How does literacy break mirror invariance in the visual system?
Identifieur interne : 003167 ( Ncbi/Merge ); précédent : 003166; suivant : 003168How does literacy break mirror invariance in the visual system?
Auteurs : Felipe Pegado [Belgique] ; Kimihiro Nakamura [Japon] ; Thomas Hannagan [France]Source :
- Frontiers in Psychology [ 1664-1078 ] ; 2014.
Url:
DOI: 10.3389/fpsyg.2014.00703
PubMed: 25071669
PubMed Central: 4091125
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">How does literacy break mirror invariance in the visual system?</title><author><name sortKey="Pegado, Felipe" sort="Pegado, Felipe" uniqKey="Pegado F" first="Felipe" last="Pegado">Felipe Pegado</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Laboratory of Biological Psychology, Department of Psychology and Educational Sciences, KU Leuven University</institution><country>Leuven, Belgium</country></nlm:aff><country xml:lang="fr">Belgique</country><wicri:regionArea></wicri:regionArea><wicri:regionArea># see nlm:aff region in country</wicri:regionArea></affiliation></author><author><name sortKey="Nakamura, Kimihiro" sort="Nakamura, Kimihiro" uniqKey="Nakamura K" first="Kimihiro" last="Nakamura">Kimihiro Nakamura</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>Human Brain Research Center, Graduate School of Medicine, Kyoto University</institution><country>Kyoto, Japan</country></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea></wicri:regionArea><wicri:regionArea># see nlm:aff region in country</wicri:regionArea></affiliation></author><author><name sortKey="Hannagan, Thomas" sort="Hannagan, Thomas" uniqKey="Hannagan T" first="Thomas" last="Hannagan">Thomas Hannagan</name><affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Laboratoire de Psychologie Cognitive, Fédération de Recherche 3C, Centre National de la Recherche Scientifique, Aix-Marseille University</institution><country>Marseille, France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea></wicri:regionArea><wicri:regionArea># see nlm:aff region in country</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">25071669</idno><idno type="pmc">4091125</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4091125</idno><idno type="RBID">PMC:4091125</idno><idno type="doi">10.3389/fpsyg.2014.00703</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000D30</idno><idno type="wicri:Area/Pmc/Curation">000D30</idno><idno type="wicri:Area/Pmc/Checkpoint">000C01</idno><idno type="wicri:Area/Ncbi/Merge">003167</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">How does literacy break mirror invariance in the visual system?</title><author><name sortKey="Pegado, Felipe" sort="Pegado, Felipe" uniqKey="Pegado F" first="Felipe" last="Pegado">Felipe Pegado</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Laboratory of Biological Psychology, Department of Psychology and Educational Sciences, KU Leuven University</institution><country>Leuven, Belgium</country></nlm:aff><country xml:lang="fr">Belgique</country><wicri:regionArea></wicri:regionArea><wicri:regionArea># see nlm:aff region in country</wicri:regionArea></affiliation></author><author><name sortKey="Nakamura, Kimihiro" sort="Nakamura, Kimihiro" uniqKey="Nakamura K" first="Kimihiro" last="Nakamura">Kimihiro Nakamura</name><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>Human Brain Research Center, Graduate School of Medicine, Kyoto University</institution><country>Kyoto, Japan</country></nlm:aff><country xml:lang="fr">Japon</country><wicri:regionArea></wicri:regionArea><wicri:regionArea># see nlm:aff region in country</wicri:regionArea></affiliation></author><author><name sortKey="Hannagan, Thomas" sort="Hannagan, Thomas" uniqKey="Hannagan T" first="Thomas" last="Hannagan">Thomas Hannagan</name><affiliation wicri:level="1"><nlm:aff id="aff3"><institution>Laboratoire de Psychologie Cognitive, Fédération de Recherche 3C, Centre National de la Recherche Scientifique, Aix-Marseille University</institution><country>Marseille, France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea></wicri:regionArea><wicri:regionArea># see nlm:aff region in country</wicri:regionArea></affiliation></author></analytic><series><title level="j">Frontiers in Psychology</title><idno type="eISSN">1664-1078</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Bara, F" uniqKey="Bara F">F. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Psychol</journal-id><journal-id journal-id-type="iso-abbrev">Front Psychol</journal-id><journal-id journal-id-type="publisher-id">Front. Psychol.</journal-id><journal-title-group><journal-title>Frontiers in Psychology</journal-title></journal-title-group><issn pub-type="epub">1664-1078</issn><publisher><publisher-name>Frontiers Media S.A.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">25071669</article-id><article-id pub-id-type="pmc">4091125</article-id><article-id pub-id-type="doi">10.3389/fpsyg.2014.00703</article-id><article-categories><subj-group subj-group-type="heading"><subject>Psychology</subject><subj-group><subject>Opinion Article</subject></subj-group></subj-group></article-categories><title-group><article-title>How does literacy break mirror invariance in the visual system?</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Pegado</surname><given-names>Felipe</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="author-notes" rid="fn001"><sup>*</sup></xref><uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/158645"></uri></contrib><contrib contrib-type="author"><name><surname>Nakamura</surname><given-names>Kimihiro</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/125524"></uri></contrib><contrib contrib-type="author"><name><surname>Hannagan</surname><given-names>Thomas</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/31088"></uri></contrib></contrib-group><aff id="aff1"><sup>1</sup><institution>Laboratory of Biological Psychology, Department of Psychology and Educational Sciences, KU Leuven University</institution><country>Leuven, Belgium</country></aff><aff id="aff2"><sup>2</sup><institution>Human Brain Research Center, Graduate School of Medicine, Kyoto University</institution><country>Kyoto, Japan</country></aff><aff id="aff3"><sup>3</sup><institution>Laboratoire de Psychologie Cognitive, Fédération de Recherche 3C, Centre National de la Recherche Scientifique, Aix-Marseille University</institution><country>Marseille, France</country></aff><author-notes><corresp id="fn001">*Correspondence: <email xlink:type="simple">felipepegado@yahoo.com</email></corresp><fn fn-type="other" id="fn002"><p>This article was submitted to Developmental Psychology, a section of the journal Frontiers in Psychology.</p></fn><fn fn-type="edited-by"><p>Edited by: Tânia Fernandes, University of Porto, Portugal</p></fn><fn fn-type="edited-by"><p>Reviewed by: Thomas Lachmann, University of Kaiserslautern, Germany</p></fn></author-notes><pub-date pub-type="epub"><day>10</day><month>7</month><year>2014</year></pub-date><pub-date pub-type="collection"><year>2014</year></pub-date><volume>5</volume><elocation-id>703</elocation-id><history><date date-type="received"><day>08</day><month>5</month><year>2014</year></date><date date-type="accepted"><day>18</day><month>6</month><year>2014</year></date></history><permissions><copyright-statement>Copyright © 2014 Pegado, Nakamura and Hannagan.</copyright-statement><copyright-year>2014</copyright-year><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/3.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p></license></permissions><kwd-group><kwd>multisensory</kwd><kwd>multi-system</kwd><kwd>reading</kwd><kwd>writing</kwd><kwd>literacy</kwd><kwd>alphabetization</kwd><kwd>mirror invariance</kwd><kwd>mirror discrimination</kwd></kwd-group><counts><fig-count count="1"></fig-count><table-count count="0"></table-count><equation-count count="0"></equation-count><ref-count count="43"></ref-count><page-count count="5"></page-count><word-count count="3472"></word-count></counts></article-meta></front><body><p>A growing literature has been showing a profound impact of alphabetization at several levels of the visual system, including the primary visual cortex (Szwed et al., <xref rid="B42" ref-type="bibr">2014</xref>) and higher-order ventral and dorsal visual areas (Carreiras et al., <xref rid="B5" ref-type="bibr">2009</xref>; Dehaene et al., <xref rid="B10" ref-type="bibr">2010</xref>). Importantly, in typical alphabetization courses, learning to read is not isolated but instead combined with both learning to write and learning to segment the spoken language, relating all these different representations to each other. Indeed, learning to write and to pronounce the elementary sounds of language promotes additional mapping between the visual and motor systems by linking visual representations of letters and motor plans for handwriting and speech production. Thus, besides the already recognized influence of the phonological system, the potential influence from other neural systems in the functioning of the visual system seems to be relatively neglected. In this opinion paper we highlight the importance of multi-systems interplay during literacy acquisition, focusing on the question of how literacy breaks mirror invariance in the visual system. Specifically, we argue for a large contribution of top-down inputs from phonological, handwriting and articulatory representations toward the ventral visual cortex during the development of the visual word form system, which then plays a pivotal role in mirror discrimination of letters in literate individuals.</p><sec><title>How phonology affects visual representations for reading</title><p>A key aspect of alphabetization is to set in place the audio-visual mapping known as “phoneme-grapheme correspondence,” whereby elementary sounds of language (i.e., phonemes) are linked to visual representations of them (i.e., graphemes) (Frith, <xref rid="B14" ref-type="bibr">1986</xref>). This correspondence is progressively acquired and becomes automatized typically after 3–4 years of training (Nicolson et al., <xref rid="B32" ref-type="bibr">2001</xref>; Van Atteveldt et al., <xref rid="B43" ref-type="bibr">2004</xref>; Lachmann and van Leeuwen, <xref rid="B20" ref-type="bibr">2008</xref>; Dehaene et al., <xref rid="B10" ref-type="bibr">2010</xref>; Lachmann et al., in this special issue). Illiterates, who do not learn this audio-visual correspondence, are unable to show “phonological awareness” (i.e., the ability to consciously manipulate language sounds) at the phonemic level (Morais et al., <xref rid="B27" ref-type="bibr">1979</xref>; Morais and Kolinsky, <xref rid="B28" ref-type="bibr">1994</xref>), presenting different visual analytical characteristics (Lachmann et al., <xref rid="B19" ref-type="bibr">2012</xref>; Fernandes et al., <xref rid="B12" ref-type="bibr">2014</xref>). Accordingly, activations in phonological areas increases in proportion to the literacy level of participants, e.g., <italic>planum temporale</italic> responses to auditory sentences and left superior temporal sulcus responses to visual presentations of written sentences (Dehaene et al., <xref rid="B10" ref-type="bibr">2010</xref>). These results therefore suggest an important link between the visual and auditory systems created by literacy training. Indeed, the reciprocal inter-regional coupling between visual and auditory cortical areas may constitute a crucial component for fluent reading, since dyslexic children, who present slow reading, show reduced activations to speech sounds in the perisylvian language areas and ventral visual cortex including the Visual Word Form Area (VWFA) (Monzalvo et al., <xref rid="B26" ref-type="bibr">2012</xref>).</p></sec><sec><title>How writing affects visual representations for reading</title><p>In parallel, children (and adults) under alphabetization also learn to draw letters of the alphabet. Indeed, writing requires fine motor coordination of hand gestures, a process guided by online feedback from somatosensory and visual systems (Margolin, <xref rid="B25" ref-type="bibr">1984</xref>). In particular, gestures of handwriting are thought to be represented in the dorsal part of the premotor cortex, rostral to the primary motor cortex responsible for hand movements, i.e., a region first coarsely described by Exner as the “graphic motor image center” (see Roux et al., <xref rid="B39" ref-type="bibr">2010</xref> for a review). Exner's area is known to be activated when participants write letters but not when they copy pseudoletters (Longcamp et al., <xref rid="B21" ref-type="bibr">2003</xref>). Moreover, direct brain stimulation of the same region produces a specific inability to write (Roux et al., <xref rid="B40" ref-type="bibr">2009</xref>). Importantly, this region is activated simply by visual presentations of handwritten stimuli (Longcamp et al., <xref rid="B21" ref-type="bibr">2003</xref>, <xref rid="B23" ref-type="bibr">2008</xref>), even when they are presented unconsciously (Nakamura et al., <xref rid="B31" ref-type="bibr">2012</xref>). Additionally these activations take place in the premotor cortex contra-lateral to the dominant hand for writing (Longcamp et al., <xref rid="B22" ref-type="bibr">2005</xref>). These results suggest that literacy training establishes a tight functional link between the visual and motor systems for reading and writing. In fact, it has been proposed that reading and writing rely on distributed and overlapping brain regions, each showing slightly different levels of activation depending on the nature of orthography (Nakamura et al., <xref rid="B31" ref-type="bibr">2012</xref>). As for the reciprocal link between the visual and motor components of this reading network, brain-damaged patients and fMRI data from normal subjects consistently suggest that top-down activation of the posterior inferior temporal region constitutes a key component for both handwriting (Nakamura et al., <xref rid="B30" ref-type="bibr">2002</xref>; Rapcsak and Beeson, <xref rid="B37" ref-type="bibr">2004</xref>) and reading (Bitan et al., <xref rid="B3" ref-type="bibr">2005</xref>; Nakamura et al., <xref rid="B29" ref-type="bibr">2007</xref>).</p></sec><sec><title>How speech production affects visual representations for reading</title><p>While the impact of auditory phonological inputs for literacy acquisition has been well demonstrated (e.g., phonological awareness studies), relatively less explored has been the connection between the speech production system and other systems during alphabetization. Indeed, although all alphabetizing children already speak fluently, an unusual segmentation and refinement of motor plans for speech production should be learned to pronounce isolated phonemes, allowing a multisensory association (explicitly or implicitly) of these new fine-grained phonatory representations with visual and auditory representations. One study has shown activation in a cortical region involved in speech production (Broca's area) in relation to handwriting learning and letter identification (Longcamp et al., <xref rid="B23" ref-type="bibr">2008</xref>). In fluent readers, the inferior frontal area involved in speech production in one hand and the VWFA in another hand show fast and strong inter-regional coupling (Bitan et al., <xref rid="B3" ref-type="bibr">2005</xref>), which operates even for unconsciously perceived words (Nakamura et al., <xref rid="B29" ref-type="bibr">2007</xref>). This distant visual and articulatory link mediating print-to-sound mapping is probably established during the earliest phase of reading acquisition and serves as a crucial foundation for the development of a dedicated reading network (Brem et al., <xref rid="B4" ref-type="bibr">2010</xref>).</p></sec><sec><title>Literacy acquisition as a multi-system learning process: the example of mirror discrimination learning</title><p>Taken together, these studies converge to the idea that far fromiinfar from a unimodal training on visual recognition, literacy acquisition is an irreducibly multi-system learning process. This lead us to predict that as one becomes literate, the expertise acquired through a given modality is not restricted to it, but can have an impact on other neural systems.</p><p>Perhaps the most spectacular case in point, and the one we choose to focus on in this article, is the spontaneous link between the motor and visual systems during literacy acquisition. This link is revealed in the beginning of the alphabetization process by the classic emergence of spontaneous mirror writing, i.e., writing letters in both orientations indistinctly (Cornell, <xref rid="B7" ref-type="bibr">1985</xref>). Indeed our primate visual system presents a mirror invariant representation of visual stimuli, which enables us to immediately recognize one image independently of left or right viewpoints (Rollenhagen and Olson, <xref rid="B38" ref-type="bibr">2000</xref>; Vuilleumier et al., <xref rid="B44" ref-type="bibr">2005</xref>; Biederman and Cooper, <xref rid="B2" ref-type="bibr">2009</xref>). This generates a special difficulty to distinguish the left-right orientation of letters (e.g., b vs. d) (Orton, <xref rid="B33" ref-type="bibr">1937</xref>; Corballis and Beale, <xref rid="B6" ref-type="bibr">1976</xref>; Lachmann, <xref rid="B18" ref-type="bibr">2002</xref>; Lachmann et al. in this special issue). One account for the emergence of mirror writing is that writing gestures can be “incorrectly” guided by mirror invariant visual representations of letters, a framework referred to as “perceptual confusion” (see Schott, <xref rid="B41" ref-type="bibr">2007</xref> for a review on this topic).</p><p>In complement, recent studies demonstrate that <italic>after</italic> literacy acquisition, mirror invariance is lost for letter strings (Kolinsky et al., <xref rid="B17" ref-type="bibr">2011</xref>; Pegado et al., <xref rid="B35" ref-type="bibr">2011</xref>, <xref rid="B34" ref-type="bibr">2014</xref>) and that the VWFA shows mirror discrimination for letters (Pegado et al., <xref rid="B35" ref-type="bibr">2011</xref>); see figure upper part. Interestingly, in this special issue, Nakamura and colleagues provide evidence for the causal role of the left occipito-temporal cortex (encompassing the VWFA) in mirror discrimination by using transcranial magnetic stimulation. However, it is still an open question whether this region becomes completely independent to discriminate the correct orientation of letters or if it still depends on inputs from phonological, gestural, and/or vocal representations.</p></sec><sec><title>A multi-system model of mirror discrimination learning</title><p>How is mirror discrimination acquired <italic>during</italic> the process of literacy acquisition? Here we sketch a model that takes into account not only the multisensory nature of alphabetization but also the multi-systems interplay, i.e., how representations in one system could influence the functioning of another system (e.g., mirror invariance in the visual system). In Figure <xref ref-type="fig" rid="F1">1</xref>, we present the hypothetical “multi-system input model” for mirror-letters discrimination learning during literacy acquisition. In order to correctly and rapidly identify letters for a fluent reading, the VWFA (in red) should visually distinguish between mirror representations of letters (see figure upper part). Top-down inputs from phonological, handwriting and speech production representations can provide discriminative information to the VWFA, helping this area that presents intrinsic mirror invariance, to accomplish its task of letter identification. This process probably requires focused attention (not represented in the figure) during the learning process and is likely to become progressively automatized. These top-down inputs toward the VWFA possibly influence this region to select relevant bottom-up inputs from lower-level visual areas (represented in pink in the figure) carrying information about the orientation of stimuli. For simplicity inter-hemispheric interactions are not represented here, but it should be acknowledged that during this learning process, local computations in the VWFA can include inhibition of mirror-inversed inputs from the other hemisphere.</p><fig id="F1" position="float"><label>Figure 1</label><caption><p><bold>Brain pathways for mirror discrimination learning during literacy acquisition</bold>. Upper: The Visual Word Form Area [VWFA] (in red) presents mirror invariance before alphabetization and mirror discrimination for letters after alphabetization. Lower: During alphabetization, the VWFA can receive top-down inputs with discriminative information from phonological, gestural (handwriting) and speech production areas and bottom-up inputs from lower level visual areas. All these inputs can help the VWFA to discriminate between mirror representations, thus correctly identifying letters to enable a fluent reading.</p></caption><graphic xlink:href="fpsyg-05-00703-g0001"></graphic></fig><p>Note that although we illustrate it by using mirror-letters (b-d or p-q), our model can eventually be extended to non-mirror letters, such as “e” or “r” for instance, given that each letter has a specific representation at the phonological, gestural (handwriting) and phonatory system. It cannot be excluded however that for these non-mirror letters, the simple extensive visual exposure to their fixed orientation could, in principle, be sufficient to induce visual orientation learning for them. In contrast, this simple passive learning mechanism is unlikely to explain orientation learning for mirror letters given that both mirror representations are regularly present (e.g., b and d). Thus at least for mirror letters, the discrimination mechanism is more likely to involve cross-modal inputs, as represented in our figure. Accordingly, it is known that learning a new set of letters by handwriting produces a better discrimination of its mirror images than when learning by typewriting (Longcamp et al., <xref rid="B24" ref-type="bibr">2006</xref>, <xref rid="B23" ref-type="bibr">2008</xref>). Moreover, despite low performances in pure perceptual visual tasks in mirror discrimination, illiterates are as sensitive as literates in mirror discrimination on vision-for-action tasks (Fernandes and Kolinsky, <xref rid="B11" ref-type="bibr">2013</xref>). Thus, inputs of gestural representations of letters influencing the VWFA perception could have a special weight in the processes of learning mirror discrimination.</p><p>It can also be expected that the existence of mirror letters forces the visual system to discriminate them, because it is necessary to correctly read words comprising mirror letters, such as in “bad” (vs. “dad”) for instance. Moreover, evidence suggest that such mirror discrimination sensitivity in literates can be partially generalized to other visual stimuli such as false-fonts (Pegado et al., <xref rid="B34" ref-type="bibr">2014</xref>) and geometric figures (Kolinsky et al., <xref rid="B17" ref-type="bibr">2011</xref>). Thus, it is plausible that during literacy acquisition mirror letters could “drive” the learning process of letter orientation discrimination, eventually extending it for non-mirror letters. Accordingly, in writing systems that do not have mirror letters in their alphabet (e.g., tamil script), even after learning to read and write, literates still present difficulties in mirror discrimination (Danziger and Pederson, <xref rid="B8" ref-type="bibr">1998</xref>). In addition, a superior mirror priming effect for inverted non-mirror letters (e.g., “r”) relative to mirror letters (e.g., “b”) has been reported (Perea et al., <xref rid="B36" ref-type="bibr">2011</xref>), suggesting thus a more intensive automatic discrimination for mirror-letters in comparison to non-mirror letters.</p><p>Although it is not known how mirror discriminations of letters and words could be achieved in the complete absence of feedback from phonological, gestural or speech representations, recent empirical and computational modeling work on baboons, who can be trained to acquire orthographic representations in a purely visual manner (Grainger et al., <xref rid="B15" ref-type="bibr">2012</xref>; Hannagan et al., <xref rid="B16" ref-type="bibr">2014</xref>) paves the way to answer this question.</p><p>Acknowledging this multi-system interplay during literacy acquisition can have potential implications for educational methods. Interestingly, experiments have suggested that multisensory reinforcement can present an advantage for literacy acquisition: arbitrary print-sound correspondences could be facilitated by adding an haptic component (tactile recognition of letters) during the learning process (Fredembach et al., <xref rid="B13" ref-type="bibr">2009</xref>; Bara and Gentaz, <xref rid="B1" ref-type="bibr">2011</xref>). Large scale studies are now needed to test if promoting multi-system learning is able to provide a clear advantage in real life alphabetization.</p><sec><title>Conflict of interest statement</title><p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p></sec></sec></body><back><ref-list><title>References</title><ref id="B1"><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Bara</surname><given-names>F.</given-names></name><name><surname>Gentaz</surname><given-names>E.</given-names></name></person-group> (<year>2011</year>). <article-title>Haptics in teaching handwriting: the role of perceptual and visuo-motor skills</article-title>. <source>Hum. Mov. 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