INTRODUCTION: According to the strong version of the orthographic depth hypothesis, in languages with transparent letter-sound mappings (shallow orthographies) the reading of both familiar words and unfamiliar nonwords may be accomplished by a sublexical pathway that relies on serial grapheme-to-phoneme conversion. However, in languages such as English characterized by inconsistent letter-sound relationships (deep orthographies), word reading is mediated by a lexical-semantic pathway that relies on mappings between word-specific orthographic, semantic, and phonological representations, whereas the sublexical pathway is used primarily to read nonwords. METHODS: In this study, we used functional magnetic resonance imaging to elucidate neural substrates of reading in Czech, a language characterized by a shallo worthography. Specifically, we contrasted patterns of brain activation and connectivity during word and nonword reading to determine whether similar or different neural mechanisms are involved. Neural correlates were measured as differences in simple whole-brain voxel-wise activation, and differences in visual word form area (VWFA) task-related connectivity were computed on the group level from data of 24 young subject. Trial-to-trial reading reaction times were used as a measure of task difficulty, and these effects were subtracted from the activation and connectivity effects in order to eliminate difference in cognitive effort which is naturally higher for nonwords and may mask the true lexicality effects. RESULTS: We observed pattern of activity well described in the literature mostly derived from data of English speakers - nonword reading (as compared to word reading) activated the sublexical pathway to a greater extent whereas word reading was associated with greater activation of semantic networks. VWFA connectivity analysis also revealed stronger connectivity to a component of the sublexical pathway - left inferior frontal gyrus (IFG), for nonword compared to word reading. DISCUSSION: These converging results suggest that the brain mechanism of skilled reading in shallow orthography languages are similar to those engaged when reading in languages with a deep orthography and are supported by a universal dual-pathway neural architecture.

Applied Neuroscience Research Group Central European Institute of Technology CEITEC Masaryk University Brno Czechia

Department of Neurology University of Arizona Tucson AZ United States

Department of Telecommunications Faculty of Electrical Engineering and Communication Brno University of Technology Brno Czechia

Institute of the Czech National Corpus Charles University Prague Czechia

International Clinical Research Center ICRC St Anne's University Hospital and Faculty of Medicine Masaryk University Brno Czechia

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Ardila A., Cuetos F. (2016). Applicability of dual-route reading models to Spanish. Psicothema 28, 71–75. doi: 10.7334/psicothema2015.103, PMID: PubMed DOI

Barton M., Marecek R., Krajcovicova L., Slavicek T., Kasparek T., Zemankova P., et al. . (2019). Evaluation of different cerebrospinal fluid and white matter fMRI filtering strategies-quantifying noise removal and neural signal preservation. Hum. Brain Mapp. 40, 1114–1138. doi: 10.1002/hbm.24433, PMID: PubMed DOI PMC

Barton M., Marecek R., Rektor I., Filip P., Janousova E., Mikl M. (2015). Sensitivity of PPI analysis to differences in noise reduction strategies. J. Neurosci. Methods 253, 218–232. doi: 10.1016/j.jneumeth.2015.06.021, PMID: PubMed DOI

Binder J. R., Desai R. H., Graves W. W., Conant L. L. (2009). Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb. Cortex 19, 2767–2796. doi: 10.1093/cercor/bhp055, PMID: PubMed DOI PMC

Binder J. R., Medler D. A., Desai R., Conant L. L., Liebenthal E. (2005). Some neurophysiological constraints on models of word naming. NeuroImage 27, 677–693. doi: 10.1016/j.neuroimage.2005.04.029, PMID: PubMed DOI

Blank I. A., Fedorenko E. (2017). Domain-general brain regions do not track linguistic input as closely as language-selective regions. J. Neurosci. 37, 9999–10011. doi: 10.1523/JNEUROSCI.3642-16.2017, PMID: PubMed DOI PMC

Botthali F., Thiebaut de Schotten M., Pinel P., Poupon C., Mangin J. F., Dehaene S., et al. . (2014). Anatomical connections of the visual word form area. J. Neurosci. 34, 15402–15414. doi: 10.1523/JNEUROSCI.4918-13.2014 PubMed DOI PMC

Branco P., Seixas D., Castro S. (2020). Mapping language with resting-state functional magnetic resonance imaging: a study on the functional profile of the language network. Hum. Brain Mapp. 41, 545–560. doi: 10.1002/hbm.24821 PubMed DOI PMC

Caffarra S., Karipidis I. I., Yablonski M., Yeatman J. D. (2021). Anatomy and physiology of word-selective visual cortex: from visual features to lexical processing. Brain Struct. Funct. 226, 3051–3065. doi: 10.1007/s00429-021-02384-8, PMID: PubMed DOI PMC

Cherodath S., Singh N. C. (2015). The influence of orthographic depth on reading networks in simultaneous biliterate children. Brain Lang. 143, 42–51. doi: 10.1016/j.bandl.2015.02.001, PMID: PubMed DOI

Chyl K., Kossowski B., Wang S., Debska A., Luniewska M., Marchewka A., et al. . (2021). The brain signature of emerging reading in two contrasting languages. NeuroImage 225:117503. doi: 10.1016/j.neuroimage.2020.117503, PMID: PubMed DOI

Cohen L., Lehericy S., Chochon F., Lemer C., Rivaud S., Dehaene S. (2002). Language-specific tuning of visual cortex functional properties of the visual word form area. Brain 125, 1054–1069. doi: 10.1093/brain/awf094, PMID: PubMed DOI

Coltheart M., Rastle K., Perry C., Langdon R., Ziegler J. (2001). DRC: a dual route cascaded model of visual word recognition and reading aloud. Psychol. Rev. 108, 204–256. doi: 10.1037/0033-295X.108.1.204, PMID: PubMed DOI

Danelli L., Marelli M., Berlingeri M., Tettamanti M., Sberna M., Paulesu E., et al. . (2015). Framing effects reveal discrete lexical-semantic and sublexical procedures in reading: an fMRI study. Front. Psychol. 6:1328. doi: 10.3389/fpsyg.2015.01328, PMID: PubMed DOI PMC

Das T., Padakannaya P., Pugh K. R., Singh N. C. (2011). Neuroimaging reveals dual routes to reading in simultaneous proficient readers of two orthographies. NeuroImage 54, 1476–1487. doi: 10.1016/j.neuroimage.2010.09.022, PMID: PubMed DOI PMC

Dehaene S., Cohen L., Sigman M., Vinckier F. (2005). The neural code for written words: a proposal. Trends Cogn. Sci. 9, 335–341. doi: 10.1016/j.tics.2005.05.004, PMID: PubMed DOI

Difalcis M., Ferreres A., Osiadacz N., Abusamra V. (2018). Reading response latencies in Spanish: effects of lexicality and frequency. Investigaciones Sobre Lectura. 9, 50–72. doi: 10.37132/isl.v0i9.223 DOI

Dixon M. L., De la Vega A., Mills C., Andrews-Hanna J., Spreng R. N., Cole M. W., et al. . (2018). Heterogeneity within the frontoparietal control network and its relationship to the default and dorsal attention networks. Proc. Natl. Acad. Sci. U. S. A. 115, E1598–E1607. doi: 10.1073/pnas.1715766115, PMID: PubMed DOI PMC

Dosenbach N. U. F., Fair D. A., Miezin F. M., Cohen A. L., Wenger K. K., Dosenbach R. A. T., et al. . (2007). Distinct brain networks for adaptive and stable task control in humans. Proc. Natl. Acad. Sci. U. S. A. 104, 11073–11078. doi: 10.1073/pnas.0704320104, PMID: PubMed DOI PMC

Duncan J. (2010). The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour. Trends Cogn. Sci. 14, 172–179. doi: 10.1016/j.tics.2010.01.004, PMID: PubMed DOI

Ekstrand C., Neudorf J., Kress S., Borowsky R. (2019). How words and space collide: lexical and sublexical reading are reliant on separable reflexive and voluntary attention regions in hybrid tasks. Cortex 121, 104–116. doi: 10.1016/j.cortex.2019.08.006, PMID: PubMed DOI

Fedorenko E., Duncan J., Kanwisher N. (2013). Broad domain generality in focal regions of frontal and parietal cortex. Proc. Natl. Acad. Sci. U. S. A. 110, 16616–16621. doi: 10.1073/pnas.1315235110, PMID: PubMed DOI PMC

Fiez J. A., Tranel D., Seager-Frerichs D., Damasio H. (2006). Specific reading and phonological processing deficits are associated with damage to the left frontal operculum. Cortex 42, 624–643. doi: 10.1016/S0010-9452(08)70399-X, PMID: PubMed DOI

Fischer-Baum S., Bruggemann D., Gallego I. F., Li D. S. P., Tamez E. R. (2017). Decoding levels of representation in reading: a representational similarity approach. Cortex 90, 88–102. doi: 10.1016/j.cortex.2017.02.017, PMID: PubMed DOI

Frost R. (2005). “Orthographic systems and skilled word recognition processes in Reading” in The Science of Reading: A Handbook. eds. Snowling M. J., Hulme C. (Blackwell Publishing; ), 272–295.

Gao W., Lin W. (2012). Frontal parietal control network regulates the anti-correlated default and dorsal attention networks. Hum. Brain Mapp. 33, 192–202. doi: 10.1002/hbm.21204, PMID: PubMed DOI PMC

Ghuman A. S., Fiez J. A. (2018). Parcellating the structure and function of the reading circuit. Proc. Natl. Acad. Sci. U. S. A. 115, 10542–10544. doi: 10.1073/pnas.1814648115, PMID: PubMed DOI PMC

Glezer L. S., Eden G., Jiang X., Luetje M., Napoliello E., Kima J., et al. . (2016). Uncovering phonological and orthographic selectivity across the reading network using fMRI-RA. NeuroImage 138, 248–256. doi: 10.1016/j.neuroimage.2016.05.072, PMID: PubMed DOI PMC

Glezer L. S., Jiang X., Riesenhuber M. (2009). Evidence for highly selective neuronal tuning to whole words in the “visual word form area”. Neuron 62, 199–204. doi: 10.1016/j.neuron.2009.03.017, PMID: PubMed DOI PMC

Glezer L. S., Riesenhuber M. (2013). Individual variability in location impacts orthographic selectivity in the “visual word form area”. J. Neurosci. 33, 11221–11226. doi: 10.1523/JNEUROSCI.5002-12.2013, PMID: PubMed DOI PMC

Glover G. H., Li T. Q., Ress D. (2000). Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn. Reson. Med. 44, 162–167. doi: 10.1002/1522-2594(200007)44:1<162::AID-MRM23>3.0.CO;2-E, PMID: PubMed DOI

Grainger J., Ziegler J. C. (2011). A dual-route approach to orthographic processing. Front. Psychol. 2:54. doi: 10.3389/fpsyg.2011.00054, PMID: PubMed DOI PMC

Ihnen S. K. Z., Petersen S. E., Schlaggar B. L. (2015). Separable roles for Attentional control sub-Systems in Reading Tasks: a combined behavioral and fMRI study. Cereb. Cortex 25, 1198–1218. doi: 10.1093/cercor/bht313, PMID: PubMed DOI PMC

Ischebeck A., Indefrey P., Usui N., Nose I., Hellwig F., Taira M. (2004). Reading in a regular orthography: an fMRI study investigating the role of visual familiarity. J. Cogn. Neurosci. 16, 727–741. doi: 10.1162/089892904970708, PMID: PubMed DOI

Kapnoula E. C., Protopapas A., Saunders S. J., Coltheart M. (2017). Lexical and sublexical effects on visual word recognition in Greek: comparing human behavior to the dual route cascaded model. Lang. Cogn. Neurosci. 32, 1290–1304. doi: 10.1080/23273798.2017.1355059 DOI

Katz L., Frost R. (1992). “Chapter 4 the Reading process is different for different orthographies: the orthographic depth hypothesis,” in Orthography, Phonology, Morphology, and Meaning. Amsterdam: Elsevier North Holland Press, 67–84.

Khachouf O. T., Chen G., Duzzi D., Porro C. A., Pagnoni G. (2017). Voluntary modulation of mental effort investment: an fMRI study. Sci. Rep. 7:17191. doi: 10.1038/s41598-017-17519-3, PMID: PubMed DOI PMC

Lerma-Usabiaga G., Carreiras M., Paz-Alonso P. M. (2018). Converging evidence for functional and structural segregation within the left ventral occipitotemporal cortex in reading. Proc. Natl. Acad. Sci. U. S. A. 115, E9981–E9990. doi: 10.1073/pnas.1803003115, PMID: PubMed DOI PMC

Li Y. O., Adali T., Calhoun V. D. (2007). Estimating the number of independent components for functional magnetic resonance imaging data. Hum. Brain Mapp. 28, 1251–1266. doi: 10.1002/hbm.20359, PMID: PubMed DOI PMC

Majerus S., Peters F., Bouffier M., Cowan N., Phillips C. (2018). The dorsal attention network reflects both encoding load and top-down control during working memory. J. Cogn. Neurosci. 30, 144–159. doi: 10.1162/jocn_a_01195, PMID: PubMed DOI

Malik-Moraleda S., Ayyash D., Gallee J., Affourtit J., Hoffmann M., Mineroff Z., et al. . (2022). An investigation across 45 languages and 12 language families reveals a universal language network. Nat. Neurosci. 25, 1014–1019. doi: 10.1038/s41593-022-01114-5, PMID: PubMed DOI PMC

Marcolini S., Burani C., Colombo L. (2009). Lexical effects on children’s pseudoword reading in a transparent orthography. Read. Writ. 22, 531–544. doi: 10.1007/s11145-008-9123-0 DOI

Marinelli C. V., Romani C., Burani C., McGowan V. A., Zoccolotti P. (2016). Costs and benefits of orthographic inconsistency in reading: evidence from a cross-linguistic comparison. PLoS One 11:e0157457. doi: 10.1371/journal.pone.0157457, PMID: PubMed DOI PMC

McLaren D. G., Ries M. L., Xu G., Johnson S. C. (2012). A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. NeuroImage 61, 1277–1286. doi: 10.1016/j.neuroimage.2012.03.068, PMID: PubMed DOI PMC

Mei L. L., Xue G., Lu Z. L., He Q. H., Wei M., Zhang M. X., et al. . (2015). Native language experience shapes neural basis of addressed and assembled phonologies. NeuroImage 114, 38–48. doi: 10.1016/j.neuroimage.2015.03.075, PMID: PubMed DOI PMC

Mineroff Z., Blank I. A., Mahowald K., Fedorenko E. (2018). A robust dissociation among the language, multiple demand, and default mode networks: evidence from inter-region correlations in effect size. Neuropsychologia 119, 501–511. doi: 10.1016/j.neuropsychologia.2018.09.011, PMID: PubMed DOI PMC

Ojemann J. G., Akbudak E., Snyder A. Z., McKinstry R. C., Raichle M. E., Conturo T. E. (1997). Anatomic localization and quantitative analysis of gradient refocused echo-planar fMRI susceptibility artifacts. NeuroImage 6, 156–167. doi: 10.1006/nimg.1997.0289, PMID: PubMed DOI

Oliver M., Carreiras M., Paz-Alonso P. M. (2017). Functional dynamics of dorsal and ventral Reading networks in bilinguals. Cereb. Cortex 27, 5431–5443. doi: 10.1093/cercor/bhw310, PMID: PubMed DOI

O’Reilly J. X., Woolrich M. W., Behrens T. E. J., Smith S. M., Johansen-Berg H. (2012). Tools of the trade: psychophysiological interactions and functional connectivity. Soc. Cogn. Affect. Neurosci. 7, 604–609. doi: 10.1093/scan/nss055, PMID: PubMed DOI PMC

Pagliuca G., Arduino L. S., Barca L., Burani C. (2008). Fully transparent orthography, yet lexical reading aloud: the lexicality effect in Italian. Lang. Cogn. Process. 23, 422–433. doi: 10.1080/01690960701626036 DOI

Paulesu E., McCrory E., Fazio F., Menoncello L., Brunswick N., Cappa S. F., et al. . (2000). A cultural effect on brain function. Nat. Neurosci. 3, 91–96. doi: 10.1038/71163 PubMed DOI

Price C. J. (2012). A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading. NeuroImage 62, 816–847. doi: 10.1016/j.neuroimage.2012.04.062, PMID: PubMed DOI PMC

Protopapas A., Orfanidou E., Taylor J. S. H., Karavasilis E., Kapnoula E. C., Panagiotaropoulou G., et al. . (2016). Evaluating cognitive models of visual word recognition using fMRI: effects of lexical and sublexical variables. NeuroImage 128, 328–341. doi: 10.1016/j.neuroimage.2016.01.013, PMID: PubMed DOI

Purcell J. J., Jiang X., Eden G. F. (2017). Shared orthographic neuronal representations for spelling and reading. NeuroImage 147, 554–567. doi: 10.1016/j.neuroimage.2016.12.054, PMID: PubMed DOI PMC

Raichle M. E., Snyder A. Z. (2007). A default mode of brain function: a brief history of an evolving idea. NeuroImage 37, 1083–1090. doi: 10.1016/j.neuroimage.2007.02.041, PMID: PubMed DOI

Raman I., Baluch B., Sneddon P. (1996). What is the cognitive System’s preferred route for deriving phonology from print? Eur. Psychol. 1, 221–227. doi: 10.1027/1016-9040.1.3.221 DOI

Rapcsak S. Z., Beeson P. M. (2015). “Neuroanatomical correlates of spelling and writing,” in Handbook of Adult Language Disorders. 2nd Edn, ed. Hillis A. E. (Taylor & Francis Ltd; ), 87–116.

Richlan F., Kronbichler M., Wimmer H. (2009). Functional abnormalities in the dyslexic brain: a quantitative meta-analysis of neuroimaging studies. Hum. Brain Mapp. 30, 3299–3308. doi: 10.1002/hbm.20752, PMID: PubMed DOI PMC

Ripamonti E., Luzzatti C., Zoccolotti P., Traficante D. (2018). Word and pseudoword superiority effects: evidence from a shallow orthography language. Q. J. Exp. Psychol. 71, 1911–1920. doi: 10.1080/17470218.2017.1363791, PMID: PubMed DOI

Rueckl J. G., Paz-Alonso P. M., Molfese P. J., Kuo W. J., Bick A., Frost S. J., et al. . (2015). Universal brain signature of proficient reading: evidence from four contrasting languages. Proc. Natl. Acad. Sci. U. S. A. 112, 15510–15515. doi: 10.1073/pnas.1509321112, PMID: PubMed DOI PMC

Saygin Z. M., Osher D. E., Norton E. S., Youssoufian D. A., Beach S. D., Feather J., et al. . (2016). Connectivity precedes function in the development of the visual word form area. Nat. Neurosci. 19, 1250–1255. doi: 10.1038/nn.4354, PMID: PubMed DOI PMC

Schmalz X., Marinus E., Coltheart M., Castles A. (2015). Getting to the bottom of orthographic depth. Psychon. Bull. Rev. 22, 1614–1629. doi: 10.3758/s13423-015-0835-2, PMID: PubMed DOI

Schuster S., Hawelka S., Hutzler F., Kronbichler M., Richlan F. (2016). Words in context: the effects of length, frequency, and predictability on brain responses during natural Reading. Cereb. Cortex 26, 3889–3904. doi: 10.1093/cercor/bhw184, PMID: PubMed DOI PMC

Sebastian R., Gomez Y., Leigh R., Davis C., Newhart M., Hillis A. E. (2014). The roles of occipitotemporal cortex in reading, spelling, and naming. Cogn. Neuropsychol. 31, 511–528. doi: 10.1080/02643294.2014.884060, PMID: PubMed DOI PMC

Seidenberg M. S. (2011). “Reading in different writing systems: one architecture, multiple solutions,” in Dyslexia across languages: Orthography and the brain–gene–behavior link. eds. McCardle P., Miller B., Lee J. R., Tzeng O. J. L. (Baltimore, MD, US: Paul H Brookes Publishing; ), 146–168.

Share D. L. (2008). On the anglocentricities of current reading research and practice: the perils of overreliance on an "outlier" orthography. Psychol. Bull. 134, 584–615. doi: 10.1037/0033-2909.134.4.584, PMID: PubMed DOI

Stevens W. D., Kravitz D. J., Peng C. S., Tessler M. H., Martin A. (2017). Privileged functional connectivity between the visual word form area and the language system. J. Neurosci. 37, 5288–5297. doi: 10.1523/JNEUROSCI.0138-17.2017, PMID: PubMed DOI PMC

Taylor J. S. H., Duff F. J., Woollams A. M., Monaghan P., Ricketts J. (2015). How word meaning influences word Reading. Curr. Dir. Psychol. Sci. 24, 322–328. doi: 10.1177/0963721415574980 DOI

Taylor J. S. H., Rastle K., Davis M. H. (2013). Can cognitive models explain brain activation during word and Pseudoword Reading? A meta-analysis of 36 neuroimaging studies. Psychol. Bull. 139, 766–791. doi: 10.1037/a0030266, PMID: PubMed DOI

Taylor J. S. H., Rastle K., Davis M. H. (2014). Interpreting response time effects in functional imaging studies. NeuroImage 99, 419–433. doi: 10.1016/j.neuroimage.2014.05.073, PMID: PubMed DOI PMC

Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., et al. . (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15, 273–289. doi: 10.1006/nimg.2001.0978, PMID: PubMed DOI

Vatansever D., Menon D. K., Stamatakis E. A. (2017). Default mode contributions to automated information processing. Proc. Natl. Acad. Sci. U. S. A. 114, 12821–12826. doi: 10.1073/pnas.1710521114, PMID: PubMed DOI PMC

Visser M., Jefferies E., Ralph M. A. L. (2010). Semantic processing in the anterior temporal lobes: a meta-analysis of the functional neuroimaging literature. J. Cogn. Neurosci. 22, 1083–1094. doi: 10.1162/jocn.2009.21309, PMID: PubMed DOI

Woollams A. M., Halai A., Lambon Ralph M. A. (2018). Mapping the intersection of language and reading: the neural bases of the primary systems hypothesis. Brain Struct. Funct. 223, 3769–3786. doi: 10.1007/s00429-018-1716-z, PMID: PubMed DOI

Zhang G. Y., Hung J. Y., Lin N. (2016). Coexistence of the social semantic effect and non-semantic effect in the default mode network. Brain Struct. Funct. 221:3843. doi: 10.1007/s00429-016-1236-7, PMID: PubMed DOI