Trends in Neuroscience and Education ∎ (∎∎∎∎) ∎∎∎–∎∎∎

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Review article

How symbols transform brain function: A review in memory of Leo Blomert Nienke van Atteveldt a,b,n, Daniel Ansari c a

Department of Cognitive Neuroscience, Faculty of Psychology & Neuroscience, Maastricht University, P.O.Box 616, 6200 MD Maastricht, The Netherlands Department of Educational Neuroscience, Faculty of Psychology and Education and Institute Learn!, VU University Amsterdam, Van der Boechorststraat 1, 1081 BT Amsterdam, The Netherlands c Department of Psychology and Brain and Mind Institute, The University of Western Ontario, London, Ontario, Canada N6A 3K7 b

art ic l e i nf o

a b s t r a c t

Article history: Received 3 December 2013 Accepted 11 April 2014

It is considered unlikely that evolution selected specialized neuronal circuits for reading. Instead, it has been suggested that acquisition of cultural skills like reading is rooted in, and interacts with, naturally evolved brain mechanisms for visual and auditory processing. Here, we review how the learning of letter symbols interacts with brain mechanisms for audiovisual and speech processing. The aim of this review is to honor the work of the late Professor Leo Blomert. His work highlights the importance of intact and automated letter/speech–sound integration for fluent reading, but also shows that this depends on the orthography, demonstrating cross-linguistic difference in how reading acquisition transforms brain function. We contend that Professor Blomert's work illustrates the importance of (cultural) neuroscience for education. & 2014 Elsevier GmbH. All rights reserved.

Keywords: Literacy Speech Audiovisual integration Orthography Cross-linguistic Culture

Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Building blocks of literacy around the world . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3. Letters modulate (audiovisual) speech processing in superior temporal cortex in transparent orthographies. 4. Modulation of speech processing by letters depends on individual differences and orthography . . . . . . . . . . 5. Universal and culture-specific aspects of the neural basis of literacy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6. Summary: the importance of (cultural) neuroscience for education. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction Learning to read, count and calculate with symbols is indispensable in modern technological societies. Reading and symbolic numerical competencies are uniquely human and represent pillars of modern civilization and culture. However, these skills are not learned automatically but require years of formal instruction. It

n Corresponding author at: Department of Educational Neuroscience, Faculty of Psychology and Education, VU University Amsterdam, Van der Boechorststraat 1, 1081 BT Amsterdam, The Netherlands. Tel.: +31 20 5983473. E-mail addresses: [email protected] (N. van Atteveldt), [email protected] (D. Ansari).

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has been suggested that an important reason for this protracted learning trajectory is that literacy and numeracy have emerged too recently for our brains to be shaped by selective forces to subserve these functions. Instead, the learning of literacy and numeracy skills is thought to involve the harnessing and reconfiguration of existing, naturally evolved circuits for visual and auditory processing. For example, our brains are probably to a large extent hardwired for perceiving and producing speech, and literacy is thought to build on these naturally evolved language mechanisms [8,35], possibly by “recycling” [19] of cortical mechanisms for audiovisual speech integration [1,41], phonological and visual (shape) processing [20]. The reciprocity of the biology-culture interplay is illustrated by evidence showing that the cultural components of

http://dx.doi.org/10.1016/j.tine.2014.04.001 2211-9493/& 2014 Elsevier GmbH. All rights reserved.

Please cite this article as: van Atteveldt N, Ansari D. How symbols transform brain function: A review in memory of Leo Blomert. Trends in Neuroscience and Education (2014), http://dx.doi.org/10.1016/j.tine.2014.04.001i

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Textbox 1–Biography Leo Blomert

In memory of Leo Blomert, Professor of Cognitive Neuroscience at the Faculty of Psychology and Neuroscience, Maastricht University, the Netherlands. Leo Blomert served as the founding Chair of the Cognitive Neuroscience Department and founding member of the Maastricht Brain Imaging Center where he started his Literacy and Numeracy Research Group in 2000, and played a major role in building the Cognitive Neuroscience research program at Maastricht University. The research in his group focused on the development of brain networks for reading and math and the role of multisensory processing in reading, resulting in a new multisensory theory to account for successful and failing (dyslexia) reading development. Leo Blomert started his career in psychology at the Radboud University in Nijmegen, The Netherlands, where he also received his Ph.D. He specialized further in brain plasticity of language functions after brain damage at the Max Planck Institute (MPI) for Psycholinguistics in Nijmegen (The Netherlands) and the MPI for Neurological Research in Cologne (Germany) and later as an Associate Research Professor at the University of California Irvine, USA. Besides his academic heritage, Leo Blomert was very influential in the domain of dyslexia care and treatment in The Netherlands. Leo directly applied his expertise by developing digital diagnostic tests for the cognitive profiling of developmental disorders dyslexia and dyscalculia. One of his most important legacies for the Netherlands is his contribution to the legislation allowing dyslexia treatment to be covered by the national health insurance. Leo passed away on November 25, 2012.

literacy and numeracy that are learned during education, e.g. the learning of letter and number symbols and their connections to speech and quantity representations, have clear influences on brain development [18,23,30,34]. Interestingly, this “cultural influence” on brain organization seems to be shaped by the specifics of, for instance, the writing system. Indeed, we recently revealed that the effect of letters on speech sound processing depends on the characteristics of the orthography ([24]). The aim of this paper is to provide a broad overview of what we know (and do not yet know) about the interaction of culture and biology in the acquisition and brain representation of symbols, by specifically honoring the academic heritage of the late Professor Leo Blomert (Box 1). We will focus on letter symbols but draw possible parallels to numerals in Box 2. Professor Blomert conducted work at both the behavioral and brain levels of analysis to better understand how acquiring cultural skills such as reading transform neurocognitive systems. His work has provided influential insights into the behavioral and neural basis of literacy (and numeracy) across countries and has resulted in implications for education, particularly in the context of developmental dyslexia (see e.g. [6,7,10,11,13,22,44]). More specifically, Blomert's work provided a coherent body of evidence to illustrate the critical importance of intact and automated neural letter/speech–sound integration for fluent reading. His work revealed how existing brain circuits for (audio–visual) speech processing become tuned to the arbitrary relationship between letters and speech sounds in individuals with and without reading difficulties. In the following sections, we will review how (audio–visual) speech processing gets transformed through literacy acquisition and how this might depend on orthography. We will begin with evidence from the relatively transparent Dutch orthography. In a review paper written a year before his passing, Blomert emphasized the importance of exploring symbol/speech–sound

Textbox 2–Parallels in symbol learning between reading and math?

One of the key parallels between learning how to read and learning about numbers and mathematics is that both involve the learning of arbitrary (non-iconic) symbols. Like letters, numerical symbols are relatively recent cultural inventions [28] and therefore the learning of numerical symbols must also involve a process whereby existing neuronal circuits need to be ‘recycled’ or ‘reconverted’ in order to allow for the processing of number symbols. However, numerical symbols differ from letters in several significant ways. First of all, while there is still some variability in the types of visual symbols used to represent number, Arabic numerals have become somewhat of a universal symbolic system for the representation of numerical information, though clear differences across languages in number naming systems which do influence how number words are learnt (e.g. [29]). Thus, while in reading there is great cross-national variability in the scripts use, numerical symbols (at least in the visual domain) vary considerably less. Another key difference between numerical symbols and letters is the referents of these symbols. The referents of letters (in alphabetic languages) are speech sounds (depending on the orthography each letter refers to one or more than one speech sound) and these referents do not vary across situational context. In contrast, for numerical symbols there are many different referents that vary as a function of the situation in which they are used. While most of the time a numerical symbol is used to refer to a given quantity (semantic referent similar to logographic systems), numerical symbols also have number names as their auditory referents and they refer to ordinal information, such the position of an athlete in a race or a house number. To date it is unclear exactly how numerical symbols are mapped onto their various referents. The available neuroimaging data suggests that numerical quantity processing is associated with the engagement of the parietal cortex, in particular the intraparietal sulcus (IPS). Furthermore, there are data to suggest that the left IPS is particularly important for the processing of symbolic representations of quantity [2,23] and that individual differences in the activation of the left IPS during symbolic number comparison correlate with children’s arithmetic scores [17]. The experience-dependent shaping of the left IPS over the course of learning and development may represent the process of ‘neuronal recycling’ that occurs when number symbols are learnt. However, the exact computational processes that allow number symbols to become referents of numerical information remains poorly understood.

integration in more opaque and non-alphabetic orthographies for understanding the neural basis of literacy across languages [8]. In light of this, the second part of this review will discuss recent neuroimaging data on symbol–sound integration in the more opaque English orthography, and considers cross-linguistic differences in the neural correlates of literacy more generally.

2. Building blocks of literacy around the world A universally important step in becoming literate is learning how a writing system represents the oral language system. However, this step is very different across different types of script, which are called orthographies [45,47]. In alphabetic scripts, symbols represent speech at the very abstract level of single speech sounds (phonemes), which by themselves are meaningless. The crucial step in becoming

Please cite this article as: van Atteveldt N, Ansari D. How symbols transform brain function: A review in memory of Leo Blomert. Trends in Neuroscience and Education (2014), http://dx.doi.org/10.1016/j.tine.2014.04.001i

N. van Atteveldt, D. Ansari / Trends in Neuroscience and Education ∎ (∎∎∎∎) ∎∎∎–∎∎∎

Textbox 3–Outstanding questions

1. How does the process of establishing automatic associations between visual symbols and phonological units develop across languages? It will be interesting to compare how processing of audiovisual pairs becomes automated in English and Dutch readers, for different units (single letter, letter-cluster, syllable, or word level). 2. To what extent does learning of letter/speech–sound correspondences “recycle” non-reading audiovisual brain circuits? It will be interesting to directly compare audiovisual (speech) processing in literates and illiterates (and/ or late literates) and to closely follow developmental trajectories. 3. Can we make the learning processes of literacy and numeracy less challenging by exploiting what we know about the biological, evolutionary shaped components, which are more natural and hence might facilitate learning? For example, lip reading is a visual component of speech that, in contrast to scripts, evolved together with oral language processing. It has recently been shown that lip reading may improve the shaping of phoneme representations in dyslexics [4]. Another example is to include a sensori-motor component in the learning of letters [26], based also on the importance of motor systems in reading handwritten symbols shown by Nakamura and colleagues ([32]; see also [5]). 4. Do bilinguals who read in two languages with different orthographies recruit different brain circuits depending on the language they read? 5. It is clear that letters are connected to speech sounds. In the domain of numbers, the process of connecting numerical symbols with their (semantic) referents occurs. What pre-existing systems do numerical symbols get connected to over the course of learning and development?

literate in alphabetic scripts is therefore to learn and automate the associations between letters and speech sounds. These associations vary in consistency across alphabetic scripts, ranging from being almost entirely (e.g. Italian) or fairly (Dutch) transparent to being very opaque (English). In other words, while in Italian a single letter (almost) always corresponds to the same sound, in English each letter corresponds to many different sounds (and vice versa), depending on the context. In logographic scripts, such as Chinese, visual symbols represent meaningful units of speech (morphemes or words), so there is a more direct relation between symbols and the meanings they convey. The variation in how visual symbols need to be mapped onto speech and semantic representations suggests that the use of pre-existing neural systems during reading acquisition has to be an adaptive process, that is, similar neuronal circuits may be used, but how they are used should be flexible to accommodate the different ways in which symbols are mapped to sounds and meanings. The question that arises is what brain areas are universally activated during reading, and how they are further shaped by the specifics of the language's orthography. In the following, we will therefore address the questions: (1) how does the acquisition of literacy transform neuronal circuitry that initially subserves nonreading functions, with a focus on (audio–visual) speech processing? And (2) how do variations in orthography and individual development influence how symbols transform brain function?

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3. Letters modulate (audiovisual) speech processing in superior temporal cortex in transparent orthographies The most direct evidence for how literacy transforms brain function comes from comparing literates and illiterates. A recent study that separated changes caused by literacy acquisition from maturational effects by including a group of late literates, showed that learning to read led to increased activation of part of the (posterior) auditory association cortex, the planum temporale [20], which is likely to be a reflection of the refinement of phonological processing that results from the acquisition of literacy [31]. The work of Blomert's group provided insights into how letters influence speech sound processing in Dutch readers. In fluent adult readers, who have fully mastered letter/speech–sound correspondences and have life-long experience using them, viewing letters that matched heard speech sounds increased the hemodynamic response to speech sounds in the planum temporale, whereas non-matching letters decreased speech sound processing [41]. Such an effect of letter/sound congruency in superior temporal cortex (STC) was found before in another transparent orthography (Finnish; [37]) and is a consequence of experience-dependent plasticity, since there is nothing natural that suggests a mapping between particular letters and speech sounds – these are learnt associations. In addition to auditory association cortex, heteromodal parts of the STC were shown to be involved in the integration of letters and speech sounds. These findings are consistent with the notion that reading is a fundamentally audio–visual process because of the elementary relation between visual (orthographic) and auditory (speech/phonological) representations. Therefore, in addition to plastic changes in auditory processing, plastic changes in the cortical circuitry allowing for cross-modal interactions are thought to lie at the heart of reading acquisition. Several studies have indeed suggested that the integration of letters and speech sounds builds upon the more naturally evolved mechanisms for audiovisual speech perception and lip reading, including auditory association cortex and heteromodal STC [1,40,41]. However, Blomert and Froyen [9] also point out important differences between natural audio–visual processing (i.e., lip movements and speech) and the audio–visual processing of letters (see also [42]). For example, the involvement of visual processing areas in the integration process seems more robust for audiovisual speech processing compared to letter/speech–sound integration. It will be interesting to obtain more direct insight in how non-reading audiovisual processes may be altered as a function of literacy acquisition, for example by comparing audiovisual (speech) processing in literates and illiterates. Another consequence of mapping symbols to phonological representations is a reorganization of ventral visual systems for object/shape processing and abstraction. Dehaene and colleagues [20] showed a notable reorganization of this ventral visual system, including an enhanced response to script in an area often called the visual word form area. Sensitivity of this area to print emerges only gradually over the course of reading acquisition [15] and is thought to emerge in interaction with the phonological system, which gets increasingly tuned to single speech–sounds when letter–sound correspondences are learned [8,36].

4. Modulation of speech processing by letters depends on individual differences and orthography Having demonstrated that the acquisition of letter–sound associations leads to changes in the auditory and audio–visual brain circuitry, the second question was how plastic the process of “re-using” existing brain circuits is. Blomert's group conducted a

Please cite this article as: van Atteveldt N, Ansari D. How symbols transform brain function: A review in memory of Leo Blomert. Trends in Neuroscience and Education (2014), http://dx.doi.org/10.1016/j.tine.2014.04.001i

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STC

Letters (V) & Speech Sounds (A)

Numerals (V) & Number Names (A)

Arbitrary units

Letters (V) & Speech Sounds (A)

V

A

C

I

Dutch readers

V

A

C

I

English readers

V

A

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English readers

Fig. 1. Superior temporal cortex tuned to learnt congruency at the letter–sound level in Dutch readers, but to larger units in English readers. The auditory association cortex, located in the superior temporal cortex (STC), shows a strong sensitivity to the congruency of letter–sound pairs in readers of the relatively transparent Dutch orthography [41], left graph. As letter–sound pairs are learnt associations, this tuning is the result of literacy acquisition. Readers of the more opaque English orthography [24] did not express this same sensitivity in the STC (middle bar graph). Instead, rather than getting tuned to congruency at the single letter/speech–sound level, the STC of English readers was sensitive to congruency at larger units, as shown here at the level of numerals and number names (right graph). STC¼ superior temporal cortex; V¼ visual, A¼ auditory, C¼congruent (audiovisual) and I¼incongruent (audiovisual).

series of developmental studies into letter/speech-sound integration in typical and atypical reading development. Using eventrelated potentials (ERP's), they were able to show that in contrast to knowledge of letter/speech–sound correspondences, their automation at the neuronal level was protracted during development [21]. Furthermore, they revealed a relationship between letter/speech–sound congruency responses in the STC and individual variability in reading ability, with dyslexic readers expressing low congruency/low reading scores [6]. Together, these findings show that the tuning of STC by letter symbols during reading acquisition emerges relatively slowly and differs between individuals, and predicts variability in reading proficiency. It has been shown repeatedly that neural signatures of reading are influenced by orthography (e.g. [34]). We recently demonstrated that within alphabetic scripts, the STC does not show the same unique response to letter–sound pairs in readers of the more opaque English orthography [24] compared to Dutch readers [41] (Fig. 1). Rather than being tuned at the single letter/speech-sound level, the evidence points to a role for STC in English readers in orthographicphonologic conversion at larger “grain size” [46]. For example, the STC of English readers was sensitive to congruency at the level of numerals and number names (Fig. 1), and other studies found evidence at the rime level (e.g. [14,27]). This supports and expands the notion of experience-driven tuning of STC by showing the effect of orthography. As mentioned before, in English, the mappings between orthography and phonology are quite inconsistent at the single letter/phoneme level, but there is more consistency at larger units. These orthography-dependent characteristics are reflected in the neural tuning of STC to audiovisual pairs. Across alphabetic and logographic scripts, it has been shown that reading engages the STC relatively more in alphabetic scripts [16], and prefrontal cortex (PFC) more in logographic scripts such as Chinese [39]. These differences are likely related

to a stronger emphasis on phonology in alphabetic languages versus gestural cues and meaning in Chinese. This was confirmed in a recent study that compared neural processing of Chinese and alphabetic symbols [32]. They controlled for gestural differences by presenting handwritten-like and dynamic (as if someone was writing) alphabetic stimuli. Manipulating alphabetic symbols in this way reduced cross-linguistic differences in the involvement of the PFC, which indicates that the PFC involvement is indeed due to gestural information related to the engagement of neural mechanisms of handwriting during reading of logographic scripts.

5. Universal and culture-specific aspects of the neural basis of literacy What can we conclude with regard to the biology-culture interplay in literacy development? The recruitment and shaping of superior temporal speech processing areas on the one hand, and frontal language areas on the other hand, seems to be very adaptive to the specifics of a script type. The first seems mostly related to variations within alphabetic orthographies, i.e., differences in orthographic depth. The involvement of frontal cortex in reading was most profound in logographic scripts [39] and related to gestural and semantic processing [32,43]. In contrast to the orthography-dependent transformation of temporal speech processing and frontal language areas, the ventral visual system seems to be recruited for reading quite universally [12]. Universal across writing systems is that they all use culturally defined visual symbols to access word meaning, which is consistent with universal recruitment of the ventral visual system. Orthographies differ in how the visual symbols get connected to speech sounds and semantic representations. In alphabetic scripts, mappings between letters and speech sounds provide access to

Please cite this article as: van Atteveldt N, Ansari D. How symbols transform brain function: A review in memory of Leo Blomert. Trends in Neuroscience and Education (2014), http://dx.doi.org/10.1016/j.tine.2014.04.001i

N. van Atteveldt, D. Ansari / Trends in Neuroscience and Education ∎ (∎∎∎∎) ∎∎∎–∎∎∎

word meaning, whereas symbols map onto meanings more directly in logographic systems. This predicts that the link between visual symbolic processing on the one hand, and auditory speech and semantic processing on the other hand, is shaped by the properties of the writing system, reorganizing mainly the temporal cortex in alphabetic readers, and frontal-premotor cortex in logographic literates. This is corroborated by the findings of impaired temporal cortex in dyslexics across alphabetic languages [33] versus decreased frontal activity in Chinese dyslexics ([38]; but see [25]). In sum, recycling of visual areas to process culturally defined symbols seems fairly universal whereas the processes of connecting these symbols to sounds and meanings are even more adaptive as they change the brain differently in different cultures.

6. Summary: the importance of (cultural) neuroscience for education Brain systems for audiovisual speech processing, visual shape processing, semantic and premotor processing are recruited by literacy acquisition around the world, but the specific way in which these brain systems are transformed is very plastic, i.e. is shaped by developmental variability and the orthography that is being learnt. Blomert's work has raised important outstanding research questions, which are summarized in Box 3. An important challenge to which Blomert's work contributed is to separate universal and culturespecific processes of plasticity that occur during reading. Such work is not only theoretically constraining but carries with it implications for universal versus culture-specific education (see also [3,47]). For example, Dutch studies suggest focusing interventions on letter/ speech–sound level, as the evidence points to letter/speech–sound integration as a proximal cause of reading deficits in dyslexia [8]. The absence of the same integration effects at the letter–sound level in English readers [24] indicates that different languages may need different interventions. Other implications for education come from the evidence Blomert's work provided for the importance of intact and automated letter/speech–sound integration for fluent reading. In Froyen et al. [21], they showed that the behavioral responses looked mature much earlier than the neuronal integration processes. This emphasizes the added value of neuroscience: while behavioral data suggested that letter–speech integration was mature, the brain data demonstrated a protracted trajectory of automation of the integration processes.

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Please cite this article as: van Atteveldt N, Ansari D. How symbols transform brain function: A review in memory of Leo Blomert. Trends in Neuroscience and Education (2014), http://dx.doi.org/10.1016/j.tine.2014.04.001i