Reading reshapes stimulus selectivity in the visual word form area.

Reading depends on a brain region known as the "visual word form area" (VWFA) in left ventral occipito-temporal cortex. This region's function is debated because its stimulus selectivity is not absolute, it is modulated by a variety of task demands, and it is inconsistently localized. We used fMRI to characterize the combination of sensory and cognitive factors that activate word-responsive regions that we precisely localized in 16 adult humans (4 male). We then presented three types of character strings: English words, pseudowords, and unfamiliar characters with matched visual features. Participants performed three different tasks while viewing those stimuli: detecting real words, detecting color in the characters, and detecting color in the fixation mark. There were three primary findings about the VWFA's response: (1) It preferred letter strings over unfamiliar characters even when the stimuli were ignored during the fixation task; (2) Compared to those baseline responses, engaging in the word reading task enhanced the response to words but suppressed the response to unfamiliar characters. (3) Attending to the stimuli to judge their font color had little effect on the response magnitudes. Thus, the VWFA is uniquely modulated by a cognitive signal that is specific to voluntary linguistic processing and is not additive. Functional connectivity analyses revealed that communication between the VWFA and a left frontal language area increased when the participant engaged in the linguistic task. We conclude that the VWFA is inherently selective for familiar orthography, but it falls under control of the language network when the task demands it.

Reading Reshapes Stimulus Selectivity in the Visual Word Form Area.

Reading depends on a brain region known as the "visual word form area" (VWFA) in the left ventral occipitotemporal cortex. This region's function is debated because its stimulus selectivity is not absolute, it is modulated by a variety of task demands, and it is inconsistently localized. We used fMRI to characterize the combination of sensory and cognitive factors that activate word-responsive regions that we precisely localized in 16 adult humans (4 male). We then presented three types of character strings: English words, pseudowords, and unfamiliar characters with matched visual features. Participants performed three different tasks while viewing those stimuli: detecting real words, detecting color in the characters, and detecting color in the fixation mark. There were three primary findings about the VWFA's response: (1) It preferred letter strings over unfamiliar characters even when the stimuli were ignored during the fixation task. (2) Compared with those baseline responses, engaging in the word reading task enhanced the response to words but suppressed the response to unfamiliar characters. (3) Attending to the stimuli to judge their color had little effect on the response magnitudes. Thus, the VWFA is uniquely modulated by a cognitive signal that is specific to voluntary linguistic processing and is not additive. Functional connectivity analyses revealed that communication between the VWFA and a left frontal language area increased when the participant engaged in the linguistic task. We conclude that the VWFA is inherently selective for familiar orthography, but it falls under control of the language network when the task demands it.

Severe processing capacity limits for sub-lexical features of letter strings.

When reading, the visual system is confronted with many words simultaneously. How much of that information can a reader process at once? Previous studies demonstrated that low-level visual features of multiple words are processed in parallel, but lexical attributes are processed serially, for one word at a time. This implies that an internal bottleneck lies somewhere between early visual and lexical analysis. We used a dual-task behavioral paradigm to investigate whether this bottleneck lies at the stage of letter recognition or phonological decoding. On each trial, two letter strings were flashed briefly, one above and one below fixation, and then masked. In the letter identification experiment, participants indicated whether a vowel was present in a particular letter string. In the phonological decoding experiment, participants indicated whether the letter string was pronounceable. We compared accuracy in a focused attention condition, in which participants judged only one of the two strings, with accuracy in a divided attention condition, in which participants judged both strings independently. In both experiments, the cost of dividing attention was so large that it supported a serial model: participants were able to process only one letter string per trial. Furthermore, we found a stimulus processing trade-off that is characteristic of serial processing: When participants judged one string correctly, they were less likely to judge the other string correctly. Therefore, the bottleneck that constrains word recognition under these conditions arises at a sub-lexical level, perhaps due to a limit on the efficiency of letter recognition.

Children with dyslexia show no deficit in exogenous spatial attention but show differences in visual encoding.

In the search for mechanisms that contribute to dyslexia, the term "attention" has been invoked to explain performance in a variety of tasks, creating confusion since all tasks do, indeed, demand "attention." Many studies lack an experimental manipulation of attention that would be necessary to determine its influence on task performance. Nonetheless, an emerging view is that children with dyslexia have an impairment in the exogenous (automatic/reflexive) orienting of spatial attention. Here we investigated the link between exogenous attention and reading ability by presenting exogenous spatial cues in the multi-letter processing task-a task relevant for reading. The task was gamified and administered online to a large sample of children (N = 187) between 6 and 17 years. Children with dyslexia performed worse overall at rapidly recognizing and reporting strings of letters. However, we found no evidence for a difference in the utilization of exogenous spatial cues, resolving two decades of ambiguity in the field. Previous studies that claimed otherwise may have failed to distinguish attention effects from overall task performance or found spurious group differences in small samples. RESEARCH HIGHLIGHTS: We manipulated exogenous visual spatial attention using pre-cues in a task that is relevant for reading and we see robust task effects of exogenous attention. We found no evidence for a deficit in utilizing exogenous spatial pre-cues in children with dyslexia. However, children with dyslexia showed reduced recognition ability for all letter positions. Children with dyslexia were just as likely to make letter transposition errors as typical readers.

The transposed word effect is consistent with serial word recognition and varies with reading speed.

The scientific study of reading has long been animated by questions of parallel vs. serial processing. Do readers recognize words serially, adding each one sequentially to a representation of the sentence structure? One fascinating phenomenon to emerge from this research is the transposed word effect: when asked to judge whether sentences are grammatical, readers often fail to notice grammatical errors caused by transposing two words. This effect could be evidence that readers recognize multiple words in parallel. Here we provide converging evidence that the transposed word effect is also consistent with serial processing because it occurs robustly when the words in each sentence are presented serially. We further investigated how the effect relates to individual differences in reading speed, to gaze fixation patterns, and to differences in difficulty across sentences. In a pretest, we first measured the natural English reading rate of 37 participants, which varied widely. In a subsequent grammatical decision task, we presented grammatical and ungrammatical sentences in two modes: one with all words presented simultaneously, and the other with single words presented sequentially at each participant's natural rate. Unlike prior studies that used a fixed sequential presentation rate, we found that the magnitude of the transposed word effect was at least as strong in the sequential presentation mode as in the simultaneous mode, for both error rates and response times. Moreover, faster readers were more likely to miss transpositions of words presented sequentially. We argue that these data favor a "noisy channel" model of comprehension in which skilled readers rely on prior knowledge to rapidly infer the meaning of sentences, allowing for apparent errors in spatial or temporal order, even when the individual words are recognized one at a time.

Engaging in word recognition elicits highly specific modulations in visual cortex.

A person's cognitive state determines how their brain responds to visual stimuli. The most common such effect is a response enhancement when stimuli are task relevant and attended rather than ignored. In this fMRI study, we report a surprising twist on such attention effects in the visual word form area (VWFA), a region that plays a key role in reading. We presented participants with strings of letters and visually similar shapes, which were either relevant for a specific task (lexical decision or gap localization) or ignored (during a fixation dot color task). In the VWFA, the enhancement of responses to attended stimuli occurred only for letter strings, whereas non-letter shapes evoked smaller responses when attended than when ignored. The enhancement of VWFA activity was accompanied by strengthened functional connectivity with higher-level language regions. These task-dependent modulations of response magnitude and functional connectivity were specific to the VWFA and absent in the rest of visual cortex. We suggest that language regions send targeted excitatory feedback into the VWFA only when the observer is trying to read. This feedback enables the discrimination of familiar and nonsense words and is distinct from generic effects of visual attention.

Oculomotor freezing indicates conscious detection free of decision bias.

The appearance of a salient stimulus rapidly and automatically inhibits saccadic eye movements. Curiously, this "oculomotor freezing" response is triggered only by stimuli that the observer reports seeing. It remains unknown, however, whether oculomotor freezing is linked to the observer's sensory experience or their decision that a stimulus was present. To dissociate between these possibilities, we manipulated decision criterion via monetary payoffs and stimulus probability in a detection task. These manipulations greatly shifted observers' decision criteria but did not affect the degree to which microsaccades were inhibited by stimulus presence. Moreover, the link between oculomotor freezing and explicit reports of stimulus presence was stronger when the criterion was conservative rather than liberal. We conclude that the sensory threshold for oculomotor freezing is independent of decision bias. Provided that conscious experience is also unaffected by such bias, oculomotor freezing is an implicit indicator of sensory awareness.NEW & NOTEWORTHY Sometimes a visual stimulus reaches awareness, and sometimes it does not. To understand why, we need objective, bias-free measures of awareness. We discovered that a reflexive freezing of small eye movements indicates when an observer detects a stimulus. Furthermore, when we biased observers' decisions to report seeing the stimulus, the oculomotor response was unaltered. This suggests that the threshold for conscious perception is independent of the decision criterion and is revealed by oculomotor freezing.

Spatial attention in encoding letter combinations.

Reading requires the correct identification of letters and letter positions within words. Selective attention is, therefore, required to select chunks of the text for sequential processing. Despite the extensive literature on visual attention, the well-known effects of spatial cues in simple perceptual tasks cannot inform us about the role of attention in a task as complex as reading. Here, we systematically manipulate spatial attention in a multi-letter processing task to understand the effects of spatial cues on letter encoding in typical adults. Overall, endogenous (voluntary) cue benefits were larger than exogenous (reflexive). We show that cue benefits are greater in the left than in the right visual field and larger for the most crowded letter positions. Endogenous valid cues reduced errors due to confusing letter positions more than misidentifications, specifically for the most crowded letter positions. Therefore, shifting endogenous attention along a line of text is likely an important mechanism to alleviate the effects of crowding on encoding letters within words. Our results help set the premise for constructing theories about how specific mechanisms of attention support reading development in children. Understanding the link between reading development and attention mechanisms has far-reaching implications for effectively addressing the needs of children with reading disabilities.

Reading: The Confluence of Vision and Language.

The scientific study of reading has a rich history that spans disciplines from vision science to linguistics, psychology, cognitive neuroscience, neurology, and education. The study of reading can elucidate important general mechanisms in spatial vision, attentional control, object recognition, and perceptual learning, as well as the principles of plasticity and cortical topography. However, literacy also prompts the development of specific neural circuits to process a unique and artificial stimulus. In this review, we describe the sequence of operations that transforms visual features into language, how the key neural circuits are sculpted by experience during development, and what goes awry in children for whom learning to read is a struggle.

Visual word recognition: Evidence for a serial bottleneck in lexical access.

Reading is a demanding task, constrained by inherent processing capacity limits. Do those capacity limits allow for multiple words to be recognized in parallel? In a recent study, we measured semantic categorization accuracy for nouns presented in pairs. The words were replaced by post-masks after an interval that was set to each subject's threshold, such that with focused attention they could categorize one word with ~80% accuracy. When subjects tried to divide attention between both words, their accuracy was so impaired that it supported a serial processing model: on each trial, subjects could categorize one word but had to guess about the other. In the experiments reported here, we investigated how our previous result generalizes across two tasks that require lexical access but vary in the depth of semantic processing (semantic categorization and lexical decision), and across different masking stimuli, word lengths, lexical frequencies and visual field positions. In all cases, the serial processing model was supported by two effects: (1) a sufficiently large accuracy deficit with divided compared to focused attention; and (2) a trial-by-trial stimulus processing tradeoff, meaning that the response to one word was more likely to be correct if the response to the other was incorrect. However, when the task was to detect colored letters, neither of those effects occurred, even though the post-masks limited accuracy in the same way. Altogether, the results are consistent with the hypothesis that visual processing of words is parallel but lexical access is serial.

The link between reading ability and visual spatial attention across development.

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.

Parallel spatial channels converge at a bottleneck in anterior word-selective cortex.

In most environments, the visual system is confronted with many relevant objects simultaneously. That is especially true during reading. However, behavioral data demonstrate that a serial bottleneck prevents recognition of more than one word at a time. We used fMRI to investigate how parallel spatial channels of visual processing converge into a serial bottleneck for word recognition. Participants viewed pairs of words presented simultaneously. We found that retinotopic cortex processed the two words in parallel spatial channels, one in each contralateral hemisphere. Responses were higher for attended than for ignored words but were not reduced when attention was divided. We then analyzed two word-selective regions along the occipitotemporal sulcus (OTS) of both hemispheres (subregions of the visual word form area, VWFA). Unlike retinotopic regions, each word-selective region responded to words on both sides of fixation. Nonetheless, a single region in the left hemisphere (posterior OTS) contained spatial channels for both hemifields that were independently modulated by selective attention. Thus, the left posterior VWFA supports parallel processing of multiple words. In contrast, activity in a more anterior word-selective region in the left hemisphere (mid OTS) was consistent with a single channel, showing (i) limited spatial selectivity, (ii) no effect of spatial attention on mean response amplitudes, and (iii) sensitivity to lexical properties of only one attended word. Therefore, the visual system can process two words in parallel up to a late stage in the ventral stream. The transition to a single channel is consistent with the observed bottleneck in behavior.

Evidence of Serial Processing in Visual Word Recognition.

To test the limits of parallel processing in vision, we investigated whether people can recognize two words at once. Participants viewed brief, masked pairs of words and were instructed in advance to judge both of the words (dual-task condition) or just one of the words (single-task condition). For judgments of semantic category, the dual-task deficit was so large that it supported all-or-none serial processing: Participants could recognize only one word and had to guess about the other. Moreover, participants were more likely to be correct about one word if they were incorrect about the other, which also supports a serial-processing model. In contrast, judgments of text color with identical stimuli were consistent with unlimited-capacity parallel processing. Thus, under these conditions, serial processing is necessary to judge the meaning of words but not their physical features. Understanding the implications of this result for natural reading will require further investigation.

Optimizing text for an individual's visual system: The contribution of visual crowding to reading difficulties.

Reading is a complex process that involves low-level visual processing, phonological processing, and higher-level semantic processing. Given that skilled reading requires integrating information among these different systems, it is likely that reading difficulty-known as dyslexia-can emerge from impairments at any stage of the reading circuitry. To understand contributing factors to reading difficulties within individuals, it is necessary to diagnose the function of each component of the reading circuitry. Here, we investigated whether adults with dyslexia who have impairments in visual processing respond to a visual manipulation specifically targeting their impairment. We collected psychophysical measures of visual crowding and tested how each individual's reading performance was affected by increased text-spacing, a manipulation designed to alleviate severe crowding. Critically, we identified a sub-group of individuals with dyslexia showing elevated crowding and found that these individuals read faster when text was rendered with increased letter-, word- and line-spacing. Our findings point to a subtype of dyslexia involving elevated crowding and demonstrate that individuals benefit from interventions personalized to their specific impairments.

Feature singletons attract spatial attention independently of feature priming.

People perform better in visual search when the target feature repeats across trials (intertrial feature priming [IFP]). Here, we investigated whether repetition of a feature singleton's color modulates stimulus-driven shifts of spatial attention by presenting a probe stimulus immediately after each singleton display. The task alternated every two trials between a probe discrimination task and a singleton search task. We measured both stimulus-driven spatial attention (via the distance between the probe and singleton) and IFP (via repetition of the singleton's color). Color repetition facilitated search performance (IFP effect) when the set size was small. When the probe appeared at the singleton's location, performance was better than at the opposite location (stimulus-driven attention effect). The magnitude of this attention effect increased with the singleton's set size (which increases its saliency) but did not depend on whether the singleton's color repeated across trials, even when the previous singleton had been attended as a search target. Thus, our findings show that repetition of a salient singleton's color affects performance when the singleton is task relevant and voluntarily attended (as in search trials). However, color repetition does not affect performance when the singleton becomes irrelevant to the current task, even though the singleton does capture attention (as in probe trials). Therefore, color repetition per se does not make a singleton more salient for stimulus-driven attention. Rather, we suggest that IFP requires voluntary selection of color singletons in each consecutive trial.

Evidence for unlimited capacity processing of simple features in visual cortex.

Performance in many visual tasks is impaired when observers attempt to divide spatial attention across multiple visual field locations. Correspondingly, neuronal response magnitudes in visual cortex are often reduced during divided compared with focused spatial attention. This suggests that early visual cortex is the site of capacity limits, where finite processing resources must be divided among attended stimuli. However, behavioral research demonstrates that not all visual tasks suffer such capacity limits: The costs of divided attention are minimal when the task and stimulus are simple, such as when searching for a target defined by orientation or contrast. To date, however, every neuroimaging study of divided attention has used more complex tasks and found large reductions in response magnitude. We bridged that gap by using functional magnetic resonance imaging to measure responses in the human visual cortex during simple feature detection. The first experiment used a visual search task: Observers detected a low-contrast Gabor patch within one or four potentially relevant locations. The second experiment used a dual-task design, in which observers made independent judgments of Gabor presence in patches of dynamic noise at two locations. In both experiments, blood-oxygen level-dependent (BOLD) signals in the retinotopic cortex were significantly lower for ignored than attended stimuli. However, when observers divided attention between multiple stimuli, BOLD signals were not reliably reduced and behavioral performance was unimpaired. These results suggest that processing of simple features in early visual cortex has unlimited capacity.

Oculomotor inhibition covaries with conscious detection.

Saccadic eye movements occur frequently even during attempted fixation, but they halt momentarily when a new stimulus appears. Here, we demonstrate that this rapid, involuntary "oculomotor freezing" reflex is yoked to fluctuations in explicit visual perception. Human observers reported the presence or absence of a brief visual stimulus while we recorded microsaccades, small spontaneous eye movements. We found that microsaccades were reflexively inhibited if and only if the observer reported seeing the stimulus, even when none was present. By applying a novel Bayesian classification technique to patterns of microsaccades on individual trials, we were able to decode the reported state of perception more accurately than the state of the stimulus (present vs. absent). Moreover, explicit perceptual sensitivity and the oculomotor reflex were both susceptible to orientation-specific adaptation. The adaptation effects suggest that the freezing reflex is mediated by signals processed in the visual cortex before reaching oculomotor control centers rather than relying on a direct subcortical route, as some previous research has suggested. We conclude that the reflexive inhibition of microsaccades immediately and inadvertently reveals when the observer becomes aware of a change in the environment. By providing an objective measure of conscious perceptual detection that does not require explicit reports, this finding opens doors to clinical applications and further investigations of perceptual awareness.

Stimulus competition mediates the joint effects of spatial and feature-based attention.

Distinct attentional mechanisms enhance the sensory processing of visual stimuli that appear at task-relevant locations and have task-relevant features. We used a combination of psychophysics and computational modeling to investigate how these two types of attention--spatial and feature based--interact to modulate sensitivity when combined in one task. Observers monitored overlapping groups of dots for a target change in color saturation, which they had to localize as being in the upper or lower visual hemifield. Pre-cues indicated the target's most likely location (left/right), color (red/green), or both location and color. We measured sensitivity (d') for every combination of the location cue and the color cue, each of which could be valid, neutral, or invalid. When three competing saturation changes occurred simultaneously with the target change, there was a clear interaction: The spatial cueing effect was strongest for the cued color, and the color cueing effect was strongest at the cued location. In a second experiment, only the target dot group changed saturation, such that stimulus competition was low. The resulting cueing effects were statistically independent and additive: The color cueing effect was equally strong at attended and unattended locations. We account for these data with a computational model in which spatial and feature-based attention independently modulate the gain of sensory responses, consistent with measurements of cortical activity. Multiple responses then compete via divisive normalization. Sufficient competition creates interactions between the two cueing effects, although the attentional systems are themselves independent. This model helps reconcile seemingly disparate behavioral and physiological findings.

Interactions between voluntary and involuntary attention modulate the quality and temporal dynamics of visual processing.

Successfully navigating a dynamic environment requires the efficient distribution of finite neural resources. Voluntary (endogenous) covert spatial attention selectively allocates those processing resources to goal-relevant locations in the visual scene in the absence of eye movements. However, the allocation of spatial attention is not always voluntary; abrupt onsets in the visual periphery automatically enhance processing of nearby stimuli (exogenous attention). In dynamic environments, exogenous events and internal goals likely compete to determine the distribution of attention, but how such competition is resolved is not well understood. To investigate how exogenous events interact with the concurrent allocation of voluntary attention, we used a speed-accuracy trade-off (SAT) procedure. SAT conjointly measures the rate of information accrual and asymptotic discriminability, allowing us to measure how attentional interactions unfold over time during stimulus processing. We found that both types of attention sped information accrual and improved discriminability. However, focusing endogenous attention at the target location reduced the effects of exogenous cues on the rate of information accrual and rendered negligible their effects on asymptotic discriminability. We verified the robustness of these findings in four additional experiments that targeted specific, critical response delays. In conclusion, the speed and quality of visual processing depend conjointly on internally and externally driven attentional states, but it is possible to voluntarily diminish distraction by irrelevant events in the periphery.