Dynamic brain lateralization patterns in Chinese naturalistic language comprehension and association with sex differences: a 7T functional magnetic resonance imaging study

Abstract

Background Although language is traditionally regarded as unique to humans and predominantly left-lateralized in the brain, the dynamic interplay between cerebral hemispheres during language processing remains poorly understood.

Methods Using 400 functional magnetic resonance imaging scans acquired with a 7T scanner under diverse narrative stimuli, this study examined whole-brain functional dynamic lateralization patterns during Chinese language processing and explored potential sex differences.

Results We identified two distinct dynamic lateralization states. While core language regions consistently showed left-lateralization, other brain regions displayed reversed lateralization. These two states-characterized by higher-level functional regions lateralizing either left or right-corresponded to the processing of rational and emotional content, respectively. Notably, males showed a stronger tendency toward the former state, whereas females inclined toward the latter, particularly during the processing of rational content. Genetic analyses further suggested that sex differences in these lateralization states may be influenced by sex hormones.

Conclusion This study offers novel insights into the dynamic organization of cerebral lateralization during Chinese language processing.

Keywords

dynamic laterality / Chinese language processing / naturalistic imaging / functional states / sex differences / sex hormones

References

[1] Arnatkevičiūtė A, Fulcher BD, Fornito A (2019) A practical guide to linking brain-wide gene expression and neuroimaging data. Neuroimage 189: 353-67.

[2] Baron-Cohen S, Richler J, Bisarya D, et al. (2003) The systemizing quotient: an investigation of adults with Asperger syndrome or high-functioning autism, and normal sex differences. Phil Trans R Soc Lond B 358(1430): 361-74.

[3] Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57(1): 289-300.

[4] Bi YC (2021) Dual coding of knowledge in the human brain. Trends Cogn Sci 25(10): 883-95.

[5] Bialystok E, Craik FI, Klein R, et al. (2004) Bilingualism, aging, and cognitive control: evidence from the Simon task. Psychol Aging 19(2): 290-303.

[6] Binder JR, Frost JA, Hammeke TA, et al. (1997) Human brain language areas identified by functional magnetic resonance imaging. J Neurosci 17(1): 353-62.

[7] Blondel VD, Guillaume J-L, Lambiotte R, et al. (2008) Fast unfolding of communities in large networks. J Stat Mech 2008(10): P10008.

[8] Bowers JM, Perez-Pouchoulen M, Edwards NS, et al. (2013) Foxp2 mediates sex differences in ultrasonic vocalization by rat pups and directs order of maternal retrieval. J Neurosci 33(8): 3276-83.

[9] Braga RM, DiNicola LM, Becker HC, et al. (2020) Situating the left-lateralized language network in the broader organization of multiple specialized large-scale distributed networks. J Neurophysiol 124(5): 1415-48.

[10] Budisavljevic S, Dell’Acqua F, Rijsdijk FV, et al. (2015) Age-related differences and heritability of the perisylvian language networks. J Neurosci 35(37): 12625-34.

[11] Burman DD, Minas T, Bolger DJ, et al. (2013) Age, sex, and verbal abilities affect location of linguistic connectivity in ventral visual pathway. Brain Lang 124(2): 184-93.

[12] Chai LR, Mattar MG, Blank IA, et al. (2016) Functional network dynamics of the language system. Cereb Cortex 26(11): 4148-59.

[13] Clements AM, Rimrodt SL, Abel JR, et al. (2006) Sex differences in cerebral laterality of language and visuospatial processing. Brain Lang 98(2): 150-8.

[14] Doron KW, Bassett DS, Gazzaniga MS (2012) Dynamic network structure of interhemispheric coordination. Proc Natl Acad Sci USA 109(46): 18661-8.

[15] Enard W, Przeworski M, Fisher SE, et al. (2002) Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418(6900): 869-72.

[16] Esteves M, Lopes SS, Almeida A, et al. (2020) Unmasking the relevance of hemispheric asymmetries-Break on through (to the other side). Prog Neurobiol 192: 101823.

[17] Federmeier KD, Jongman SR, Szewczyk JM (2020) Examining the role of general cognitive skills in language processing: a window into complex cognition. Curr Dir Psychol Sci 29(6): 575-82.

[18] Fedorenko E, Hsieh P-J, Nieto-Castañón A, et al. (2010) New method for fMRI investigations of language: defining ROIs functionally in individual subjects. J Neurophysiol 104(2): 1177-94.

[19] Fedorenko E, Thompson-Schill SL (2014) Reworking the language network. Trends Cogn Sci 18(3): 120-6.

[20] Feng G, Chen H-C, Zhu Z, et al. (2015) Dynamic brain architectures in local brain activity and functional network efficiency associate with efficient reading in bilinguals. Neuroimage 119: 103-18.

[21] Fernandino L, Binder JR, Desai RH, et al. (2016) Concept representation reflects multimodal abstraction: a framework for embodied semantics. Cereb Cortex 26(5): 2018-34.

[22] Friederici AD (2017) Evolution of the neural language network. Psychon Bull Rev 24(1): 41-7.

[23] Fulcher BD, Little MA, Jones NS (2013) Highly comparative time-series analysis: the empirical structure of time series and their methods. J R Soc Interface 10(83): 20130048.

[24] Gerrits R, Verhelst H, Vingerhoets G (2020) Mirrored brain organization: statistical anomaly or reversal of hemispheric functional segregation bias? Proc Natl Acad Sci USA 117(25): 14057-65.

[25] Glasser MF, Coalson TS, Robinson EC, et al. (2016) A multi-modal parcellation of human cerebral cortex. Nature 536(7615): 171-8.

[26] Greenberg DM, Warrier V, Abu-Akel A, et al. (2023) Sex and age differences in “theory of mind” across 57 countries using the English version of the “Reading the Mind in the Eyes” Test. Proc Natl Acad Sci USA 120(1): e2022385119.

[27] Greenberg DM, Warrier V, Allison C, et al. (2018) Testing the empathizing-systemizing theory of sex differences and the extreme male brain theory of autism in half a million people. Proc Natl Acad Sci USA 115(48): 12152-7.

[28] Haesler S, Rochefort C, Georgi B, et al. (2007) Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus Area X. PLoS Biol 5(12): e321.

[29] Hakim AA, Erwin A, Eng KI, et al. (2014) Automated document classification for news article in Bahasa Indonesia based on term frequency inverse document frequency (TF-IDF) approach. In: 2014 6th International Conference on Information Technology and Electrical Engineering (ICITEE), Yogyakarta, Indonesia, 1-4.

[30] Hausmann M (2017) Why sex hormones matter for neuroscience: a very short review on sex, sex hormones, and functional brain asymmetries. J Neurosci Res 95(1-2): 40-9.

[31] Hawrylycz M, Miller JA, Menon V, et al. (2015) Canonical genetic signatures of the adult human brain. Nat Neurosci 18(12): 1832-44.

[32] Hawrylycz MJ, Lein ES, Guillozet-Bongaarts AL, et al. (2012) An anatomically comprehensive atlas of the adult human brain transcriptome. Nature 489(7416): 391-9.

[33] Hiltunen T, Kantola J, Abou Elseoud A, et al. (2014) Infra-slow EEG fluctuations are correlated with resting-state network dynamics in fMRI. J Neurosci 34(2): 356-62.

[34] Huang CC, Rolls ET, Feng J, et al. (2022) An extended Human Connectome Project multimodal parcellation atlas of the human cortex and subcortical areas. Brain Struct Funct 227(3): 763-78.

[35] Huth AG, De Heer WA, Griffiths TL, et al. (2016) Natural speech reveals the semantic maps that tile human cerebral cortex. Nature 532(7600): 453-8.

[36] Joliot M, Tzourio-Mazoyer N, Mazoyer B (2016) Intra-hemispheric intrinsic connectivity asymmetry and its relationships with handedness and language lateralization. Neuropsychologia 93: 437-47.

[37] Jung-Beeman M, Bowden EM, Haberman J, et al. (2004) Neural activity when people solve verbal problems with insight. PLoS Biol 2(4): e97.

[38] Kansaku K (2000) Sex differences in lateralization revealed in the posterior language areas. Cereb Cortex 10(9): 866-72.

[39] Kimura D (1992) Cognitive function: sex differences and hormonal influence. Neuroscience year: supplement 2: 41-3.

[40] Kucyi A, Tambini A, Sadaghiani S, et al. (2018) Spontaneous cognitive processes and the behavioral validation of time-varying brain connectivity. Network Neurosci 2(4): 397-417.

[41] Labache L, Ge T, Yeo BT, et al. (2023) Language network lateralization is reflected throughout the macroscale functional organization of cortex. Nat Commun 14(1): 3405.

[42] Landis JR, Koch GG (1977) An application of hierarchical kappa-type statistics in the assessment of majority agreement among multiple observers. Biometrics 33: 363-74.

[43] Lazard DS, Collette JL, Perrot X (2012) Speech processing: from peripheral to hemispheric asymmetry of the auditory system. Laryngoscope 122(1): 167-73.

[44] Levy J (1969) Possible basis for the evolution of lateral specialization of the human brain. Nature 224: 614-615.

[45] Li S, Zhao Z, Hu R, et al. , (2018) Analogical reasoning on Chinese morphological and semantic relations. In: Proceedings of the 56th Annual Meeting of the Association for Computational Linguistics (Volume 2: Short Papers), p. 138-43. Melbourne, Australia: Association for Computational Linguistics.

[46] MacArthur J, Bowler E, Cerezo M, et al. (2017) The new NHGRI-EBI Catalog of published genome-wide association studies (GWAS Catalog). Nucleic Acids Res 45(D1): D896-901.

[47] Makuuchi M, Friederici AD (2013) Hierarchical functional connectivity between the core language system and the working memory system. Cortex 49(9): 2416-23.

[48] Maney DL (2016) Perils and pitfalls of reporting sex differences. Phil Trans R Soc B 371(1688): 20150119.

[49] McAvoy M, Mitra A, Coalson RS, et al. (2015) Unmasking language lateralization in human brain intrinsic activity. Cereb Cortex 26(4): 1733-46.

[50] Nielsen F (2016) Introduction to HPC with MPI for Data Science. Cham: Springer.

[51] Novick JM, Trueswell JC, Thompson-Schill SL (2010) Broca’s area and language processing: evidence for the cognitive control connection. Language Linguist Compass 4(10): 906-24.

[52] Olulade OA, Seydell-Greenwald A, Chambers CE, et al. (2020) The neural basis of language development: changes in lateralization over age. Proc Natl Acad Sci USA 117(38): 23477-83.

[53] Packheiser J, Schmitz J, Arning L, et al. (2020) A large-scale estimate on the relationship between language and motor lateralization. Sci Rep 10(1): 13027.

[54] Peng X, Liu Q, Hubbard CS, et al. (2023) Robust dynamic brain coactivation states estimated in individuals. Sci Adv 9(3): eabq8566.

[55] Pinheiro JC, Bates DM (1996) Unconstrained parametrizations for variance-covariance matrices. Stat Comput 6 (3): 289-96.

[56] Pliatsikas C (2020) Understanding structural plasticity in the bilingual brain: the Dynamic Restructuring Model. Bilingualism 23(2): 459-71.

[57] Price CJ (2012) A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading. Neuroimage 62(2): 816-47.

[58] Quackenbush J (2002) Microarray data normalization and transformation. Nat Genet 32(4): 496-501.

[59] Rousseeuw PJ (1987) Silhouettes: a graphical aid to the interpretation and validation of cluster analysis. J Comput Appl Math 20: 53-65.

[60] Ryali S, Supekar K, Chen T, et al. (2016) Temporal dynamics and developmental maturation of salience, default and central-executive network interactions revealed by variational Bayes hidden Markov modeling. PLoS Comput Biol 12(12): e1005138.

[61] Shaywitz BA, Shaywltz SE, Pugh KR, et al. (1995) Sex differences in the functional organization of the brain for language. Nature 373(6515): 607-9.

[62] Stoyanov Z, Decheva L, Pashalieva I, et al. (2012) Brain asymmetry, immunity, handedness. Central Eur J Med 7: 1-8.

[63] Vallortigara G, Chiandetti C, Sovrano VA (2011) Brain asymmetry (animal). Wiley Interdisciplinary Reviews: Cognitive Science 2(2): 146-57.

[64] Verhelst H, Dhollander T, Gerrits R, et al. (2021) Fibre-specific laterality of white matter in left and right language dominant people. Neuroimage 230: 117812.

[65] Watanabe H, Fitting S, Hussain MZ, et al. (2015) Asymmetry of the endogenous opioid system in the human anterior cingulate: a putative molecular basis for lateralization of emotions and pain. Cereb Cortex 25(1): 97-108.

[66] Watanabe K, Taskesen E, Van Bochoven A, et al. (2017) Functional mapping and annotation of genetic associations with FUMA. Nat Commun 8(1): 1826.

[67] Wermke K, Quast A, Hesse V (2018) From melody to words: the role of sex hormones in early language development. Horm Behav 104: 206-15.

[68] Westerhausen R, Kompus K, Hugdahl K (2014) Mapping hemispheric symmetries, relative asymmetries, and absolute asymmetries underlying the auditory laterality effect. Neuroimage 84: 962-70.

[69] Wirsich J, Giraud A-L, Sadaghiani S (2020) Concurrent EEG-and fMRI-derived functional connectomes exhibit linked dynamics. Neuroimage 219: 116998.

[70] Wu X, Kong X, Vatansever D, et al. (2022) Dynamic changes in brain lateralization correlate with human cognitive performance. PLoS Biol 20(3): e3001560.

[71] Xu M, Liang X, Ou J, et al. (2020) Sex differences in functional brain networks for language. Cereb Cortex 30(3): 1528-37.

[72] Yang Y, Tam F, Graham SJ, et al. (2020) Men and women differ in the neural basis of handwriting. Hum Brain Mapp 41(10): 2642-55.

[73] Yeo BTT, Krienen FM, Eickhoff SB, et al. (2015) Functional specialization and flexibility in human association cortex. Cereb Cortex 25(10): 3654-72.

[74] Zheng B, Báez S, Su L, et al. (2020) Semantic and attentional networks in bilingual processing: fMRI connectivity signatures of translation directionality. Brain Cogn 143: 105584.

[75] Zhou Q, Zhang L, Feng J, et al. (2019) Tracking the main states of dynamic functional connectivity in resting state. Front Neurosci 13: 685.