intracranial recording electrodes in electrocorticography. Front. Neuroinform. 11, 62 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  62. VS Fonov, A. E., McKinstry, R. C., Almli, C. R. & Collins, D. L. Unbiased nonlinear average age-appropriate brain templates from birth to adulthood. NeuroImage 47, S102 (2009).

    Article  Google Scholar 

  63. Friederici, A. D. & Meyer, M. The brain knows the difference: Two types of grammatical violations. Brain Res. 1000, 72–77 (2004).

    CAS  PubMed  Article  Google Scholar 

  64. Hahne, A. & Friederici, A. D. Differential task effects on semantic and syntactic processes as revealed by ERPs. Cognitive Brain Res. 13, 339–356 (2002).

    Article  Google Scholar 

  65. Pedregosa, F. et al. Scikit-learn: machine learning in Python. J. Mach. Learn. Res. 12, 2825–2830 (2011).

    Google Scholar 

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Acknowledgements

This work was supported by a grant on child brain-mind development in China’s Brain Initiative (no. SQ2021AAA010024) and by the Shenzhen Peacock Team Plan (no. KQTD2015033016104926), a Guangdong Pearl River Talents Plan Innovative and Entrepreneurial Team grant (no. 2016ZT06S220), The National Natural Science Foundation of China (grant no. 32171054), a Guangdong Key Basic Research Grant (no. 2018B030332001), Shenzhen Basic Research Grants (nos. JCYJ20170818110103216, JCYJ20170412164413575 and 2021SHIBS0003), the National Top Talent Undergraduate Training Programme (NTTUTP), the Shanghai Municipal Science and Technology Major Project (no. 2018SHZDZX01), the Shanghai Shenkang Hospital Development Centre (no. SHDC12018114), the Shanghai Rising-Star Programme (no. 19QA1401700) and the Shanghai Pujiang Programme (no. 21PJD007).

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Contributions

L.H.T. and J.W. conceived and supervised the project. J.L., M.X., Y. Zhu, V.P.Y.K., Y. Zhou, D.Y., B.W. and J.Z. collected the data. J.H., L.H.T., M.X., Y. Zhu, J.L. and J.W. designed the experiment. Y. Zhu, J.L. and M.X. analysed the data. Y. Zhu, J.L., M.X., J.H., J.W. and L.H.T. interpreted the data. Y. Zhu, M.X., J.L., J.H., J.W. and L.H.T. wrote the manuscript.

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Correspondence to Jinsong Wu or Li Hai Tan.

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Nature Human Behaviour thanks Heidi Harley and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Zhu, Y., Xu, M., Lu, J. et al. Distinct spatiotemporal patterns of syntactic and semantic processing in human inferior frontal gyrus. Nat Hum Behav 6, 1104–1111 (2022). https://doi.org/10.1038/s41562-022-01334-6

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