Abstract
Neuroimaging studies have indicated that a brain network distributed in the supramodal cortical regions of the frontal, temporal, and parietal lobes plays a central role in conceptual processing. The activation of this network is modulated by two orthogonal dimensions in conceptual processing—the semantic features of individual concepts and the meaningfulness of conceptual combinations—but it remains unclear how the network is functionally organized along these two dimensions. In this fMRI study, we focused on two specific factors, i.e. the social semantic richness of words and the semantic plausibility of word combinations, along the two dimensions. In literature, the distributions of the effects of the two factors are very similar, but have not been rigorously compared in one study. We orthogonally manipulated the two factors in a phrase comprehension task and found a clear dissociation between their effects. The combination of these results with our previous findings reveals three adjacently distributed subnetworks of the supramodal semantic network, associated with the sociality effect, imageability effect, and semantic plausibility effect, respectively. Further analysis of the resting-state functional connectivity data indicated that the functional dissociation among the three subnetworks is associated with their underlying intrinsic connectivity structures.
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Notes
Supramodal cortical regions: cortical regions that receive multimodal input not dominated by any single modality (Binder and Desai 2011).
References
Ashburner J, Friston KJ (2005) Unified segmentation. Neuroimage 26(3):839–851
Bemis DK, Pylkkänen L (2011) Simple composition: a magnetoencephalography investigation into the comprehension of minimal linguistic phrases. J Neurosci 31(8):2801–2814
Bemis DK, Pylkkänen L (2013) Basic linguistic composition recruits the left anterior temporal lobe and left angular gyrus during both listening and reading. Cereb Cortex 23(8):1859–1873
Binder JR, Conant LL, Humphries CJ, Fernandino L, Simons SB, Aguilar M, Desai RH (2016) Toward a brain-based componential semantic representation. Cogn Neuropsychol 33(3–4):130–174
Binder JR, Desai RH (2011) The neurobiology of semantic memory. Trends Cogn Sci 15(11):527–536
Binder JR, Desai RH, Graves WW, Conant LL (2009) Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb Cortex 19(12):2767–2796
Blanco-Elorrieta E, Ferreira VS, Del Prato P, Pylkkänen L (2018) The priming of basic combinatory responses in MEG. Cognition 170:49–63
Blank I, Balewski Z, Mahowald K, Fedorenko E (2016) Syntactic processing is distributed across the language system. Neuroimage 127:307–323
Bonhage CE, Fiebach CJ, Bahlmann J, Mueller JL (2014) Brain signature of working memory for sentence structure: enriched encoding and facilitated maintenance. J Cogn Neurosci 26(8):1654–1671
Boylan C, Trueswell JC, Thompson-Schill SL (2017) Relational vs. attributive interpretation of nominal compounds differentially engages angular gyrus and anterior temporal lobe. Brain Lang 169:8–21
Chinese Linguistic Data Consortium (2003). [Chinese lexicon] (CLDC-LAC-2003-001) Beijing, China: Tsinghua University, State Key Laboratory of Intelligent Technology and Systems, and Chinese Academy of Sciences, Institute of Automation
Contreras JM, Banaji MR, Mitchell JP (2012) Dissociable neural correlates of stereotypes and other forms of semantic knowledge. Soc Cogn Affect Neursci 7(7):764–770
Fernandino L, Binder JR, Desai RH, Pendl SL, Humphries CJ, Gross WL, Conant LL, Seidenberg MS (2016) Concept representation reflects multimodal abstraction: a framework for embodied semantics. Cereb Cortex 26(5):2018–2034
Ferstl EC, Neumann J, Bogler C, von Cramon DY (2008) The extended language network: a meta-analysis of neuroimaging studies on text comprehension. Hum Brain Mapp 29(5):581–593
Forgács B, Bohrn I, Baudewig J, Hofmann MJ, Pleh C, Jacobs AM (2012) Neural correlates of combinatorial semantic processing of literal and figurative noun noun compound words. Neuroimage 63(3):1432–1442
Gallagher HL, Happe F, Brunswick N, Fletcher PC, Frith U, Frith CD (2000) Reading the mind in cartoons and stories: an fMRI study of 'theory of mind' in verbal and nonverbal tasks. Neuropsychologia 38(1):11–21
Graves WW, Binder JR, Desai RH, Conant LL, Seidenberg MS (2010) Neural correlates of implicit and explicit combinatorial semantic processing. Neuroimage 53(2):638–646
Hagoort P (2013) MUC (memory, unification, control) and beyond. Front Psychol 4:416
Humphreys GF, Ralph MAL (2017) Mapping domain-selective and counterpointed domain-general higher cognitive functions in the lateral parietal cortex: evidence from fMRI comparisons of difficulty-varying semantic versus visuo-spatial tasks, and functional connectivity analyses. Cereb Cortex 27(8):4199–4212
Humphries C, Binder JR, Medler DA, Liebenthal E (2006) Syntactic and semantic modulation of neural activity during auditory sentence comprehension. J Cogn Neurosci 18(4):665–679
Huth AG, de Heer WA, Griffiths TL, Theunissen FE, Gallant JL (2016) Natural speech reveals the semantic maps that tile human cerebral cortex. Nature 532(7600):453–458
Jung-Beeman M (2005) Bilateral brain processes for comprehending natural language. Trends Cogn Sci 9(11):512–518
Lerner Y, Honey CJ, Silbert LJ, Hasson U (2011) Topographic mapping of a hierarchy of temporal receptive windows using a narrated story. J Neurosci 31(8):2906–2915
Leslie AM (1994) Pretending and believing: issues in the theory of ToMM. Cognition 50(1–3):211–238
Lin N, Bi YC, Zhao Y, Luo CM, Li XS (2015) The theory-of-mind network in support of action verb comprehension: evidence from an fMRI study. Brain Lang 141:1–10
Lin N, Wang X, Xu Y, Hua H, Zhao Y, Li X (2018) Fine subdivisions of the semantic network supporting social and sensory–motor semantic processing. Cereb Cortex 28(8):2699–2710
Lin N, Yu X, Zhao Y, Zhang M (2016) Functional anatomy of recognition of Chinese multi-character words: convergent evidence from effects of transposable nonwords, lexicality, and word frequency. PLoS ONE 11(2):e0149583
Mahon BZ, Caramazza A (2009) Concepts and categories: a cognitive neuropsychological perspective. Annu Rev Psychol 60:27–51
Martin A (2007) The representation of object concepts in the brain. Annu Rev Psychol 58:25–45
Mattheiss SR, Levinson H, Graves WW (2018) Duality of function: activation for meaningless nonwords and semantic codes in the same brain areas. Cereb Cortex 28(7):2516–2524
Mellem MS, Jasmin KM, Peng C, Martin A (2016) Sentence processing in anterior superior temporal cortex shows a social–emotional bias. Neuropsychologia 89:217–224
Meyer ML, Spunt RP, Berkman ET, Taylor SE, Lieberman MD (2012) Evidence for social working memory from a parametric functional MRI study. Proc Natl Acad Sci USA 109(6):1883–1888
Meyer ML, Taylor SE, Lieberman MD (2015) Social working memory and its distinctive link to social cognitive ability: an fMRI study. Soc Cogn Affect Neursci 10(10):1338–1347
Mitchell JP, Heatherton TF, Macrae CN (2002) Distinct neural systems subserve person and object knowledge. Proc Natl Acad Sci USA 99(23):15238–15243
Pallier C, Devauchelle AD, Dehaene S (2011) Cortical representation of the constituent structure of sentences. Proc Natl Acad Sci USA 108(6):2522–2527
Price AR, Bonner MF, Peelle JE, Grossman M (2015) Converging evidence for the neuroanatomic basis of combinatorial semantics in the angular gyrus. J Neurosci 35(7):3276–3284
Pylkkänen L, Bemis DK, Elorrieta EB (2014) Building phrases in language production: an MEG study of simple composition. Cognition 133(2):371–384
Pylkkänen L, Brennan J, Bemis DK (2011) Grounding the cognitive neuroscience of semantics in linguistic theory. Lang Cogn Proc 26(9):1317–1337
Rice GE, Hoffman P, Binney RJ, Ralph MAL (2018) Concrete versus abstract forms of social concept: an fMRI comparison of knowledge about people versus social terms. Philos Trans R Soc B 373(1752):20170136
Saxe R, Kanwisher N (2003) People thinking about thinking people: the role of the temporo-parietal junction in “theory of mind”. Neuroimage 19(4):1835–1842
Saxe R, Wexler A (2005) Making sense of another mind: the role of the right temporo-parietal junction. Neuropsychologia 43(10):1391–1399
Schurz M, Radua J, Aichhorn M, Richlan F, Perner J (2014) Fractionating theory of mind: a meta-analysis of functional brain imaging studies. Neurosci Biobehav Rev 42:9–34
Shrout PE, Fleiss JL (1979) Intraclass correlations—uses in assessing rater reliability. Psychol Bull 86(2):420–428
Silver NC, Dunlap WP (1987) Averaging correlation coefficients: should Fisher's z transformation be used? J Appl Psychol 72(1):146–148
Song XW, Dong ZY, Long XY, Li SF, Zuo XN, Zhu CZ, He Y, Yan CG, Zang YF (2011) REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS ONE 6(9):e25031
Stowe LA, Broere CAJ, Paans AMJ, Wijers AA, Mulder G, Vaalburg W, Zwarts F (1998) Localizing components of a complex task: sentence processing and working memory. NeuroReport 9(13):2995–2999
Tamir DI, Thornton MA, Contreras JM, Mitchell JP (2016) Neural evidence that three dimensions organize mental state representation: rationality, social impact, and valence. Proc Natl Acad Sci USA 113(1):194–199
Thompson CK, Bonakdarpour B, Fix SC, Blumenfeld HK, Parrish TB, Gitelman DR, Mesulam MM (2007) Neural correlates of verb argument structure processing. J Cogn Neurosci 19(11):1753–1767
Thompson CK, Bonakdarpour B, Fix SF (2010) Neural mechanisms of verb argument structure processing in agrammatic aphasic and healthy age-matched listeners. J Cogn Neurosci 22(9):1993–2011
Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15(1):273–289
Vandenberghe R, Nobre AC, Price CJ (2002) The response of left temporal cortex to sentences. J Cogn Neurosci 14(4):550–560
Wang X, Wang B, Bi Y (2019) Close yet independent: dissociation of social from valence and abstract semantic dimensions in the left anterior temporal lobe. Hum Brain Mapp 40(16):4759–4776
Williams A, Reddigari S, Pylkkänen L (2017) Early sensitivity of left perisylvian cortex to relationality in nouns and verbs. Neuropsychologia 100:131–143
Xia MR, Wang JH, He Y (2013) BrainNet viewer: a network visualization tool for human brain connectomics. PLoS ONE 8(7):e68910
Xu J, Kemeny S, Park G, Frattali C, Braun A (2005) Language in context: emergent features of word, sentence, and narrative comprehension. Neuroimage 25(3):1002–1015
Xu YW, Lin QX, Han ZZ, He Y, Bi YC (2016) Intrinsic functional network architecture of human semantic processing: modules and hubs. Neuroimage 132:542–555
Yarkoni T, Barch DM, Gray JR, Conturo TE, Braver TS (2009) BOLD correlates of trial-by-trial reaction time variability in gray and white matter: a multi-study fMRI analysis. PLoS ONE 4(1):e4257
Yeo BTT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M, Roffman JL, Smoller JW, Zoller L, Polimeni JR, Fischl B, Liu HS, Buckner RL (2011) The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol 106(3):1125–1165
Zahn R, Moll J, Krueger F, Huey ED, Garrido G, Grafman J (2007) Social concepts are represented in the superior anterior temporal cortex. Proc Natl Acad Sci USA 104(15):6430–6435
Zhang LM, Pylkkänen L (2015) The interplay of composition and concept specificity in the left anterior temporal lobe: an MEG study. Neuroimage 111:228–240
Zhang LM, Pylkkänen L (2018) Composing lexical versus functional adjectives: evidence for uniformity in the left temporal lobe. Psychon Bull Rev 25(6):2309–2322
Acknowledgements
This work was supported by National Natural Science Foundation of China (Grant numbers: 31871105 and 31300842) and by CAS Key Laboratory of Behavioral Science. We thank Yu Wang for her help in the preparation of experiment and Xiaohong Yang for helpful discussions.
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This study was funded by National Natural Science Foundation of China (Grant numbers: 31871105 and 31300842) and by CAS Key Laboratory of Behavioral Science.
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Lin, N., Xu, Y., Yang, H. et al. Dissociating the neural correlates of the sociality and plausibility effects in simple conceptual combination. Brain Struct Funct 225, 995–1008 (2020). https://doi.org/10.1007/s00429-020-02052-3
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DOI: https://doi.org/10.1007/s00429-020-02052-3