Both mOTS-words and pOTS-words prefer emoji stimuli over text stimuli during a lexical judgment task.

The visual word form area in the occipitotemporal sulcus (here OTS-words) is crucial for reading and shows a preference for text stimuli. We hypothesized that this text preference may be driven by lexical processing. Hence, we performed three fMRI experiments (n = 15), systematically varying participants' task and stimulus, and separately evaluated middle mOTS-words and posterior pOTS-words. Experiment 1 contrasted text with other visual stimuli to identify both OTS-words subregions. Experiment 2 utilized an fMRI adaptation paradigm, presenting compound words as texts or emojis. In experiment 3, participants performed a lexical or color judgment task on compound words in text or emoji format. In experiment 2, pOTS-words, but not mOTS-words, showed fMRI adaptation for compound words in both formats. In experiment 3, both subregions showed higher responses to compound words in emoji format. Moreover, mOTS-words showed higher responses during the lexical judgment task and a task-stimulus interaction. Multivariate analyses revealed that distributed responses in pOTS-words encode stimulus and distributed responses in mOTS-words encode stimulus and task. Together, our findings suggest that the function of the OTS-words subregions goes beyond the specific visual processing of text and that these regions are flexibly recruited whenever semantic meaning needs to be assigned to visual input.

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.

Relationship Between Resting State Functional Connectivity and Reading-Related Behavioural Measures in 69 Adults.

In computational models of reading, written words can be read using print-to-sound and/or print-to-meaning pathways. Neuroimaging data associate dorsal stream regions (left posterior occipitotemporal cortex, intraparietal cortex, dorsal inferior frontal gyrus [dIFG]) with the print-to-sound pathway and ventral stream regions (left anterior fusiform gyrus, middle temporal gyrus) with the print-to-meaning pathway. In 69 typical adults, we investigated whether resting state functional connectivity (RSFC) between the visual word form area (VWFA) and dorsal and ventral regions correlated with phonological (nonword reading, nonword repetition, spoonerisms), lexical-semantic (vocabulary, sensitivity to morpheme units in reading), and general literacy (word reading, spelling) skills. VWFA activity was temporally correlated with activity in both dorsal and ventral reading regions. In pre-registered whole-brain analyses, spoonerisms performance was positively correlated with RSFC between the VWFA and left dorsal regions (dIFG, superior parietal and intraparietal cortex). In exploratory region-of-interest analyses, VWFA-dIFG connectivity was also positively correlated with nonword repetition, spelling, and vocabulary. Connectivity between the VWFA and ventral stream regions was not associated with performance on any behavioural measure, either in whole-brain or region-of-interest analyses. Our results suggest that tasks such as spoonerisms and spellings, which are both complex (i.e., involve multiple subprocesses) and have high between-subject variability, provide greater opportunity for observing resting-state brain-behaviour associations. However, the complexity of these tasks limits the conclusions we can draw about the specific mechanisms that drive these associations. Future research would benefit from constructing latent variables from multiple tasks tapping the same reading subprocess.

Reading instruction causes changes in category-selective visual cortex.

Education sculpts specialized neural circuits for skills like reading that are critical to success in modern society but were not anticipated by the selective pressures of evolution. Does the emergence of brain regions that selectively process novel visual stimuli like words occur at the expense of cortical representations of other stimuli like faces and objects? "Neuronal Recycling" predicts that learning to read should enhance the response to words in ventral occipitotemporal cortex (VOTC) and decrease the response to other visual categories such as faces and objects. To test this hypothesis, and more broadly to understand the changes that are induced by the early stages of literacy instruction, we conducted a randomized controlled trial with pre-school children (five years of age). Children were randomly assigned to intervention programs focused on either reading skills or oral language skills and magnetoencephalography (MEG) data collected before and after the intervention was used to measure visual responses to images of text, faces, and objects. We found that being taught reading versus oral language skills induced different patterns of change in category-selective regions of visual cortex, but that there was not a clear tradeoff between the response to words versus other categories. Within a predefined region of VOTC corresponding to the visual word form area (VWFA) we found that the relative amplitude of responses to text, faces, and objects changed, but increases in the response to words were not linked to decreases in the response to faces or objects. How these changes play out over a longer timescale is still unknown but, based on these data, we can surmise that high-level visual cortex undergoes rapid changes as children enter school and begin establishing new skills like literacy.

The transition from vision to language: Distinct patterns of functional connectivity for subregions of the visual word form area.

Reading entails transforming visual symbols to sound and meaning. This process depends on specialized circuitry in the visual cortex, the visual word form area (VWFA). Recent findings suggest that this text-selective cortex comprises at least two distinct subregions: the more posterior VWFA-1 is sensitive to visual features, while the more anterior VWFA-2 processes higher level language information. Here, we explore whether these two subregions also exhibit different patterns of functional connectivity. To this end, we capitalize on two complementary datasets: Using the Natural Scenes Dataset (NSD), we identify text-selective responses in high-quality 7T adult data (N = 8), and investigate functional connectivity patterns of VWFA-1 and VWFA-2 at the individual level. We then turn to the Healthy Brain Network (HBN) database to assess whether these patterns replicate in a large developmental sample (N = 224; age 6-20 years), and whether they relate to reading development. In both datasets, we find that VWFA-1 is primarily correlated with bilateral visual regions. In contrast, VWFA-2 is more strongly correlated with language regions in the frontal and lateral parietal lobes, particularly the bilateral inferior frontal gyrus. Critically, these patterns do not generalize to adjacent face-selective regions, suggesting a specific relationship between VWFA-2 and the frontal language network. No correlations were observed between functional connectivity and reading ability. Together, our findings support the distinction between subregions of the VWFA, and suggest that functional connectivity patterns in the ventral temporal cortex are consistent over a wide range of reading skills.

Rethinking cortical recycling in ventral temporal cortex.

High-level visual areas in ventral temporal cortex (VTC) support recognition of important categories, such as faces and words. Word-selective regions are left lateralized and emerge at the onset of reading instruction. Face-selective regions are right lateralized and have been documented in infancy. Prevailing theories suggest that face-selective regions become right lateralized due to competition with word-selective regions in the left hemisphere. However, recent longitudinal studies examining face- and word-selective responses in childhood do not provide support for this theory. Instead, there is evidence that word representations recycle cortex previously involved in processing other stimuli, such as limbs. These findings call for more longitudinal investigations of cortical recycling and a new era of work that links visual experience and behavior with neural responses.

Beyond the Visual Word Form Area - a cognitive characterization of the left ventral occipitotemporal cortex.

The left ventral occipitotemporal cortex has been traditionally viewed as a pathway for visual object recognition including written letters and words. Its crucial role in reading was strengthened by the studies on the functionally localized "Visual Word Form Area" responsible for processing word-like information. However, in the past 20 years, empirical studies have challenged the assumptions of this brain region as processing exclusively visual or even orthographic stimuli. In this review, we aimed to present the development of understanding of the left ventral occipitotemporal cortex from the visually based letter area to the modality-independent symbolic language related region. We discuss theoretical and empirical research that includes orthographic, phonological, and semantic properties of language. Existing results showed that involvement of the left ventral occipitotemporal cortex is not limited to unimodal activity but also includes multimodal processes. The idea of the integrative nature of this region is supported by the broad functional and structural connectivity with language-related and attentional brain networks. We conclude that although the function of the area is not yet fully understood in human cognition, its role goes beyond visual word form processing. The left ventral occipitotemporal cortex seems to be crucial for combining higher-level language information with abstract forms that convey meaning independently of modality.

Incidence of resting-state functional connectivity to secondary language areas and contralateral language areas in patients with brain tumors.

PURPOSE: Secondary language areas, including the pre-supplementary motor area (pre-SMA), dorsolateral prefrontal cortex (DLPFC), and the visual word form area (VWFA) play important roles in speech, but have been under-evaluated in the realm of resting-state (rs)-fMRI. The purpose of this study is to determine the incidence that secondary language areas and contralateral language areas can be localized using seed-based correlation (SBC) rs-fMRI. METHODS: We retrospectively reviewed 40 rs-fMRIs for functional connectivity (FC) to secondary language areas in cases where FC to Broca's or Wernicke's area near tumor in the left hemisphere were successfully generated using SBC analysis. Logistical regression was used for statistical analysis. RESULTS: SBC rs-fMRI with a seed in the left Broca's or Wernicke's area ipsilateral to the tumor was performed in the 40 patients. 72.5% of cases showed FC to the left DLPFC, 67.5% to left pre-SMA, and 52.5% of cases had FC to right Broca's area. In addition to other correlations, we found older patients have a lower incidence of FC to the right Wernicke's area when seeded from both left Broca's and left Wernicke's area (p-value = .016, odds ratio = 0.94). CONCLUSION: SBC rs-fMRI can detect left hemispheric secondary language areas as well as right hemispheric primary and secondary language areas. The left DLPFC showed the highest incidence of FC, followed by the left pre-SMA when seeded from both left Broca's and Wernicke's area. Logistics regression also showed in some instances, differences in the incidence of FC to language areas was dependent on age, seed location, and gender.

Neurodevelopmental trajectories of letter and speech sound processing from preschool to the end of elementary school.

Learning to read alphabetic languages starts with learning letter-speech-sound associations. How this process changes brain function during development is still largely unknown. We followed 102 children with varying reading skills in a mixed-longitudinal/cross-sectional design from the prereading stage to the end of elementary school over five time points (n = 46 with two and more time points, of which n = 16 fully-longitudinal) to investigate the neural trajectories of letter and speech sound processing using fMRI. Children were presented with letters and speech sounds visually, auditorily, and audiovisually in kindergarten (6.7yo), at the middle (7.3yo) and end of first grade (7.6yo), and in second (8.4yo) and fifth grades (11.5yo). Activation of the ventral occipitotemporal cortex for visual and audiovisual processing followed a complex trajectory, with two peaks in first and fifth grades. The superior temporal gyrus (STG) showed an inverted U-shaped trajectory for audiovisual letter processing, a development that in poor readers was attenuated in middle STG and absent in posterior STG. Finally, the trajectories for letter-speech-sound integration were modulated by reading skills and showed differing directionality in the congruency effect depending on the time point. This unprecedented study captures the development of letter processing across elementary school and its neural trajectories in children with varying reading skills.

Dyslexia: Causes and Concomitant Impairments.

In recent decades, theories have been presented to explain the nature of dyslexia, but the causes of dyslexia remained unclear. Although the investigation of the causes of dyslexia presupposes a clear understanding of the concept of cause, such an understanding is missing. The present paper proposes the absence of at least one necessary condition or the absence of all sufficient conditions as causes for impaired reading. The causes of impaired reading include: an incorrect fixation location, too short a fixation time, the attempt to recognize too many letters simultaneously, too large saccade amplitudes, and too short verbal reaction times. It is assumed that a longer required fixation time in dyslexic readers results from a functional impairment of areas V1, V2, and V3 that require more time to complete temporal summation. These areas and areas that receive input from them, such as the fusiform gyrus, are assumed to be impaired in their ability to simultaneously process a string of letters. When these impairments are compensated by a new reading strategy, reading ability improves immediately.

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.

Functional neuroanatomy of lexical access in contextually and visually guided spoken word production.

Lexical access is commonly studied using bare picture naming, which is visually guided, but in real-life conversation, lexical access is more commonly contextually guided. In this fMRI study, we examined the underlying functional neuroanatomy of contextually and visually guided lexical access, and its consistency across sessions. We employed a context-driven picture naming task with fifteen healthy speakers reading incomplete sentences (word-by-word) and subsequently naming the picture depicting the final word. Sentences provided either a constrained or unconstrained lead-in setting for the picture to be named, thereby approximating lexical access in natural language use. The picture name could be planned either through sentence context (constrained) or picture appearance (unconstrained). This procedure was repeated in an equivalent second session two to four weeks later with the same sample to test for test-retest consistency. Picture naming times showed a strong context effect, confirming that constrained sentences speed up production of the final word depicted as an image. fMRI results showed that the areas common to contextually and visually guided lexical access were left fusiform and left inferior frontal gyrus (both consistently active across-sessions), and middle temporal gyrus. However, non-overlapping patterns were also found, notably in the left temporal and parietal cortices, suggesting a different neural circuit for contextually versus visually guided lexical access.

White matter connections of high-level visual areas predict cytoarchitecture better than category-selectivity in childhood, but not adulthood.

Ventral temporal cortex (VTC) consists of high-level visual regions that are arranged in consistent anatomical locations across individuals. This consistency has led to several hypotheses about the factors that constrain the functional organization of VTC. A prevailing theory is that white matter connections influence the organization of VTC, however, the nature of this constraint is unclear. Here, we test 2 hypotheses: (1) white matter tracts are specific for each category or (2) white matter tracts are specific to cytoarchitectonic areas of VTC. To test these hypotheses, we used diffusion magnetic resonance imaging to identify white matter tracts and functional magnetic resonance imaging to identify category-selective regions in VTC in children and adults. We find that in childhood, white matter connections are linked to cytoarchitecture rather than category-selectivity. In adulthood, however, white matter connections are linked to both cytoarchitecture and category-selectivity. These results suggest a rethinking of the view that category-selective regions in VTC have category-specific white matter connections early in development. Instead, these findings suggest that the neural hardware underlying the processing of categorical stimuli may be more domain-general than previously thought, particularly in childhood.

The effects of bilateral posterior parietal cortex tRNS on reading performance.

According to established cognitive neuroscience knowledge based on studies on disabled and typically developing readers, reading is based on a dual-stream model in which a phonological-dorsal stream (left temporo-parietal and inferior frontal areas) processes unfamiliar words and pseudowords, whereas an orthographic-ventral stream (left occipito-temporal and inferior frontal areas) processes known words. However, correlational neuroimaging, causal longitudinal, training, and pharmacological studies have suggested the critical role of visuo-spatial attention in reading development. In a double blind, crossover within-subjects experiment, we manipulated the neuromodulatory effect of a short-term bilateral stimulation of posterior parietal cortex (PPC) by using active and sham tRNS during reading tasks in a large sample of young adults. In contrast to the dual-stream model predicting either no effect or a selective effect on the stimulated phonological-dorsal stream (as well as to a general multisensory effect on both reading streams), we found that only word-reading performance improved after active bilateral PPC tRNS. These findings demonstrate a direct neural connectivity between the PPC, controlling visuo-spatial attention, and the ventral stream for visual word recognition. These results support a neurobiological model of reading where performance of the orthographic-ventral stream is boosted by an efficient deployment of visuo-spatial attention from bilateral PPC stimulation.

Neural Specialization for English and Arabic Print in Early Readers.

Learning to read requires the specialization of a region in the left fusiform gyrus known as the visual word form area (VWFA). This region, which initially responds to faces and objects, develops specificity for print over a long trajectory of instruction and practice. VWFA neurons may be primed for print because of their pre-literate tuning properties, becoming specialized through top-down feedback mechanisms during learning. However, much of what is known about the VWFA comes from studies of Western orthographies, whose alphabets share common visual characteristics. Far less is known about the development of the VWFA for Arabic, which is a complex orthography and is significantly more difficult to achieve fluency in in reading. In the current study, electroencephalography responses were collected from first grade children in the United Arab Emirates learning to read in both English and Arabic. Children viewed words and false font strings in English and Arabic while performing a vigilance task. The P1 and N1 responses to all stimulus categories were quantified in two occipital and two parietal electrodes as well as the alpha band signal across all four electrodes of interest. Analysis revealed a significantly stronger N1 response to English compared to Arabic and decreased alpha power to Arabic compared to English. These findings suggest a fundamental difference in neural plasticity for these two distinct orthographies, even when instruction is concurrent. Future work is needed to determine whether VWFA specialization for Arabic takes longer than more well-studied orthographies and if differences in reading instruction approaches help accelerate this process.

Visual word form area hyperexcitability associated with focal epileptiform activity in a case of reading epilepsy

Reading epilepsy recruits critical language-related areas, with synchronization and subsequent spreading of excitation in response to the epileptogenic stimulus. The mechanism by which possible generalized discharges result in the expression of bilateral or unilateral clinical symptoms remains controversial. The cortical and subcortical areas involved may constitute part of the normal reading network, such as the visual word form area (VWFA). A right-handed, 59-year-old man was diagnosed with epilepsy at the age of 15 after tonic-clonic seizures. Later, the patient described myoclonic jerks of the masticatory and perioral muscles while reading. A multimodal approach with magnetic resonance imaging and ambulatory and video-electroencephalogram was used for seizure characterization and source analysis. A left hemisphere spontaneous occipital-temporal epileptic focus, activated by reading, was observed, spreading broadly throughout frontal and temporal language networks. There was an abnormally increased cortical response to visual word presentation in comparison to pseudowords. Spatial localization of spike sources suggested a close association between the primary epileptic focus and the VWFA. This epileptiform activity seems to be selectively triggered at an early stage of lexical processing, with a functional connection between the epileptic network and the VWFA. This multimodal and functional connectivity approach could be helpful in determining the epileptic network in reading epilepsy.

Acquired dyslexias following temporal lesions.

The acquisition of reading by children is supported by deep changes in the brain systems devoted to vision and language. The left temporal lobe contributes critically to both systems, and lesions affecting it may therefore cause both peripheral vision-related and central language-related reading impairments. The diversity of peripheral dyslexias reflects the anatomical and functional division of the visual cortex into early visual regions, whose lesions have a limited impact on reading; ventral regions, whose lesions are mostly associated to Pure Alexia; and dorsal regions, whose lesions may yield spatial, neglect-related, and attentional dyslexias. Similarly, central alexias reflect the broad distinction, within language processes, between phonological and lexico-semantic components. Phonological and surface dyslexias roughly result from impairment of the former and the latter processes, respectively, while deep dyslexia may be seen as the association of both. In this chapter, we review such types of acquired dyslexias, their clinical features, pathophysiology, and anatomical correlates.

Effective connectivity of the left-ventral occipito-temporal cortex during visual word processing: Direct causal evidence from TMS-EEG co-registration.

As an interface between the visual and language system, the left ventral occipito-temporal cortex (left-vOT) plays a key role in reading. This functional role is supported by anatomical and functional connections between the area and other brain regions within and outside the language network. Nevertheless, only a few studies have investigated how the functional state of this area, which is dependent upon the nature of the task demand and the stimulus being processed, could influence the activity of the connected brain regions. In the present combined TMS-EEG study, we studied the left-vOT effective connectivity by adopting a direct, causal intervention approach. Using TMS, we probed left-vOT activation in different processing contexts and measured the neural propagation of activity from this area to other brain regions. A comparison of neural propagation measured during low-level visual detection of language versus non-language stimuli showed that processing language stimuli reduced neural propagation from the left-vOT to the right occipital cortex. Additionally, compared to the low-level visual detection of language stimuli, performing semantic judgments on the same stimuli further reduced neural propagation to the posterior part of the corpus callosum, right superior parietal lobule and the right anterior temporal lobe. This reduction of cross-hemispheric neural propagation was accompanied by an increase in the collaboration between areas within the left-hemisphere language network. Together, this first evidence from a direct causal intervention approach suggests that processing language stimuli and performing a high-level language task reduce effective connectivity from the left-vOT to the right hemisphere, and may contribute to the left-hemisphere lateralization typically observed during language processing.

Evolution of reading and face circuits during the first three years of reading acquisition.

Although words and faces activate neighboring regions in the fusiform gyrus, we lack an understanding of how such category selectivity emerges during development. To investigate the organization of reading and face circuits at the earliest stage of reading acquisition, we measured the fMRI responses to words, faces, houses, and checkerboards in three groups of 60 French children: 6-year-old pre-readers, 6-year-old beginning readers and 9-year-old advanced readers. The results showed that specific responses to written words were absent prior to reading, but emerged in beginning readers, irrespective of age. Likewise, specific responses to faces were barely visible in pre-readers and continued to evolve in the 9-year-olds, yet primarily driven by age rather than by schooling. Crucially, the sectors of ventral visual cortex that become specialized for words and faces harbored their own functional connectivity prior to reading acquisition: the VWFA with left-hemispheric spoken language areas, and the FFA with the contralateral region and the amygdalae. The results support the view that reading acquisition occurs through the recycling of a pre-existing but plastic circuit which, in pre-readers, already connects the VWFA site to other distant language areas. We argue that reading acquisition does not compete with the face system directly, through a pruning of preexisting face responses, but indirectly, by hindering the slow growth of face responses in the left hemisphere, thus increasing a pre-existing right hemispheric bias.