The link between reading ability and visual spatial attention across development

Abstract

Interacting with a cluttered and dynamic environment requires making decisions about visual information at relevant locations while ignoring irrelevant locations. Typical adults can do this with covert spatial attention: prioritizing particular visual field locations even without moving the eyes. Deficits of covert spatial attention have been implicated in developmental dyslexia, a specific reading disability. Previous studies of children with dyslexia, however, have been complicated by group differences in overall task ability that are difficult to distinguish from selective spatial attention. Here, we used a single-fixation visual search task to estimate orientation discrimination thresholds with and without an informative spatial cue in a large sample (N = 123) of people ranging in age from 5 to 70 years and with a wide range of reading abilities. We assessed the efficiency of attentional selection via the cueing effect: the difference in log thresholds with and without the spatial cue. Across our whole sample, both absolute thresholds and the cueing effect gradually improved throughout childhood and adolescence. Compared to typical readers, individuals with dyslexia had higher thresholds (worse orientation discrimination) as well as smaller cueing effects (weaker attentional selection). Those differences in dyslexia were especially pronounced prior to age 20, when basic visual function is still maturing. Thus, in line with previous theories, literacy skills are associated with the development of selective spatial attention.

Introduction

Complex and cluttered environments pose a challenge when using vision to navigate and interact: only a subset of the information entering the eyes is relevant to the task at hand. Fortunately, the brain is equipped with multiple mechanisms – generally referred to as “attention” – that prioritize relevant information and filter out irrelevant information. Selective spatial attention prioritizes information at specific locations in the scene, and is critical for everyday tasks. A prominent example is reading: pages of text are extremely cluttered, and letters are only identifiable in the central visual field (Legge et al., 2007). Even within the central visual field, it is difficult to fully process more than one word at a time (White, Palmer, & Boynton, 2018). Therefore, reading requires rapid shifts of spatial attention to select individual words on a page (Rayner, 2009).

Given its importance in reading, one might hypothesize that a deficiency in spatial attention would cause reading difficulty. In fact, many researchers have argued for an association between spatial attention and developmental dyslexia, a reading disability that affects 5–10% of the population (e.g., Bosse et al., 2007, Facoetti et al., 2000, Franceschini et al., 2012, Vidyasagar and Pammer, 2010). Some authors link the attentional deficits to a more general abnormality in the “dorsal visual stream” (e.g., Pammer et al., 2006, Vidyasagar and Pammer, 1999), based on performance in tasks thought to rely on the magnocellular visual pathway (Boden and Giaschi, 2007, Demb et al., 1998, Demb et al., 1997; Gori et al., 2015, Kevan and Pammer, 2008). However, many other etiological explanations for dyslexia have been proposed, involving the auditory system, phonological processing, or higher-level language skills (reviewed by Vellutino, Fletcher, Snowling, & Scanlon, 2004).

The goal of the present investigation was to evaluate the link between spatial attention and reading ability over development. Methods for measuring spatial attention have been inconsistent across studies of children and adults with dyslexia. That is important because visual spatial attention comes in several forms: (1) Overt spatial attention involves movements of the head and eyes to align the high-resolution fovea with task-relevant objects. While reading this page, for example, you are making roughly four rapid eye movements per second (Rayner, 2009). (2) Covert spatial attention is the selective prioritization of locations in the visual field without moving the eyes. There are two types of covert spatial attention: (a) Endogenous attention is voluntary and driven by knowledge and goals. While fixating on the word “endogenous” in the previous sentence, your attention shifted to the next word, “attention”, before your eyes moved on (Rayner, 2009). (b) Exogenous attention is involuntary, triggered by salient external events that may or may not be task-relevant, like an email notification appearing in the corner of the screen while you try to read a manuscript.

Although there is some evidence for abnormal eye movement control (overt attention) in dyslexia (e.g., Eden et al., 1994, Hawelka and Wimmer, 2005, Rayner, 1985), here we focus on covert spatial attention. During reading, endogenous covert attention is required to begin processing parafoveal words before the eyes move, to plan the saccades themselves, and perhaps even to select individual letters within fixated words (Rayner, 2009, Vidyasagar and Pammer, 2010).

In the laboratory, covert spatial attention is often studied by requiring an observer to fixate and respond to target stimuli presented in the peripheral visual field. Prior to the stimuli, a cue directs attention to one or more locations (Posner, 1980). A cue could be an arrow that points to the location most likely to contain task-relevant stimuli, or a small shape that draws attention by flashing near a potential stimulus location. The effects of covert spatial attention include increased discrimination accuracy and decreased response time when the target stimulus's location is cued compared to uncued (reviewed by Carrasco, 2011). Physiologically, neural responses are greater for stimuli at cued locations than at uncued locations (Maunsell, 2015, Reynolds and Chelazzi, 2004).

In this study, we are interested in how covert spatial attention differs between individuals with and without dyslexia, in childhood as well as in adulthood. Because our goal is to measure visual task performance across a wide age range, we must first consider more general developmental changes in visual perception and attention.

Since the 1980s, psychologists have studied the development of covert spatial attention using spatial cueing paradigms (Akhtar and Enns, 1989, Brodeur and Boden, 2000, Brodeur and Enns, 1997, Enns and Brodeur, 1989, Iarocci et al., 2009, Leclercq and Siéroff, 2013, Pearson and Lane, 1990, Plude et al., 1994, Ristic and Enns, 2015, Ristic and Kingstone, 2009, Wainwright and Bryson, 2002). Nearly all such studies assess spatial attention by comparing reaction times (RTs) across different cue conditions (e.g., valid vs invalid). The question is how the differences in RT, which index attention effects, change across development. There is a general consensus that exogenous (automatic, stimulus-driven) cueing effects are present from at least pre-school age and are stable through the lifespan. Endogenous (voluntary, top-down) cueing effects show more gradual developmental change, suggesting an increase in strategic control over spatial attention.

Beyond that, there is little agreement on the details of the time course and which internal mechanisms are changing. Some studies claim that endogenous attention becomes “adult-like” by age 10 (Goldberg et al., 2001, Landry et al., 2019, Michael et al., 2013, Ristic and Enns, 2015, Wainwright and Bryson, 2005), but others suggest later maturation (Brodeur and Enns, 1997, Leclercq and Siéroff, 2013, Schul et al., 2003).

A general challenge in this type of study is to separate developmental change in a specific mechanism of attention from developmental change in overall task performance. Younger participants tend to respond slower and less accurately to the same stimulus as older participants. Does a valid-invalid cueing effect of 50 msec reflect the same degree of attentional modulation in a 5-year-old as it does in a 20-year old? It is difficult to say, especially if their accuracies differ. Several previous studies have attempted to address this difficulty, for instance by normalizing RTs across age groups (Gaspelin et al., 2015, Goldberg et al., 2001). It remains an open question, however, whether the mechanisms of selective spatial attention develop independently of basic visual sensitivity and task performance.

Moreover, cueing effects on reaction times could have many underlying causes: change in the quality of the sensory representation, the speed of evidence accumulation, response bias, and/or motor preparation. Only a handful of developmental studies have focused on how spatial cues affect detection or discrimination accuracy (Akhtar and Enns, 1989, Brodeur and Boden, 2000, Schul et al., 2003), which can give more information about the underlying mechanisms. Even then, it is difficult to compare cueing effects in units of proportion correct across groups that differ in their absolute levels of accuracy. The conclusion depends on an interaction between cue condition and age. Such interactions are difficult to interpret if the measurement (e.g., differences in proportion correct) may not be linearly related to the theoretical variable of interest (e.g., the effect of attention on visual processing; Loftus, 1978).

Studies that compare spatial attention across good and poor readers face the same challenges as studies that compare across age groups. Many in the past have not precisely specified what differs in dyslexic individuals: overall visual sensitivity, motor ability, overt eye movements, or endogenous covert selection, etc. Many rely on RTs, and the participant groups often differ in their overall performance level (e.g., people with dyslexia can have slow processing speed in general; Peterson & Pennington, 2015) as well as any putative attention effects.

One research team overcame those challenges by measuring orientation discrimination thresholds in a simple visual search task with and without an informative spatial pre-cue (Roach and Hogben, 2004, Roach and Hogben, 2007, Roach and Hogben, 2008). The participants' task was to report the tilt direction (clockwise or counterclockwise from vertical) of a single Gabor stimulus that was presented along with a variable number of vertical distractors, all equidistant from fixation (Baldassi & Burr, 2000). The display was presented briefly enough to avoid eye movements to the stimuli, and the target's location varied randomly from trial to trial. On some trials, a 100% valid spatial cue (a small dot) flashed near the target's location, just prior to the stimulus array. In each condition, the experimenters used a staircase procedure to estimate each participant's orientation discrimination threshold: the degrees of tilt required to perform the task with ∼75% correct. Without the spatial cue, thresholds rise with increasing set size, because the internal representation of each stimulus is noisy and each distractor could be mistaken for the target. With the spatial cue, thresholds in control participants are much lower (better performance) and less affected by increasing set size. This difference in threshold represents the benefit of spatial attention: the cue allows the participant to base their decision primarily on information at the target's location and exclude noise from the distractors (Roach and Hogben, 2007, Roach and Hogben, 2008).

Roach & Hogben found that although adults with dyslexia performed normally in the uncued condition, their thresholds were abnormally high (worse performance compared to control subjects) in the cued condition. In other words, adults with dyslexia failed to capitalize on the information conveyed by the cue to reduce uncertainty about the target's location. Thresholds in the cued condition distinguished adults with dyslexia from controls better than a variety of other psychophysical and widely used clinical measures (Roach & Hogben, 2007). The difference between good and poor readers was strongest when the set size was largest (16 items). Importantly, the stimuli were not linguistic, which avoided a potential confound in comparing performance between good and poor readers. Overall, Roach & Hogben provided some of the strongest evidence to date that adults with dyslexia have an impairment in covert spatial attention.

One unusual feature of this paradigm is that the peripheral cue could potentially trigger both exogenous and endogenous spatial attention. The cue could be exogenous because it appears peripherally, adjacent to and immediately before the target. It could be endogenous because it always indicates the target's location, so the participant can use that information to voluntarily select the most relevant information. Based on a series of additional experiments, Roach and Hogben (2008) concluded that the primary mechanism of the cueing effect in this paradigm is endogenous. We therefore chose to use this paradigm because the interval between the cue and the stimuli is short enough to prevent eye movements to the target, a potential pitfall when studying covert attention in young children. We will return to the endogenous versus exogenous question in the Discussion.

We adapted and extended Roach and Hogben's (2007) method to study the development of covert spatial attention and how it differs in children and adults with dyslexia. Although Roach & Hogben focused on set size 16, we used a fixed set size of 8 items in the cued and uncued conditions. With a larger set size, performance may be limited by crowding, which is also known to differ in dyslexia (Callens et al., 2013, Cassim et al., 2014, Gori and Facoetti, 2015, Joo et al., 2018, Moores et al., 2011). In addition, we increased the size and duration of the cue and made it red, so it would be salient enough for younger participants. In a subset of adult participants we also replicated a condition with the small black cue used by Roach and Hogben, 2004, Roach and Hogben, 2007. Finally, we added a “single stimulus” condition, in which the tilted target is presented alone.

There are advantages to measuring thresholds, which are “stimulus-referred” measurements, rather than reaction time or accuracy with a fixed stimulus. First, we set the stimulus difficulty on each trial with an adaptive staircase that converged on the orientation difference that yields ∼75% correct performance. The level of overall task difficulty was therefore equalized across participants, regardless of age or reading skill. Second, we fit psychometric functions with separate parameters for the threshold and the upper asymptote. The latter parameter can capture differences in the participants' abilities to stay engaged and follow instructions. Third, we operationalized the effect of attention as the difference in log thresholds between cued and uncued conditions, which can be theoretically linked to a difference in the noise of the internal representations used to make the perceptual decision (see the Supplemental Material). That helps us interpret the interactions between cue condition and age or reading ability. Finally, thresholds in the single stimulus condition provide a baseline measure of group differences in the ability to make fine visual discriminations, independent of attention.