Abstract
Writing sequences play an important role in handwriting of Chinese characters. However, little is known regarding the integral brain patterns and network mechanisms of processing Chinese character writing sequences. The present study decoded brain patterns during observing Chinese characters in motion by using multi-voxel pattern analysis, meta-analytic decoding analysis, and extended unified structural equation model. We found that perception of Chinese character writing sequence recruited brain regions not only for general motor schema processing, i.e., the right inferior frontal gyrus, shifting, and inhibition functions, i.e., the right postcentral gyrus and bilateral pre-SMA/dACC, but also for sensorimotor functions specific for writing sequences. More importantly, these brain regions formed a cooperatively top-down brain network where information was transmitted from brain regions for general motor schema processing to those specific for writing sequences. These findings not only shed light on the neural mechanisms of Chinese character writing sequences, but also extend the hierarchical control model on motor schema processing.
Similar content being viewed by others
References
Alink A, Euler F, Kriegeskorte N, Singer W, Kohler A (2012) Auditory motion direction encoding in auditory cortex and high-level visual cortex. Hum Brain Mapp 33(4):969–978. https://doi.org/10.1002/hbm.21263
Aron AR, Robbins TW, Poldrack RA (2014) Inhibition and the right inferior frontal cortex: one decade on. Trends Cogn Sci 18(4):177–185. https://doi.org/10.1016/j.tics.2013.12.003
Ashe J, Lungu OV, Basford AT, Lu X (2006) Cortical control of motor sequences. Current Opinions in Neurobiology 16(2):213–221. https://doi.org/10.1016/j.conb.2006.03.008
Badre D (2008) Cognitive control, hierarchy, and the rostro-caudal organization of the frontal lobes. Trends Cogn Sci 12(5):193–200. https://doi.org/10.1016/j.tics.2008.02.004
Badre D, Nee DE (2018) Frontal cortex and the hierarchical control of behavior. Trends Cogn Sci 22(2):170–188. https://doi.org/10.1016/j.tics.2017.11.005
Badre D, Wagner AD (2004) Selection, integration, and conflict monitoring: assessing the nature and generality of prefrontal cognitive control mechanisms. Neuron 41:473–487
Badre D, Kayser AS, D’Esposito M (2010) Frontal cortex and the discovery of abstract action rules. Neuron 66(2):315–326. https://doi.org/10.1016/j.neuron.2010.03.025
Baldassano C, Hasson U, Norman KA (2018) Representation of real-world event schemas during narrative perception. J Neurosci 38(45):9689–9699. https://doi.org/10.1523/JNEUROSCI.0251-18.2018
Bellucci G, Molter F, Park SQ (2019) Neural representations of honesty predict future trust behavior. Nat Commun 10(1):5184. https://doi.org/10.1038/s41467-019-13261-8
Bergmann HC, Rijpkema M, Fernandez G, Kessels RP (2012) Distinct neural correlates of associative working memory and long-term memory encoding in the medial temporal lobe. Neuroimage 63(2):989–997. https://doi.org/10.1016/j.neuroimage.2012.03.047
Bolger DJ, Perfetti CA, Schneider W (2005) Cross-cultural effect on the brain revisited: universal structures plus writing system variation. Hum Brain Mapp 25(1):92–104. https://doi.org/10.1002/hbm.20124
Botvinick MM, Cohen JD, Carter CS (2004) Conflict monitoring and anterior cingulate cortex: an update. Trends Cogn Sci 8(12):539–546. https://doi.org/10.1016/j.tics.2004.10.003
Braun U, Schafer A, Walter H, Erk S, Romanczuk-Seiferth N, Haddad L, Schweiger JI, Grimm O, Heinz A, Tost H, Meyer-Lindenberg A, Bassett DS (2015) Dynamic reconfiguration of frontal brain networks during executive cognition in humans. Proc Natl Acad Sci USA 112(37):11678–11683. https://doi.org/10.1073/pnas.1422487112
Bubic A, von Cramon DY, Schubotz RI (2009) Motor foundations of higher cognition: similarities and differences in processing regular and violated perceptual sequences of different specificity. Eur J Neurosci 30(12):2407–2414. https://doi.org/10.1111/j.1460-9568.2009.07030.x
Calvo-Merino B, Grezes J, Glaser DE, Passingham RE, Haggard P (2006) Seeing or doing? Influence of visual and motor familiarity in action observation. Curr Biol 16(19):1905–1910. https://doi.org/10.1016/j.cub.2006.07.065
Cao F, Vu M, Chan DH, Lawrence JM, Harris LN, Guan Q, Xu Y, Perfetti CA (2013) Writing affects the brain network of reading in Chinese: a functional magnetic resonance imaging study. Hum Brain Mapp 34(7):1670–1684. https://doi.org/10.1002/hbm.22017
Chatham CH, Claus ED, Kim A, Curran T, Banich MT, Munakata Y (2012) Cognitive control reflects context monitoring, not motoric stopping, in response inhibition. PLoS ONE 7(2):e31546. https://doi.org/10.1371/journal.pone.0031546
Chen HY, Chang EC, Chen SHY, Lin YC, Wu DH (2016) Functional and anatomical dissociation between the orthographic lexicon and the orthographic buffer revealed in reading and writing Chinese characters by fMRI. Neuroimage 129:105–116. https://doi.org/10.1016/j.neuroimage.2016.01.009
Chow TE, Westphal AJ, Rissman J (2018) Multi-voxel pattern classification differentiates personally experienced event memories from secondhand event knowledge. Neuroimage 176:110–123. https://doi.org/10.1016/j.neuroimage.2018.04.024
Cooper RP (2019) Action production and event perception as routine sequential behaviors. Top Cogn Sci. https://doi.org/10.1111/tops.12462
Cross ES, Stadler W, Parkinson J, Schutz-Bosbach S, Prinz W (2011) The influence of visual training on predicting complex action sequences. Hum Brain Mapp 34(2):467–486. https://doi.org/10.1002/hbm.21450
Davis T, LaRocque KF, Mumford JA, Norman KA, Wagner AD, Poldrack RA (2014) What do differences between multi-voxel and univariate analysis mean? How subject-, voxel-, and trial-level variance impact fMRI analysis. Neuroimage 97:271–283. https://doi.org/10.1016/j.neuroimage.2014.04.037
Desmurget M, Sirigu A (2012) Conscious motor intention emerges in the inferior parietal lobule. Curr Opin Neurobiol 22(6):1004–1011. https://doi.org/10.1016/j.conb.2012.06.006
Duque J, Olivier E, Rushworth M (2013) Top-down inhibitory control exerted by the medial frontal cortex during action selection under conflict. J Cogn Neurosci 25(10):1634–1648. https://doi.org/10.1162/jocn_a_00421
Eichenbaum H, Lipton PA (2008) Towards a functional organization of the medial temporal lobe memory system: role of the parahippocampal and medial entorhinal cortical areas. Hippocampus 18(12):1314–1324. https://doi.org/10.1002/hipo.20500
Eichenbaum H, Yonelinas AP, Ranganath C (2007) The medial temporal lobe and recognition memory. Annu Rev Neurosci 30:123–152. https://doi.org/10.1146/annurev.neuro.30.051606.094328
Erika-Florence M, Leech R, Hampshire A (2014) A functional network perspective on response inhibition and attentional control. Nat Commun 5:4073. https://doi.org/10.1038/ncomms5073
Gao X, Yu H, Saez I, Blue PR, Zhu L, Hsu M, Zhou X (2018) Distinguishing neural correlates of context-dependent advantageous- and disadvantageous-inequity aversion. Proc Natl Acad Sci USA 115(33):E7680–E7689. https://doi.org/10.1073/pnas.1802523115
Gates KM, Molenaar PC, Hillary FG, Slobounov S (2011) Extended unified SEM approach for modeling event-related fMRI data. Neuroimage 54(2):1151–1158. https://doi.org/10.1016/j.neuroimage.2010.08.051
Gehring WJ, Knight RT (2000) Prefrontal–cingulate interactions in action monitoring. Nat Neurosci 3(5):516–520
Giovanni FBdA (1994) Order of strokes writing as a cue for retrieval in reading Chinese characters. Eur J Cogn Psychol 6(4):337–355. https://doi.org/10.1080/09541449408406519
Grafton ST, Hamilton AF (2007) Evidence for a distributed hierarchy of action representation in the brain. Hum Mov Sci 26(4):590–616. https://doi.org/10.1016/j.humov.2007.05.009
Hampshire A, Chamberlain SR, Monti MM, Duncan J, Owen AM (2010) The role of the right inferior frontal gyrus: inhibition and attentional control. Neuroimage 50(3):1313–1319. https://doi.org/10.1016/j.neuroimage.2009.12.109
Haynes JD, Rees G (2006) Decoding mental states from brain activity in humans. Nat Rev Neurosci 7(7):523–534. https://doi.org/10.1038/nrn1931
Hodges JR (1991) Pure apraxic agraphia with recovery after drainage of a left frontal cyst. Cortex 27(3):469–473. https://doi.org/10.1016/s0010-9452(13)80043-3
Huang J-T, Wang M-Y (1992) From unit to gestalt: perceptual dynamics in recognizing chinese characters. In: Chen H-C, Tzeng OJL (eds) Language processing in Chinese. Advances in psychology. Elsevier, pp 3–35. https://doi.org/10.1016/s0166-4115(08)61885-3
Igelstrom KM, Graziano MSA (2017) The inferior parietal lobule and temporoparietal junction: a network perspective. Neuropsychologia 105:70–83. https://doi.org/10.1016/j.neuropsychologia.2017.01.001
Jeneson A, Squire LR (2012) Working memory, long-term memory, and medial temporal lobe function. Learn Mem 19(1):15–25. https://doi.org/10.1101/lm.024018.111
Kang C, Ma F, Li S, Kroll JF, Guo T (2020) Domain-general inhibition ability predicts the intensity of inhibition on non-target language in bilingual word production: an ERP study. Biling Lang Cogn. https://doi.org/10.1017/s1366728920000085
Keller C, Meister IG (2014) Agraphia caused by an infarction in Exner’s area. J Clin Neurosci 21(1):172–173. https://doi.org/10.1016/j.jocn.2013.01.014
Kim J, Zhu W, Chang L, Bentler PM, Ernst T (2007) Unified structural equation modeling approach for the analysis of multisubject, multivariate functional MRI data. Hum Brain Mapp 28(2):85–93. https://doi.org/10.1002/hbm.20259
Kim YK, Park E, Lee A, Im CH, Kim YH (2018) Changes in network connectivity during motor imagery and execution. PLoS ONE 13(1):e0190715. https://doi.org/10.1371/journal.pone.0190715
Koechlin E, Jubault T (2006) Broca’s area and the hierarchical organization of human behavior. Neuron 50(6):963–974. https://doi.org/10.1016/j.neuron.2006.05.017
Kriegeskorte N (2011) Pattern-information analysis: from stimulus decoding to computational-model testing. Neuroimage 56(2):411–421. https://doi.org/10.1016/j.neuroimage.2011.01.061
Kriegeskorte N, Kievit RA (2013) Representational geometry: integrating cognition, computation, and the brain. Trends Cogn Sci 17(8):401–412. https://doi.org/10.1016/j.tics.2013.06.007
Kriegeskorte N, Goebel R, Bandettini P (2006) Information-based functional brain mapping. Proc Natl Acad Sci USA 103(10):3863–3868
LaConte S, Strother S, Cherkassky V, Anderson J, Hu X (2005) Support vector machines for temporal classification of block design fMRI data. Neuroimage 26(2):317–329. https://doi.org/10.1016/j.neuroimage.2005.01.048
Lagarrigue A, Longcamp M, Anton JL, Nazarian B, Prevot L, Velay JL, Cao F, Frenck-Mestre C (2017) Activation of writing-specific brain regions when reading Chinese as a second language. Effects of training modality and transfer to novel characters. Neuropsychologia 97:83–97. https://doi.org/10.1016/j.neuropsychologia.2017.01.026
Latora V, Marchiori M (2001) Efficient behavior of small-world networks. Phys Rev Lett 87(19):198701. https://doi.org/10.1103/PhysRevLett.87.198701
Law N, Ki WW, Chung ALS, Ko PY, Lam HC (1998a) Children’s stroke sequence errors in writing Chinese characters. Read Writ 10:267–292
Law N, Ki WW, Chung ALS, Ko PY, Lam HC (1998b) Children’s stroke sequence errors in writing Chinese characters. Read Writ Interdiscip J 10:267–292
Linke A, Roach-Fox E, Vriezen E, Prasad AN, Cusack R (2018) Altered activation and functional asymmetry of exner’s area but not the visual word form area in a child with sudden-onset, persistent mirror writing. Neuropsychologia 117:322–331. https://doi.org/10.1016/j.neuropsychologia.2018.05.022
Lo L-Y, Yeung P-S, Ho CS-H, ChanChung DW-OK (2016) The role of stroke knowledge in reading and spelling in Chinese. J Res Read 39(4):367–388. https://doi.org/10.1111/1467-9817.12058
Luck D, Danion JM, Marrer C, Pham BT, Gounot D, Foucher J (2010) The right parahippocampal gyrus contributes to the formation and maintenance of bound information in working memory. Brain Cogn 72(2):255–263. https://doi.org/10.1016/j.bandc.2009.09.009
Ma F, Xu J, Li X, Wang P, Wang B, Liu B (2018) Investigating the neural basis of basic human movement perception using multi-voxel pattern analysis. Exp Brain Res 236(3):907–918. https://doi.org/10.1007/s00221-018-5175-9
Maeda K, Ogawa N (2014) Agraphia for Kana predominance induced by a cerebral infarction involving the left middle frontal gyrus (Exner’s Area). Austin J Cerebrovasc Dis Stroke 1(4):1016
Molnar-Szakacs I, Kaplan J, Greenfield PM, Iacoboni M (2006) Observing complex action sequences: the role of the fronto-parietal mirror neuron system. Neuroimage 33(3):923–935. https://doi.org/10.1016/j.neuroimage.2006.07.035
Nakamura K, Kuo WJ, Pegado F, Cohen L, Tzeng OJ, Dehaene S (2012) Universal brain systems for recognizing word shapes and handwriting gestures during reading. Proc Natl Acad Sci USA 109(50):20762–20767. https://doi.org/10.1073/pnas.1217749109
Norman KA, Polyn SM, Detre GJ, Haxby JV (2006) Beyond mind-reading: multi-voxel pattern analysis of fMRI data. Trends Cogn Sci 10(9):424–430. https://doi.org/10.1016/j.tics.2006.07.005
Obeso I, Robles N, Marron EM, Redolar-Ripoll D (2013) Dissociating the role of the pre-SMA in response inhibition and switching: a combined online and offline TMS approach. Front Hum Neurosci 7:150. https://doi.org/10.3389/fnhum.2013.00150
Otsuki M, Soma Y, Arai T, Otsuka A, Tsuji S (1999) Pure apraxic agraphia with abnormal writing stroke sequences: report of a Japanese patient with a left superior parietal haemorrhage. J Neurol Neurosurg Psychiatry 66(2):233–237
Padmala S, Pessoa L (2010) Interactions between cognition and motivation during response inhibition. Neuropsychologia 48(2):558–565. https://doi.org/10.1016/j.neuropsychologia.2009.10.017
Pitzalis S, Sereno MI, Committeri G, Fattori P, Galati G, Tosoni A, Galletti C (2013) The human homologue of macaque area V6A. Neuroimage 82:517–530. https://doi.org/10.1016/j.neuroimage.2013.06.026
Pitzalis S, Fattori P, Galletti C (2015) The human cortical areas V6 and V6A. Vis Neurosci 32:E007. https://doi.org/10.1017/S0952523815000048
Planton S, Jucla M, Roux FE, Demonet JF (2013) The “handwriting brain”: a meta-analysis of neuroimaging studies of motor versus orthographic processes. Cortex 49(10):2772–2787. https://doi.org/10.1016/j.cortex.2013.05.011
Reineberg AE, Banich MT (2016) Functional connectivity at rest is sensitive to individual differences in executive function: a network analysis. Hum Brain Mapp 37(8):2959–2975. https://doi.org/10.1002/hbm.23219
Robin J, Moscovitch M (2017) Details, gist and schema: hippocampal–neocortical interactions underlying recent and remote episodic and spatial memory. Curr Opin Behav Sci 17:114–123. https://doi.org/10.1016/j.cobeha.2017.07.016
Rozzi S, Ferrari PF, Bonini L, Rizzolatti G, Fogassi L (2008) Functional organization of inferior parietal lobule convexity in the macaque monkey: electrophysiological characterization of motor, sensory and mirror responses and their correlation with cytoarchitectonic areas. Eur J Neurosci 28(8):1569–1588. https://doi.org/10.1111/j.1460-9568.2008.06395.x
Rubin TN, Koyejo O, Gorgolewski KJ, Jones MN, Poldrack RA, Yarkoni T (2017) Decoding brain activity using a large-scale probabilistic functional-anatomical atlas of human cognition. PLoS Comput Biol 13(10):e1005649. https://doi.org/10.1371/journal.pcbi.1005649
Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52(3):1059–1069. https://doi.org/10.1016/j.neuroimage.2009.10.003
Rubinov M, Sporns O (2011) Weight-conserving characterization of complex functional brain networks. Neuroimage 56(4):2068–2079. https://doi.org/10.1016/j.neuroimage.2011.03.069
Schmidt R (1975) A schema theory of discrete motor sckill learning. Psychol Rev 82(4):225–260
Sepulveda P, Sitaram R, Rana M, Montalba C, Tejos C, Ruiz S (2016) How feedback, motor imagery, and reward influence brain self-regulation using real-time fMRI. Hum Brain Mapp 37(9):3153–3171. https://doi.org/10.1002/hbm.23228
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. https://doi.org/10.1371/journal.pone.0025031
Spiers HJ, Maguire EA (2007) Decoding human brain activity during real-world experiences. Trends Cogn Sci 11(8):356–365. https://doi.org/10.1016/j.tics.2007.06.002
Squire LR, Wixted JT, Clark RE (2007) Recognition memory and the medial temporal lobe: a new perspective. Nat Rev Neurosci 8(11):872–883. https://doi.org/10.1038/nrn2154
Sundermann B, Pfleiderer B (2012) Functional connectivity profile of the human inferior frontal junction: involvement in a cognitive control network. BMC Neurosci 13(1):119
Takahashi E, Ohki K, Miyashita Y (2002) The role of the parahippocampal gyrus in source memory for external and internal events. NeuroReport 13(15):1951–1956
Thomas RM, De Sanctis T, Gazzola V, Keysers C (2018) Where and how our brain represents the temporal structure of observed action. Neuroimage 183:677–697. https://doi.org/10.1016/j.neuroimage.2018.08.056
Wang Z, Childress AR, Wang J, Detre JA (2007) Support vector machine learning-based fMRI data group analysis. Neuroimage 36(4):1139–1151. https://doi.org/10.1016/j.neuroimage.2007.03.072
Wang L, Uhrig L, Jarraya B, Dehaene S (2015) Representation of numerical and sequential patterns in macaque and human brains. Curr Biol 25(15):1966–1974. https://doi.org/10.1016/j.cub.2015.06.035
Ward AM, Schultz AP, Huijbers W, Van Dijk KR, Hedden T, Sperling RA (2014) The parahippocampal gyrus links the default-mode cortical network with the medial temporal lobe memory system. Hum Brain Mapp 35(3):1061–1073. https://doi.org/10.1002/hbm.22234
Wu CY, Ho MH, Chen SH (2012) A meta-analysis of fMRI studies on Chinese orthographic, phonological, and semantic processing. Neuroimage 63(1):381–391. https://doi.org/10.1016/j.neuroimage.2012.06.047
Yang Y, Zuo Z, Tam F, Graham SJ, Tao R, Wang N, Bi H-Y (2019) Brain activation and functional connectivity during Chinese writing: an fMRI study. J Neurolinguistics 51:199–211. https://doi.org/10.1016/j.jneuroling.2019.03.002
Yang Y, Tam F, Graham SJ, Sun G, Li J, Gu C, Tao R, Wang N, Bi HY, Zuo Z (2020) Men and women differ in the neural basis of handwriting. Hum Brain Mapp 41(10):2642–2655. https://doi.org/10.1002/hbm.24968
Yu H, Gong L, Qiu Y, Zhou X (2011) Seeing Chinese characters in action: an fMRI study of the perception of writing sequences. Brain Lang 119(2):60–67. https://doi.org/10.1016/j.bandl.2010.11.007
Acknowledgements
The study was supported by the National Natural Science Foundation of China (31871097) to Taomei Guo, the National Key Basic Research Program of China (2014CB846102), the Interdiscipline Research Funds of Beijing Normal University, and the Fundamental Research Funds for the Central Universities (2017XTCX04). We thank Leshan Chen for inspiring the research idea, Alex Titus for proofreading the manuscript, and three anonymous reviewers for their valuable comments. All the authors declare no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhang, Z., Yuan, Q., Liu, Z. et al. The cortical organization of writing sequence: evidence from observing Chinese characters in motion. Brain Struct Funct 226, 1627–1639 (2021). https://doi.org/10.1007/s00429-021-02276-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-021-02276-x