1.1 Reading, executive functions, and visual attention

Developmental dyslexia (henceforth, dyslexia) is a heritable neurodevelopmental disorder affecting 5–12% of children (Peterson & Pennington, 2015). It is characterized by an impaired reading acquisition that cannot be explained by deficient neurological or sensorial functioning or below-average intelligence (American Psychiatric Association, 2015). Vast scientific research has been conducted aiming to clarify its etiology and provide effective treatment. However, there is a controversy regarding the most effective type of intervention (Peters, De Losa, Bavin, & Crewther, 2019; Peterson & Pennington, 2015). This controversy is partly due to several components involved in the reading process.

The Simple View of Reading model divides the reading process into decoding skills and language comprehension, both contributing to reading comprehension (Hoover & Gough, 1990). These two components are of equal importance, both being necessary for reading success and none of them being sufficient by itself (Hoover & Gough, 1990). Decoding is defined as efficient word recognition, that is, the ability to access the appropriate mental lexicon representation from a printed series of graphemes (Hoover & Gough, 1990). Language comprehension is the ability to understand language, to derive and interpret the relevant information from a complex linguistic stimulus. The Simple View of Reading was selected as the supporting framework for our analyses for two main reasons: first, other models like the Componential Model of Reading and different interactive reading models, such as Goodman's model, seem to be influenced greatly by the Simple View of Reading and their main claims included in this model (Harm & Seidenberg, 2004; Joshi, 2019). Second, the Simple View of Reading has received extensive empirical support and has been updated recently, including executive functions (EF) as a relevant factor (Spencer, Richmond, & Cutting, 2020).

An updated version of the model suggested the involvement of EF as a contributor to reading comprehension—specifically working memory and cognitive flexibility (Spencer et al., 2020). EFs are an umbrella term for a set of mental abilities allowing individuals to engage in goal-directed behavior and respond to new situations in an adaptive manner (Cristofori, Cohen-Zimerman, & Grafman, 2019). Reading requires a multitude of different processes including various EFs, such as the ability to retain and manipulate phonological information (i.e., working memory), the ability to repress multiple competing lexicon entries crowding in on consciousness (i.e., inhibition), and the capability to shift between multiple sources of orthographic, phonological, and semantic information (i.e., cognitive flexibility) (Spencer et al., 2020). Furthermore, the development of EF is tightly connected to reading development and reading difficulties: impairments in inhibition, working memory, shifting, planning, speed of processing and attention have been related to dyslexia (Farah, Ionta, & Horowitz-Kraus, 2021).

Arguably, the main challenge in dyslexia is a deficient decoding skill (oral language comprehension is typically more intact), which has been traditionally considered as a phonological system dysfunction (Langerberg et al., 2000; Melby-Lervag, Lyster, & Hulme, 2012). According to the phonological deficit hypothesis, the decoding deficit in dyslexia (compared with typical reading) stems from an impairment in phonological awareness, defined as the ability to think, reflect and manipulate the sounds in speech (Preston & Edwards, 2010). However, the multifactorial nature of the disorder has been elaborated to include additional challenges. Research has shown that deficits in phonological awareness and reading fluency, defined as fast and accurate reading, which traditionally were considered as dyslexia's core features (Peterson & Pennington, 2012), are not the exclusive impairments suffered by individuals with dyslexia. Deficits in nonverbal processing, such as impaired visual attention (Facoetti, Corradi, Ruffino, Gori, & Zorzi, 2010; Franceschini, Gori, Ruffino, Pedrolli, & Facoetti, 2012) and multiple EF (Smith-Spark, Henry, Messer, Edvardsdottir, & Ziecik, 2016) have been reported as well.

There is a large amount of experimental data suggesting that the reading deficit in dyslexia is closely linked to EF: children with dyslexia often show reduced EF when compared to age-matched typical readers (TR) (Barbosa, Rodrigues, Mello, Silva, & Bueno, 2019). Individuals with dyslexia show impaired EF such as inhibition, working memory (Brosnan et al., 2002), and shifting (Hari & Renvall, 2001), among others. Furthermore, EF-related brain regions show lower connectivity indices in children with dyslexia in comparison with TR (Horowitz-Kraus, Buck, & Dorrmann, 2016). EF rely on the executive component of the attention system of the brain (Petersen & Posner, 2012). Several brain networks (e.g., fronto-parietal network, cingulo-opercular network) play an extensive role in setting goals, choosing a behavioral response, and monitoring the executed plan (Petersen & Posner, 2012). Midline cortex areas (anterior cingulate cortex, medial frontal gyrus), the dorsolateral prefrontal cortex, and the posterior parietal cortex constitute the executive component of the attention system (Petersen & Posner, 2012; Smith et al., 2009).

Visual attention is defined as the process by which one item—the target—is selected for analysis from among several competing items or distractors (American Psychiatric Association, 2007). Visual attention is sustained by the orienting component of the attention system (Petersen & Posner, 2012). The orienting component, comprised of the dorsal attention network (DAN) and ventral attention networks (VANs), supports the ability to prioritize sensory input and to shift attention, and accounts for both bottom-up reorienting processes and top-down visuospatial functions (Petersen & Posner, 2012). Active visual reorienting is required for reading; precise gaze direction characterizes fluent reading (Biscaldi, Fischer, & Hartnegg, 2016). Visual orienting occurs when attention is directed to a given spatial location. This process can occur overtly (with eye movements) or covertly—when the facilitation toward a visual location exists, without convergent visual gaze toward this location (Petersen & Posner, 2012; Posner & Petersen, 1990). The orienting attention network includes distinct areas within the frontal and parietal lobules, such as the inferior frontal gyrus (IFG), frontal eye fields, posterior parietal lobe, and the temporoparietal junction (Corbetta & Shulman, 2002).

The literature suggests that visual attention impairment plays a key role in the reading difficulties of individuals with dyslexia: children with dyslexia show deficits in distinct visual abilities such as visual perception, visual temporal processing, and the rapid engagement of attention (Peters et al., 2019). In the pre-reading stage, visual attention abilities are predictive of reading acquisition (Facoetti et al., 2010; Franceschini et al., 2012). For these reasons, visual attention is a basic skill for reading development, as was also previously demonstrated neurobiologically by highlighting the increased functional connections between the dorsal attention system and the putative visual word form area (VWFA) over development and in relations to reading ability (Vogel, Petersen, & Schlaggar, 2014). Several authors support the hypothesis that faulty activity of visual pathways is a fundamental cause of dyslexia and argue against the assumption that a phonological deficit per se is the cause of reading deficiencies (Lawton, 2016; Vidyasagar, 2019; Vidyasagar & Pammer, 2010). As such, a greater reliance on visual attention-related brain regions seems to be beneficial for reading performance (Horowitz-Kraus, DiFrancesco, Kay, Wang, & Holland, 2015).

1.2 Neurobiological correlates for EFs and visual attention difficulties in dyslexia

Dyslexia has been related to reduced activity in different areas of the reading network, comprising left ventral occipito-temporal and perisylvian areas such as the inferior parietal, IFG, inferior and middle temporal lobules (IPL, IFG, ITL, and MTL, respectively), fusiform regions (Norton, Beach, & Gabrieli, 2015; Richlan, Kronbichler, & Wimmer, 2009), and the putative VWFA—which was found to be linked to the dorsal attention system in relations to reading skills (Vogel et al., 2014). Some of the constituent regions of the reading network are also key nodes within the VAN and DAN, namely distinct areas within the parietal and frontal lobes (Igelstrom & Graziano, 2017).

Existing literature suggests that stronger functional connections between higher-order cognitive, visual, and language-related areas are related to improved reading ability, both at rest (Krishnamurthy et al., 2019; Stevens, Kravitz, Peng, Tessler, & Martin, 2017) and during reading (Schurz et al., 2015). In the same vein, atypical functional connectivity (specifically lower connectivity) between these areas has been described in children and adults with dyslexia (Finn et al., 2014). The areas reported in previous research include the fusiform gyrus, the IFG, the middle and superior temporal lobe, and more. Noteworthy, as already mentioned, most of these areas are constituent regions of the DAN and VAN. Taken together, the aforementioned experimental evidence suggests that the reading deficiencies in children with dyslexia are related to brain regions involved in visuo-attentional processes. Inefficient functioning of these areas might be provoking an abnormal serial selection of the graphemes within a word further impeding the individual to read fluently and accurately. In the current work, we aim to describe the neurobiological correlates for the visual attention deficit in individuals with dyslexia.

The traditional approach to the study of brain networks architecture is based on resting-state functional magnetic resonance imaging (fMRI) data. A different methodology, termed task-residual functional connectivity, has been developed in recent years (Fornito, Harrison, Zalesky, & Simons, 2012; Tran et al., 2018). This method can be defined as: functional connectivity analysis based on blood oxygenated level-dependent (BOLD) signal registered during the performance of a task. Cognitive brain networks can be identified and analyzed by correlating the BOLD timeseries of different regions-of-interest (ROIs). It has been observed that task-residuals highlight specific network patterns to a greater degree than resting-state analyses (Tran et al., 2018). Importantly, the effect of the task blocks is removed from the signal using linear regression. Subsequent functional connectivity analysis can reveal patterns of synchronous network activity characteristic of the task that the participant is performing.

Numerous studies show that visual attention trainings are capable of enhancing reading speed and accuracy in individuals with dyslexia (Facoetti, Lorusso, Paganoni, Umilta, & Mascetti, 2003; Franceschini et al., 2013; Lorusso, Facoetti, Paganoni, Pezzani, & Molteni, 2006; Peters et al., 2019). Vidyasagar and Pammer (2010) proposed that poor visual coding and deficient attentional mechanisms are the main causes of the disorder, further giving rise to deficient phonological processing and thus, poor general reading ability. According to these authors, poor phonological awareness in dyslexia “could be the result of the poor orthographic inputs feeding into the regions mediating grapheme–phoneme correspondence” (Vidyasagar & Pammer, 2010). A consensus regarding the role of visual attention in dyslexia is lacking. Several research questions guided the present investigation: Do children with dyslexia have an impairment in visual attention? How is this impairment related to the reading difficulty? Are there connectivity differences between TR and children with dyslexia in visual attention-related brain networks?

The goal of the present study is to characterize the role of visual attention during the reading process in typical and atypical readers and to add this component to the Simple View of Reading model. We will compare the functional connectivity patterns associated with visual and orienting attention in children with dyslexia and TR in a task that presents written materials in a way that triggers visual attention abilities. We will achieve that by presenting deleted text from the screen, a manipulation that was found to trigger visual attention (Breznitz et al., 2013; Karni & Sagi, 1993). Reading interventions based on deleted text reading were found to enhance reading speed (Horowitz-Kraus, Vannest, et al., 2014) and comprehension (Horowitz-Kraus, Cicchino, Amiel, Holland, & Breznitz, 2014). Neurobiologically, deleted text reading has been related to increased functional connectivity between cognitive-control networks and visual regions (Horowitz-Kraus et al., 2015). However, to our knowledge, functional connectivity occurring while reading deleted text has not been investigated.

We hypothesize that visual attention will play a key role in reading in both TR and children with dyslexia: the group of children with dyslexia will show impaired performance on reading and visual attention tasks. Visual attention scores will be a statistical predictor of reading scores. Furthermore, the functional connectivity between different neural systems related to visual attention and reading will be altered in children with dyslexia, when compared to TR. Specifically, we expect to find lower functional connectivity between distinct brain systems related to visual attention, that is, the DAN and VAN (the attention system) and brain regions supporting reading in children with dyslexia compared with TR. We chose the DAN and VAN defined by Power et al. (2011) to conduct our analyses.