Typical and Atypical Development of Visual Expertise for Print as Indexed by the Visual Word N1 (N170w) : A Systematic Review

This is a self-archived version of an original article. This version may differ from the original in pagination and typographic details. Author(s): Title: Year: Version: Copyright: Rights: Rights url: Please cite the original version: CC BY 4.0 https://creativecommons.org/licenses/by/4.0/ Typical and Atypical Development of Visual Expertise for Print as Indexed by the Visual Word N1 (N170w) : A Systematic Review © 2022 Amora, Tretow, Verwimp, Tijms, Leppänen and Csépe. Published version Amora, Kathleen Kay; Tretow, Ariane; Verwimp, Cara; Tijms, Jurgen; Leppänen, Paavo H. T.; Csépe, Valéria Amora, K. K., Tretow, A., Verwimp, C., Tijms, J., Leppänen, P. H. T., & Csépe, V. (2022). Typical and Atypical Development of Visual Expertise for Print as Indexed by the Visual Word N1 (N170w) : A Systematic Review. Frontiers in Neuroscience, 16, Article 898800. https://doi.org/10.3389/fnins.2022.898800 2022 SYSTEMATIC REVIEW published: 30 June 2022 doi: 10.3389/fnins.2022.898800 Frontiers in Neuroscience | www.frontiersin.org 1June 2022 | Volume 16 | Article 898800 Edited by: Li-Hai Tan, Shenzhen Institute of Neuroscience, China Reviewed by: Anthony James Krafnick, Dominican University, United States Yang Zhang, University of Minnesota Health Twin Cities, United States *Correspondence: Kathleen Kay Amora [email protected]; [email protected] †These authors have contributed equally to this work and share first authorship Specialty section: This article was submitted to Neurodevelopment, a section of the journal Frontiers in Neuroscience Received: 17 March 2022 Accepted: 24 May 2022 Published: 30 June 2022 Citation: Amora KK, Tretow A, Verwimp C, Tijms J, Leppänen PHT and Csépe V (2022) Typical and Atypical Development of Visual Expertise for Print as Indexed by the Visual Word N1 (N170w): A Systematic Review. Front. Neurosci. 16:898800. doi: 10.3389/fnins.2022.898800 Typical and Atypical Development of Visual Expertise for Print as Indexed by the Visual Word N1 (N170w): A Systematic Review Kathleen Kay Amora1,2*†, Ariane Tretow3†, Cara Verwimp 4,5†, Jurgen Tijms4,5, Paavo H. T. Leppänen3and Valéria Csépe 1,6 1Brain Imaging Centre, Research Centre for Natural Sciences, Budapest, Hungary, 2Faculty of Modern Philology and Social Sciences, Multilingualism Doctoral School, University of Pannonia, Veszprém, Hungary, 3Department of Psychology, University of Jyväskylä, Jyväskylä, Finland, 4Department of Developmental Psychology, University of Amsterdam, Amsterdam, Netherlands, 5Rudolf Berlin Center, Amsterdam, Netherlands, 6Institute for Hungarian and Applied Linguistics, University of Pannonia, Veszprém, Hungary The visual word N1 (N170w) is an early brain ERP component that has been found to be a neurophysiological marker for print expertise, which is a prelexical requirement associated with reading development. To date, no other review has assimilated existing research on reading difficulties and atypical development of processes reflected in the N170w response. Hence, this systematic review synthesized results and evaluated neurophysiological and experimental procedures across different studies about visual print expertise in reading development. Literature databases were examined for relevant studies from 1995 to 2020 investigating the N170w response in individuals with or without reading disorders. To capture the development of the N170w related to reading, results were compared between three different age groups: pre-literate children, schoolaged children, and young adults. The majority of available N170w studies (N=69) investigated adults (n=31) followed by children (school-aged: n=21; pre-literate: n=4) and adolescents (n=1) while some studies investigated a combination of these age groups (n=12). Most studies were conducted with German-speaking populations (n=17), followed by English (n=15) and Chinese (n=14) speaking participants. The N170w was primarily investigated using a combination of words, pseudowords, and symbols (n=20) and mostly used repetition-detection (n=16) or lexical-decision tasks (n=16). Different studies posed huge variability in selecting electrode sites for analysis; however, most focused on P7, P8, and O1 sites of the international 10–20 system. Most of the studies in adults have found a more negative N170w in controls than poor readers, whereas in children, the results have been mixed. In typical readers, N170w ranged from having a bilateral distribution to a left-hemispheric dominance throughout development, whereas in young, poor readers, the response was mainly right-lateralized and then remained in a bilateral distribution. Moreover, the N170w latency has varied according to age group, with adults having an earlier onset yet with shorter latency than school-aged and pre-literate children. This systematic review provides a comprehensive picture of the development of Amora et al. Visual Word N170w Systematic Review print expertise as indexed by the N170w across age groups and reading abilities and discusses theoretical and methodological differences and challenges in the field, aiming to guide future research. Systematic Review Registration: https://www.crd.york.ac.uk/prospero/display_ record.php?ID=CRD42021228444. Keywords: reading development, dyslexia, words, developmental reading disorder (DRD), event-related potentials (ERP), visual expertise, N170, systematic review INTRODUCTION Reading, which involves successfully and fluently linking letters to sounds, is one of the prerequisites to participate in today’s society. Learning to read is commonly shaped through years of exposure to text and formal teaching. Although we are constantly exposed to text, some do not successfully develop fluent reading skills, with the poorest 3–10% of the children being considered to have developmental dyslexia or developmental reading disorder (DRD; Snowling, 2013). Fast recognition of words is critical for attaining automatized reading in alphabetic orthographies (McCandliss et al., 2003) and is associated with a reorganization of the visual systems that are evolving to process the new word forms efficiently. Event-related potential (ERP) studies have associated the visual N170 component, which peaks around 170 milliseconds after stimulus onset, with the expertise for visual stimuli such as words. The visual word N170 (hereafter referred to as N170w) is a response with a negative deflection commonly largest over occipitotemporal regions, and its lateralization depends on maturation and reading experience (Maurer and McCandliss, 2008). The emergence of N170w is supposedly rooted in the visual word form area (VWFA) within the ventral occipitotemporal cortex (vOTC) of the left hemisphere, which has been known to show sensitivity to visual words throughout literacy (McCandliss et al., 2003; Rossion et al., 2003; Dehaene et al., 2010). Moreover, it has been considered as a neurophysiological marker for print expertise with prelexical sensitivity to letter/character strings (Maurer et al., 2006; Luck, 2012). Higher N1 amplitudes for words than low-level visual control stimuli such as meaningless symbol strings or shapes have been reported across languages (e.g., Dutch: Fraga González et al., 2014, German: Maurer et al., 2006, Portuguese: Araújo et al., 2012). Several studies have explored the N170 component, which is reported as a category-specific visual expertise marker (Maurer et al., 2008b), and has been studied extensively in face perception studies (e.g., Bentin et al., 1996; Feuerriegel et al., 2015). Other studies have also associated the N170 with sensory processing related to auditory information (Leppänen and Lyytinen, 1997) and referred to the modulation of N170 by attention (Herrmann and Knight, 2001). However, the N170w associated with print tuning has become of particular interest in reading disorder studies in recent years. Aside from the mismatch negativity (MMN) which is commonly used to discuss the role of auditory processing in reading development, the N170w provides a more readingspecific insight related to visual processing for print, which is the primary visual stimuli for reading. Moreover, N170 is reported to possibly predict later reading outcomes as the N170w response is modulated by reading skills (Brem et al., 2013). Furthermore, the N170 has a role in attention, which could be taken into consideration in relation to the visual attention span deficit theory, referring to a higher attention level required in dyslexics for processing of words. Different investigations aiming at characterizing the N170w have identified two different processes; coarse and fine print tuning (e.g., Zhao et al., 2014; Tong et al., 2016a; Kemény et al., 2018). Coarse print tuning, which indicates sublexical processing, entails differential processing of words and non-orthographic symbol strings, whereas fine print tuning usually taps into lexical processes and is required for processing of differences between print and closely matched false font or pseudo-character strings (Maurer et al., 2005; Eberhard-Moscicka et al., 2016). Even though many studies have aspired to shed light on the main visual component with reading development, most of them performed in typical readers or reading disordered individuals have produced contradictory results. These could be due to variability in participant groups, stimuli, and task-specific factors. Zhao et al. (2014) demonstrated that coarse and even finetuning of the N170w can be developed within 1 year of reading instruction. However, N170w print specialization has been found to occur later in children with DRD (Maurer et al., 2007, 2011), suggesting differences in the developmental trajectory of N170w specialization of individuals with DRD compared to their typically developing peers. Longitudinal studies have shown an inverted U-shape development curve of the N170w, with an increased response for orthographic stimuli in beginning readers followed by a slight decrease when readers become fluent (Maurer et al., 2006; Fraga González et al., 2021). However, some studies have shown evidence for a persistent N170w print tuning deficit in individuals with DRD, with no or small differences in the N170w responses to word-like stimuli and matched symbol strings in adults compared to their typically developing peers (Mahé et al., 2012). In addition, for print, it has been found that a bilateral, though somewhat right hemisphere-dominated N170w topography in children changes gradually into leftlateralized topography when reading becomes more automatized. This change occurs shortly after the start of formal reading instruction, contributing to letter-speech sound integration in the form of grapheme-phoneme correspondences (Maurer et al., 2006; Brem et al., 2013). However, for individuals with DRD, the response lateralization showed no consistent pattern: left (e.g., Frontiers in Neuroscience | www.frontiersin.org 2June 2022 | Volume 16 | Article 898800 Amora et al. Visual Word N170w Systematic Review Araújo et al., 2012), bilateral (e.g., Fraga González et al., 2014), or right-lateralized (e.g., van Setten et al., 2019) distributions were reported. Although numerous studies have demonstrated an atypical N170w response to words in individuals with DRD, the effects regarding amplitude, latency, and lateralization have been inconsistent. Moreover, the variation in experimental designs and setups could pose challenges in interpreting results for interested researchers in the field. Therefore, our systematic review assimilated existing research on typical and atypical development of visual reading processes as reflected by the N170w response. The main objective of this review was to give an overview of the status quo of the N170w literature related to reading development in terms of reading ability (typically vs. atypically developing readers) and age group (from preliterate age until adulthood). For our secondary objectives, we examined differences in N170w in comparison with other word-like conditions (e.g., pseudowords, nonwords) and the potential impact of various linguistic factors (e.g., language, orthographic depth). In addition, we investigated theoretical and methodological differences applied in the N170w studies to guide future research using this component to investigate typical and atypical reading. MATERIALS AND METHODS Protocol and Registration The protocol for this systematic review was pre-registered and uploaded to https://www.crd.york.ac.uk/prospero/display_ record.php?ID=CRD42021228444. All aspects of this review adhered to the Preferred Reporting Items in Systematic Reviews (PRISMA) guidelines (Moher et al., 2009). Eligibility Criteria and Study Selection Studies included in the current review satisfied the following criteria after the full-text review: (1) cross-sectional, longitudinal, and intervention studies on the visual word N1/N170 employing different stimulus conditions, i.e., letter/character strings vs. non-letter/non-character stimuli (case studies, reviews, theses or dissertations, and gray literature were excluded; as well as using single letters only as stimuli was excluded); (2) a sample involving participants with or/and without developmental reading disorders (DRD) (studies that focused only on other neurological/developmental conditions or comorbidities aside from DRD (e.g., ADHD) as well as with impaired hearing or a (severely) visual handicap were excluded); (3) participants that could be categorized into one of the following age groups: preliterate children (3–6 years old), school-aged/literate children (7–11 years old) and young adults (18–35 years old); and (4) reported findings in an English-language, peer-reviewed journal between 1995 and 2020. The earlier year limitation (1995) was implemented to not have a bias toward earlier works, but also to have a clear limitation that helps in keeping the methodological considerations consistent and comparable (i.e., equipment, sample size), whereas the late year limitation (2020) served as a clear cut-off of the search date when the search terms were applied. Systematic Review Procedure Information Sources, Search, Data Collection Process We searched Web of Science, PubMed (MEDLINE), PsychINFO, PubPsych, ProQuest, Scopus, PsycNET, and Cochrane for studies using the following search strings: (N1 OR N170) AND (EEG OR ERP OR event-related potential∗) AND (visual OR word OR print) AND (expertise OR read∗OR develop∗) AND [read∗AND (disorder∗OR disab∗OR dyslexi∗OR difficult∗OR problem∗OR develop∗)] AND (participant∗OR child∗OR adult∗). Final searches were conducted on the 11th and 19th of January 2021. The articles underwent four rounds of screening: removal of duplicates, abstract screening, full-text reading, and data extraction. Removal of duplicates, title, and abstract screening were performed using the Rayyan software for systematic reviews (Ouzzani et al., 2016). The evaluation process was conducted by three independent raters, with title and abstract screening being performed fully blinded. Risk of Bias in Individual Studies Included studies underwent a risk-of-bias assessment using the Newcastle—Ottawa Scale (NOS) adapted to cross-sectional studies (Modesti et al., 2016). Each rater judged every study based on seven quality items categorized into three sections: the study group selection (representativeness of the sample, sample size, non-respondents, measurement tool for assessment of reading skill), the comparability of the groups; and the outcome (assessment and statistics). Each rater awarded a star per item if the study fits the criteria. Obtained NOS scores (M= 7, SD =2) were reported in Supplementary Table S1. Interrater reliability was assessed through percentage agreement of rater1, rater2, and rater3 of the NOS. For this, 10% of the reviewed studies (n=7) were randomly selected and reassessed by the second and third rater. Interrater reliability between each rater pair was 71.24% (R1/R2, R1/R3, R3/R2). Data Items The following data were extracted from all selected papers: participant information (e.g., sample size, participant age, reading ability groups), EEG parameters (e.g., pre-processing steps and region/scalp areas of interest as defined by electrode set used in the analyses), stimuli and task characteristics (e.g., language, experimental design), and ERP results (i.e., amplitude, lateralization, latency). We based our ERP summary on the statistical results and the graphical representations present in the text. The full details of the extracted data can be found in Supplementary Table S2. Synthesis of Results We employed a narrative synthesis to compile the results regarding N170w, amplitude, latency, and lateralization of the selected studies and provided summary tables that included essential extracted features of the study (e.g., participants, age, task, results). In extracting the results for individual studies, we excluded ERP results using other forms of analyses (e.g., topographic analysis of variance, LORETA). The original scope of means and effect sizes extraction of the selected papers had to be reviewed due to the lack of reported means and effect Frontiers in Neuroscience | www.frontiersin.org 3June 2022 | Volume 16 | Article 898800 Amora et al. Visual Word N170w Systematic Review sizes in the papers included in this review. For evaluation of lateralization and amplitude, variables were introduced, which enabled comparison across papers despite the missing mean and effect sizes (i.e., C>DRD, referring to the amplitude of control subjects being enhanced compared to subjects with reading difficulties). Effects of intervention studies on N170w were not assessed; thus, the pre-intervention EEG data only was used for data extraction on N170w for those studies involving training. RESULTS Study Selection The initial database search identified 572 articles. Out of 282 non-duplicates, 146 articles were excluded after title and abstract screening using the Rayyan software for systematic reviews (Ouzzani et al., 2016), leaving a number of 136 articles in the fulltext screening. All articles were reviewed by authors K. K. A., A. T., and C. V. with a two out of the three-majority decision for inclusion. Twelve conflicting articles were additionally reviewed by the remaining co-authors, leading to the inclusion of two out of twelve articles. After applying the inclusion and exclusion criteria, 59 articles were excluded during full-text screening and eight articles during data extraction, resulting in 69 articles included in the review. A flowchart of this selection process is displayed in Figure 1. A normal distribution across publication years is significantly noticeable among the included articles (see Figure 2). Dense publication years were 2011 (n=9) and 2013 (n=8). Specific characteristics of each of the studies can be found in Supplementary Table S2. Methodological Characteristics Participants Of the 69 studies included in this systematic review, eight examined the N170w in pre-literate children, 31 in school-aged children, three in adolescents, and 41 in young adults aged between 18 and 35. The total number exceeds 69 studies, as 12 of these included more than one age group. The results of the three studies that examined the N170w in adolescents, are combined with the young adult group, as the mean age of the adolescents (Mage =17.24 years) was close to our lower edge of the young adults age range, and the reported results in terms of amplitude and lateralization were comparable to the results in adults. A substantial number of studies only included typical readers (n=42), whereas 27 studies compared controls with people with dyslexia only (n=23) and/or otherwise defined sample (i.e., poor readers or spellers, illiterate or atrisk individuals; n=8). The number of participants included in each of the studies demonstrated a wide range from 11 to 72. The exact values for each of the reviewed studies together with participant, age, and gender distribution can be obtained via Supplementary Table S2. Criteria to consider participants as reading impaired or control varied widely across studies. Participants were considered reading impaired based on either a formal dyslexia diagnosis or the evaluation of reading scores below the 25th, 20th, 16th, and 10th percentile; or 1.5 or 1 standard deviation below the average. On the other hand, typical readers had percentile scores above 10 to >25 in reading tests. These lead to discrepancies across studies as DRD and TD readers overlap across studies reporting criteria (n=23). Language, Stimuli, and Procedure Most of the studies were conducted in German-speaking populations (n=17), followed by English (n=15), and Chinese (n=14). A minority of five studies investigated a second language. Paradigm types varied between repetition-detectiontask (n=16), lexical decision task (n=16), N-back task (n= 6), and other paradigms (n=31). All 69 studies used words as a condition, and either had it as the only condition (n=7) or compared words to pseudowords (n=10), pseudo-homophones (n=2) or non-words (n=1). Other comparisons were made to symbols (n=13), faces (n=5) or pictures (n=2). Thirty studies used more than two conditions, mainly comprising words, pseudowords and symbols (n=20). For a detailed overview of all stimuli per study we refer to Supplementary Table S2. Words presented had an average character length of M=6.62 (SD =2.39, 3–13) letters or strokes. When reported, the word frequency of words commonly ranged in high (n=23) or low to high (n=10) frequency values. Stimuli duration of words across studies varied between 100 and 5,250 ms, which differed across participants age groups: adults M=489.22, SD =317.49; school-aged children M= 845.77, SD =724.62; pre-literate children M=1,125, SD = 1683.96. Paradigm difference in stimulus duration was visible for the bigger clusters of detection tasks (M=550.31 ms, SD = 460.19) and lexical decision tasks (M=784.38 ms, SD =903.09). The explicit word/symbol processing task (5,250 ms) and dual valence task (100 ms) were the most deviating paradigms. The number of presented trials was another dividing factor, ranging from 40 to 576 trials for the word conditions (Brem et al., 2013; Collins et al., 2017). Distance to screen for the word presentation ranged from 50 cm to 145 cm (M=81.59 cm, SD =23.82 cm) across studies. Interstimulus intervals (ISI) were composed of different components (e.g., fixation cross and blank screen) across studies. Common feedback, response screens, and blink screens were among the reported procedures for the composition of trials (see Supplementary Table S2). EEG Analysis The presented studies (N=69) had a significant difference in the number of EEG channels recorded (19–128, Madult =64.57, SDadult =38.67; Mlitchild =68.23, SDlitchild =41.27; Mprelitchild =44.13, SDprelitchild =13.29). Across all studies, most common electrode setups were 64 (n=17) and 128 (n=16) electrodes, with one additional study having both setups. Electrodes were reported as Ag/AgCl (n=53), TiN (n=7), implemented in caps of various manufacturers (see Supplementary Table S2). For EGI systems, the common impedance threshold laid at 50 kΩ; for other systems, it varied between the 5–20 kΩthreshold, with a high distribution across systems and studies in general (5–100, M=22.40, SD =22.31). EEG data were recorded at various sampling rates, ranging from 200 to 2,048 Hz. Most studies did not report on downsampling procedures (n=55); if reported, we recorded values between 256 and 500 Hz. While the reference Frontiers in Neuroscience | www.frontiersin.org 4June 2022 | Volume 16 | Article 898800 Amora et al. Visual Word N170w Systematic Review FIGURE 1 | PRISMA flow diagram of the article search, screening, and selection methods. Design adapted from Page et al. (2021). electrodes used varied across studies (e.g., mastoid, nose tip, Cz, and Biosemi CMS/DRL), re-referencing to the average was a common practice (n=50) as preprocessing step. Other rereferencing methods were reported as Cz, average of mastoids, and multi-electrode referencing (Simon et al., 2007: using 20 out of 32 electrodes, F7, F3, C3, T3, CP3, TP7, T5, P3, F8, F4, C4, T4, CP4, TP8, T6, P4, Fz, Cz, Cpz, and Pz). During recording, common online filtering ranged between 0.1 and 100 Hz. Further, low- (20–48 Hz) and high-pass (0.01–1Hz) filters were applied. Common baseline windows ranged between 50 and 500 ms prestimulus, whereas the most used time frames for baseline were at 100 ms (n=28) and 200 ms (n=18) pre-stimulus onset. A difference between the applied baseline windows was visible between pre-literate and other age groups (Mprelit= −112.5, SD =13.36, Mother = −154.68, SD =81.50), possibly related to the small number of papers (n =8) targeting pre-literate population. Independent Component Analysis (ICA) for ocular artifacts and automated artifact rejection with threshold (between ±80 and 125 µV) was commonly reported; if manual rejection was performed, it was commonly performed in combination with another approach. The number of trials included after artifact rejection was sparsely reported. Regarding the further analysis, the epochs around the target word varied across studies, ranging in the length of the epochs from 250 ms to 2 s, M= −158.98 ms (−500–0) to M= 860.03 ms (250–1,550). The timeframe in which the peak of N170w was obtained in studies regarding the three age groups differed significantly between adult and child groups (pre-literate children: 175–238.5, M=216.56, SD =20.53; school-aged children: 175–238.5, M=215.25, SD =16.43; adults: 150–270, M=183.01, SD =22.29). These studies have mostly used either global field power (GFP) analyses (n=23), visual peak detection Frontiers in Neuroscience | www.frontiersin.org 5June 2022 | Volume 16 | Article 898800 Amora et al. Visual Word N170w Systematic Review FIGURE 2 | Distribution of included studies across publication years. (n=14), or literature reviewing (n=7) for selection of the N170w time window. The regions of interest (ROI) examined for N170w have varied across studies, though most studies focused on P7 (n=47), P8 (n=38), and O1 (n=36). N170w amplitudes were obtained using the mean amplitude of the identified ERP time window (n=37) or maximum peak amplitude within the ERP time window (n=21). A lack of reported mean values of the N170w amplitudes to words was observed in most studies, with reliance on the presentation of the mean amplitudes in graphs and ERP waveforms. This form of presentation led to the analysis of N170w amplitude being limited to a qualitative approach of the presented graphs, as also presented statistical results did not include word condition only results. Statistical Analysis Forty of the reviewed studies obtained their statistical results by applying analysis of variance (ANOVA). Multivariate analysis of variance (MANOVA) was performed in six studies. GreenhouseGeisser, Tukey HSD, or Bonferroni corrections were mentioned to be applied by nine studies. Linear models were in the minority, with three applications across studies. Meanwhile, a ttest as a lone standing evaluation of N170w specific values was reported by two studies. Between-subject factors across studies were group, age, gender, reading level, hearing level, and others. Within-subject factors mainly consisted of condition and stimuli features and hemispheres/electrode site. Commonly, the study design and statistical computations were not designed to be investigating the N170 response to words alone. Results of Individual Studies The full details of the extracted results can be found in Supplementary Table S3. N170w in Typically Developing vs. Developmental Reading Disorder/Poor Readers Results are reviewed by age group relative to the number of studies that compared different reading ability groups (typically developing: TD, and atypically developing such as developmental reading disorder/poor readers/low reading ability: DRD/PR). Some studies that used the term “Developmental Dyslexia/Dyslexia” are referred to as DRD in this paper. Amplitude, latency, and lateralization comparisons for each age group are displayed in Tables 1,2. Amplitude Forty studies investigated the N170w amplitude in TD and DRD/PR. A total of 29 studies compared the N170w amplitudes between TD and DRD/PR individuals in pre-literate children (n =3), school-aged children (n=14), or young adults (n=12). In pre-literate children, only three studies investigated the N170w between TD and at risk of DRD/PR. Studies revealed contradictory results, wherein one found larger N170w amplitudes in controls (Li et al., 2013), and two found no amplitude differences between TD and at-risk of DRD/PR groups (Maurer et al., 2007; Brem et al., 2013). Thirty-one studies explored the N170w in school-aged children, of which 14 compared TD with DRD/PR. Five studies showed a larger N170w amplitude for DRD/PR as compared to controls (Brem et al., 2013; Fraga González et al., 2014, 2016b; Zhao et al., 2014; van Setten et al., 2019), five showed a larger N170w amplitude for controls than DRD/PR (Maurer et al., 2007, 2011; Jucla et al., 2010; Kast et al., 2010; Bakos et al., 2018), and four showed no difference (Araújo et al., 2012; Hasko et al., 2013; Kemény et al., 2018; Pleisch et al., 2019). One specific study further divided the TD and DRD children into young (Mage =8.3) and old (Mage =11.4) sub-groups and found that in younger groups, TD exhibited a more negative N170w Frontiers in Neuroscience | www.frontiersin.org 6June 2022 | Volume 16 | Article 898800 Amora et al. Visual Word N170w Systematic Review TABLE 1 | N170w Amplitude and Latency results in comparing TD and DRD/PR by age group. Studies Amplitude (N=29) Latency (N=7) C>DRD/PR C <DRD/PR C =DRD/PR Total C >DRD/PR C <DRD/PR C =DRD/PR Total Pre-literate 1 0 2 3 – – – 0 School-aged 5 5 4 14 1 – 4 5 Young adults 11 1 (right)* 1 (left)* 12 – 2 – 2 Counts in each column refer to the number of studies reporting that result. *Different sub-groupings in one study (Dujardin et al., 2011). TABLE 2 | N170w Lateralization results in comparing TD and DRD/PR by age group. Studies Lateralization (N=20) C=left DRD/PR =equal C=right DRD/PR =equal C=left DRD/PR =right C=equal DRD/PR =right No difference Pre-literate (n=2) 1 0 0 1 0 School-aged (n=11) 1 3 0 0 4 (bilateral), 2 (left), 1 (right) Young adults (n=7) 6* 0 1* 0 2 (left)* Counts in each column refer to the number of studies reporting that result. *Different sub-groupings in one study (Dujardin et al., 2011: C, left, DRD1, left at trend level, DRD2, bilateral; Mahé et al., 2013: C, left; PR, bilateral, DRD, right at trend level). than DRD/PR, whereas the opposite pattern was found for older children (Maurer et al., 2011). Forty-two studies investigated the N170w amplitude in young adults, of which 12 compared TD and DRD/PR groups. Eleven studies showed that controls exhibited a larger, thus more negative, N170w than DRD/PR subgroups (Savill and Thierry, 2011a,b; Korinth et al., 2012; Mahé et al., 2012, 2013; Waldie et al., 2012; González-Garrido et al., 2014; Korinth and Breznitz, 2014; Araújo et al., 2015; van Setten et al., 2016; Collins et al., 2017). One specific study examined two subgroups of people with DRD based on the inspection of the ERPs; one that exhibited an N170 but no N320 and one with the two waves fused together (Dujardin et al., 2011). The authors found no difference on N170w amplitudes between TD and the first subgroup of DRD over the left hemisphere, but the latter showed more negativity than the former on the right hemisphere electrodes. Latency Only 20 out of 69 selected studies explored the latency of the N170w. Thirteen of these provided specific mean latency values. Reported latency results were mainly from the studies comparing different groups (TD vs. DRD/PR or age). Some studies also analyzed the N170w latency values regarding hemispheric distribution (left vs. right) within participant groups. Eight studies compared the mean N170w latencies of TD and DRD/PR groups. No such studies were conducted in pre-literate TD and at-risk of DRD/PR children. In school-aged children, four studies showed similar mean latencies for both TD and DRD/PR groups (Kast et al., 2010; Maurer et al., 2011; Hasko et al., 2013; Zhao et al., 2014), whereas one study reported that controls had longer mean latencies than DRD (van Setten et al., 2019). In young adults, two studies reported longer mean latencies for DRD than controls (Savill and Thierry, 2011a; Waldie et al., 2012). van Setten et al. (2016, 2019) were interested in the assumed interaction of mean N170w latency and hemispheric distribution in TD and DRD groups and found a significantly longer mean N170w latency in the right hemisphere compared to the left in both TD and DD/PR groups in young adults and schoolaged children. Lateralization Out of all the selected 69 studies, 61 investigated the lateralization of the N170w. However, only 20 compared the lateralization between typically developing and reading impaired participants. In pre-literate children, two studies compared the N170w lateralization between TD and at-risk of PR. Li et al. (2013) reported a left-lateralized N170w for controls, but bilateral activity in at-risk of PR. In contrast, Brem et al. (2013) found bilateral activity for pre-literate controls and a right-dominated N170w, although only at a trend level for pre-literate at-risk of PRs. Twenty-seven studies investigated the lateralization of the N170w in school-aged children, of which 11 compared TD and DRD/PR groups. Out of the 11 studies, seven studies showed no difference in hemispheric dominance of the N170w between TD and DRD/PR children: four studies reported bilateral activation (Jucla et al., 2010; Hasko et al., 2013; Kemény et al., 2018; Pleisch et al., 2019), two reported left (Maurer et al., 2011; Araújo et al., 2012) and one reported right activation preponderance (van Setten et al., 2019) in both groups. The remaining four studies Frontiers in Neuroscience | www.frontiersin.org 7June 2022 | Volume 16 | Article 898800 Amora et al. Visual Word N170w Systematic Review reported either left (Kast et al., 2010) or right-lateralization (Fraga González et al., 2014, 2016b; Zhao et al., 2014) for controls only, but found bilateral activity in DRD/PR children. To conclude, lateralization in DRD/PR school-aged children was mainly reported to be bilateral (n=8) and control school-aged children appeared to show left, right and bilateral dominance (n =11, n=7, n=12). Thirty-six studies on N170w lateralization were found in young adults. Seven of these compared TD and DRD/PR groups, of which six studies showed left lateralization of the N170w for the controls and a bilateral activation for DRD/PR groups (Dujardin et al., 2011; Mahé et al., 2012, 2013; González-Garrido et al., 2014; Araújo et al., 2015; Collins et al., 2017). Aside from bilateral activation, the other DRD subtype in Dujardin and colleagues’ (2011) study showed left lateralization of the N170w, though at trend level only. Moreover, one study showed left-lateralization for both TD and DRD (van Setten et al., 2016), and another study found left-lateralization for controls but investigated poor readers and adults with DRD separately and found that the former exhibited a bilateral activation of the N170w whereas the latter showed a right-lateralized N170w at trend level (Mahé et al., 2013). These results indicate a clear left-hemispheric distribution for typical reading adults (n=33), with more bilateral distribution occurrences in reading impaired adults (n=6). N170w From Pre-literate Age to Adulthood Eighteen studies gave additional insights on the development of N170w amplitude by including different age groups using a crosssectional or longitudinal design. These studies mainly evaluated control subjects (Maurer et al., 2005, 2006, 2007, 2011; Brem et al., 2006, 2009, 2013; Spironelli and Angrilli, 2009; Van Strien et al., 2009; Cao and Zhang, 2011; Cao et al., 2011; Dundas et al., 2014; Coch and Meade, 2016; Eberhard-Moscicka et al., 2016; Tong et al., 2016a; Curzietti et al., 2017; van Setten et al., 2019; Zhao et al., 2019). Amplitude Only two studies compared the N170w across pre-literate age, school-aged, and adulthood in typically developing individuals (Maurer et al., 2006; Eberhard-Moscicka et al., 2016). Eberhard-Moscicka et al. (2016) investigated the development of the N170w in the context of foreign language learning (English). However, the results in this review only included N170w response to the stimuli in the native language, German. Both authors found that N170w amplitudes consistently decreased in adults. However, two studies showed a reversed effect in the children groups, wherein Eberhard-Moscicka et al. (2016) showed a decrease of N170w amplitude from pre-literate to school-children, and Maurer et al. (2006) found the opposite: school-aged children produced a larger N170w amplitude compared to pre-literate children. Two other studies included TD school-aged children, adolescents (Mage =16.2 years), and adults: the adolescents exhibited a larger N170w compared to adults (Brem et al., 2006, 2009) but smaller when compared to school-aged children (Brem et al., 2009). Eleven studies compared two TD age groups. Maurer et al. (2007) found that pre-literate children exhibited smaller N170w amplitudes than school-aged children. Five studies compared TD school-aged children and adults (Spironelli and Angrilli, 2009; Cao and Zhang, 2011; Cao et al., 2011; Coch and Meade, 2016; van Setten et al., 2019), whereas one study compared pre-literate children and TD adults (Maurer et al., 2005). All found similar results, i.e., larger N170w amplitudes in children compared to adults. In addition, four papers compared young (Mage=8) and old school-aged (Mage =11) children and collectively corroborated the finding of Maurer et al. (2011), i.e., larger N170w amplitudes in younger children compared to the older group (Van Strien et al., 2009; Cao et al., 2011; Tong et al., 2016a; Zhao et al., 2019). One study divided the adults into young (20–30 years old) and old (>40 years old) groups, wherein the latter exhibited a larger N170w than the former (Curzietti et al., 2017). Lastly, one study compared gender differences, with boys showing larger N170w amplitude than girls (Spironelli et al., 2010). Latency Six studies compared the mean latencies of two or three age groups. Five of these showed that the N170w peaked earlier in adults than in pre-literate children (Maurer et al., 2005), schoolaged children (Brem et al., 2009; Cao and Zhang, 2011; Cao et al., 2011), and adolescents (Brem et al., 2006). Only one study showed similar mean latencies in school-aged children and adults (Coch and Meade, 2016). Five studies investigated the interaction of mean latency and hemispheric distribution of the N170w. Three studies were conducted on pre-literate children and revealed opposite results. (Zhao et al., 2015) reported in their training study that the N170w occurred later over the right than the left hemisphere for the visual learning group (visual identification of characters); however, they saw a reversed pattern in the writing condition group (manual tracing and copying of characters) at the pretest phase before training. The same research group (Zhao et al., 2018) found, according to their earlier finding, that the N170w latency was only slightly delayed in the right hemisphere compared to the left (Zhao et al., 2018), and another study did not find any latency differences between the hemispheres (Maurer et al., 2005). To examine whether the reported latencies across studies differed significantly between the hemispheres, we conducted a two-tailed t-test, which did not reveal significant differences across the three studies presented for pre-literate children (Mleft =215.5, SDleft =7.5; Mright =217.2, SDright = 5.1). Two studies divided their school-aged sample into a young and old subgroup (Maurer et al., 2011; Tong et al., 2016a). Maurer et al. (2011) found a longer latency for the younger children compared to the older ones, whereas Tong et al. (2016a) reported the opposite pattern. However, school-aged children generally showed nearly no differences in the mean N170w latencies between the left and right hemispheres (Mleft =214.7 ms, Mright =215.5 ms). For young adults, controversial latency values have been reported, with a longer mean latency of the N170w over the right hemisphere than the left in one study (van Setten et al., 2016), and the opposite was observed in another one (Xue et al., Frontiers in Neuroscience | www.frontiersin.org 8June 2022 | Volume 16 | Article 898800 Amora et al. Visual Word N170w Systematic Review words. For a recent review of fixation-related potentials and reading, one can explore Degno and Liversedge (2020). Lastly, dyslexia screening and assessment tools varied widely across the included studies, yielding different criteria to classify participants as reading impaired or typical reader. This variation might be important to consider in comparing results due to the possibility of different degrees of reading difficulties, as well the potential inclusion of different DRD subtypes. Previous studies successfully identified subtypes of DRD using learning algorithms such as mixed modeling (Torppa et al., 2007), latent profile analysis (Wolff, 2010) and confirmatory latent profile analysis (Niileksela and Templin, 2019). Although it would be interesting to see how DRD subtypes affect N170w development, this might be challenging in brain research due to lower sample sizes. Only two studies in the current review looked into subtypes; One study looked into specific difficulties in reading and spelling (Kemény et al., 2018) but did not find significant differences between the reading and spelling deficit groups, and Dujardin et al. (2011) identified dyslexia subgroups on the basis of N170 but not on the basis of their reading related skills as those did not yield a significant difference. CONCLUSION This review provides a more comprehensive overview of the development of the N170w across age groups (pre-literate age, school-aged and adulthood) and reading abilities (typically developing, developmental reading disorders/ developmental dyslexia/poor readers), as well as the response of N170 between word and word-like stimuli. Lastly, we discussed theoretical and methodological differences and challenges in the field to guide future research. Results showed that in adult studies, N170w amplitude is more negative in the controls than the poor readers, although mixed results were reported for children with varying reading ability. N170w lateralization is also in question, as leftlateralization is more straightforwardly reported in typical adults but still variable during childhood. Lastly, N170w vs. other wordlike conditions gave mixed results across studies, depending on the investigated hemisphere, stimuli and tasks employed, as well as linguistic variables. DATA AVAILABILITY STATEMENT The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author/s. AUTHOR CONTRIBUTIONS KA and VC: conceptualization. KA, AT, CV, JT, PL, and VC: protocol writing, revisions, and writing—revision and editing. KA, AT, and CV: database search, synthesis of results, analysis, and writing—original draft. All authors contributed to the article and approved the submitted version. FUNDING This research was funded by the Neo-PRISM-C project (European Union Horizon 2020 Program, H2020-MSCA-ITN2018) under the Marie Skłodowska-Curie Innovative Training Network (Grant Agreement No. 813546). SUPPLEMENTARY MATERIAL The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fnins. 2022.898800/full#supplementary-material REFERENCES Araújo, S., Bramão, I., Faísca, L., Petersson, K. M., and Reis, A. (2012). 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