Author response: Massive cortical reorganization in sighted Braille readers

Learning tactile Braille reading leverages cross-modal plasticity, emphasizing the brain's ability to reallocate functions across sensory domains. This neuroplasticity engages motor and somatosensory areas and reaches language and cognitive centers like the visual word form area (VWFA), even in sighted subjects following training. No study has employed a complex reading task to monitor neural activity during the first weeks of Braille training. Since neuroplasticity can occur within days, understanding neural reorganization during early learning stages is critical. Moreover, such activation was not tested in visual and tactile domains using comparable tasks. Furthermore, implicit reading has not been studied in tactile Braille. Although visual reading in the native script occurs automatically, it remains uncertain whether the same applies to tactile reading. An implicit reading task could extend the knowledge of linguistic processing in Braille. Our study involved 17 sighted adults who learned Braille for 7 months and 19 controls. The experimental group participated in 7 testing sessions (1 week before the course, on the first day, after 1 and 6 weeks, after 3 and 7 months, and after 3 month-long hiatus). Using the fMRI Lexical Decision Task, we observed increased activity within the reading network, including the inferior frontal and supramarginal gyri, 1 week into learning in tactile and visual Braille. Interestingly, VWFA activation was observed after 1 week in the visual domain but only after 6 weeks in the tactile domain. This suggests that skill level in tactile reading influences the onset of involvement of VWFA. Once this activation was achieved, the peak level of VWFA engagement remained stable, even after the follow-up. Furthermore, an implicit reading task revealed increased activity within the reading network, including the VWFA, among participants learning Braille compared to the passive controls. Possibly, implicit reading occurs during non-reading tactile tasks where the Braille alphabet is present. We showed that the VWFA activity peak occurs faster in the visual domain compared to the tactile domain. We also showed that sighted subjects can process tactile Braille implicitly. These results enrich our understanding of neural adaptation mechanisms and the interplay between sensory modalities during complex, cross-modal learning.

The brain is capable of large-scale reorganization in blindness or after massive injury. Such reorganization crosses the division into separate sensory cortices (visual, somatosensory...). As its result, the visual cortex of the blind becomes active during tactile Braille reading. Although the possibility of such reorganization in the normal, adult brain has been raised, definitive evidence has been lacking. Here, we demonstrate such extensive reorganization in normal, sighted adults who learned Braille while their brain activity was investigated with fMRI and transcranial magnetic stimulation (TMS). Subjects showed enhanced activity for tactile reading in the visual cortex, including the visual word form area (VWFA) that was modulated by their Braille reading speed and strengthened resting-state connectivity between visual and somatosensory cortices. Moreover, TMS disruption of VWFA activity decreased their tactile reading accuracy. Our results indicate that large-scale reorganization is a viable mechanism recruited when learning complex skills.

The visual word form area (VWFA) is a region in the left occipitotemporal sulcus of literate individuals that is purportedly specialized for visual word recognition. However, there is considerable controversy about its functional specificity and connectivity, with some arguing that it serves as a domain-general, rather than word-specific, visual processor. The VWFA is a critical region for testing hypotheses about the nature of cortical organization, because it is known to develop only through experience (i.e., reading acquisition), and widespread literacy is too recent to have influenced genetic determinants of brain organization. Using a combination of advanced fMRI analysis techniques, including individual functional localization, multivoxel pattern analysis, and high-resolution resting-state functional connectivity (RSFC) analyses, with data from 33 healthy adult human participants, we demonstrate that (1) the VWFA can discriminate words from nonword letter strings (pseudowords); (2) the VWFA has preferential RSFC with Wernicke's area and other core regions of the language system; and (3) the strength of the RSFC between the VWFA and Wernicke's area predicts performance on a semantic classification task with words but not other categories of visual stimuli. Our results are consistent with the hypothesis that the VWFA is specialized for lexical processing of real words because of its functional connectivity with Wernicke's area.SIGNIFICANCE STATEMENT The visual word form area (VWFA) is critical for determining the nature of category-related organization of the ventral visual system. However, its functional specificity and connectivity are fiercely debated. Recent work concluded that the VWFA is a domain-general, rather than word-specific, visual processor with no preferential functional connectivity with the language system. Using more advanced techniques, our results stand in stark contrast to these earlier findings. We demonstrate that the VWFA is highly specialized for lexical processing of real words, and that a fundamental factor driving this specialization is its preferential intrinsic functional connectivity with core regions of the language system. Our results support the hypothesis that intrinsic functional connectivity contributes to category-related specialization within the human ventral visual system.

Perception via different sensory modalities was traditionally believed to be supported by largely separate brain systems. However, a growing number of studies demonstrate that the visual cortices of typical, sighted adults are involved in tactile and auditory perceptual processing. Here, we investigated the spatiotemporal dynamics of the visual cortex’s involvement in a complex tactile task: Braille letter recognition. Sighted subjects underwent Braille training and then participated in a transcranial magnetic stimulation (TMS) study in which they tactually identified single Braille letters. During this task, TMS was applied to their left early visual cortex, visual word form area (VWFA), and left early somatosensory cortex at five time windows from 20 to 520 ms following the Braille letter presentation’s onset. The subjects’ response accuracy decreased when TMS was applied to the early visual cortex at the 120–220 ms time window and when TMS was applied to the VWFA at the 320–420 ms time window. Stimulation of the early somatosensory cortex did not have a time-specific effect on the accuracy of the subjects’ Braille letter recognition, but rather caused a general slowdown during this task. Our results indicate that the involvement of sighted people’s visual cortices in tactile perception respects the canonical visual hierarchy—the early tactile processing stages involve the early visual cortex, whereas more advanced tactile computations involve high-level visual areas. Our findings are compatible with the metamodal account of brain organization and suggest that the whole visual cortex may potentially support spatial perception in a task-specific, sensory-independent manner.

Neural Representation in Visual Word Form Area during Word Reading

Cortical localisation of the visual and auditory word form areas: A reconsideration of the evidence

Specialization for written words over objects in the visual cortex

Objective To investigate the underlying neural mechanism of left hemiparalexia and left hemialexia in reading Chinese characters. Methods A patient with reading disorders caused by brain infarctions at the left ventralis medialis occipitotemporal lobe and the splenium of the corpus callosum was studied. A series of neuropsychological tests, such as reading Chinese characters presented in the central foveal field or in the left and right half of the foveal field, were conducted with the patient, and neuroimaging techniques including high spatial resolution 3D-MRI and diffusion tensor tractography （DTT） were used to examine whether or not there were lesions of the neural pathway. Results The patient showed left hemiparalexia, which was characterized by making substitution or omission mistakes, mostly in the left parts of Chinese characters, and also left hemialexia（alexia for characters presented in left visual field）. 3D-MRI demonstrated infarctions in the left ventral mesial occipitotemporal area and in the left side of the splenium of the corpus callosum. The left lateral mid-fusiform cortex, which has been identified as the visual word form area（VWFA）, was almost intact. DTT indicated the major forceps fibers running through the splenium were all disconnected due to the infarction of the left splenium. Conclusion As a result of disruption of the splemium-major forceps pathway, visual character information in the left visual field which is initially projected to the right occipital cortex cannot be transferred from the right visual cortex to the left VWFA. This mechanism of left hemiparalexia and left hemialexia in reading Chinese characters is similar to that in reading English words. Key words: Left hemiparalexia; Left hemialexia; Corpus callosum; Visual word form area

The visual word form area (VWFA) is a region of left inferior occipitotemporal cortex that is critically involved in visual word recognition. Previous studies have investigated whether and how experience shapes the functional characteristics of VWFA by comparing neural response magnitude in response to words and nonwords. Conflicting results have been obtained, however, perhaps because response magnitude can be influenced by other factors such as attention. In this study, we measured neural activity in monozygotic twins, using functional magnetic resonance imaging. This allowed us to quantify differences in unique environmental contributions to neural activation evoked by words, pseudowords, consonant strings, and false fonts in the VWFA and striate cortex. The results demonstrate significantly greater effects of unique environment in the word and pseudoword conditions compared to the consonant string and false font conditions both in VWFA and in left striate cortex. These findings provide direct evidence for environmental contributions to the neural architecture for reading, and suggest that learning phonology and/or orthographic patterns plays the biggest role in shaping that architecture.

Word and non-word reading: What role for the Visual Word Form Area?

The white matter (WM) architecture of the human brain changes in response to training, though fine-grained temporal characteristics of training-induced white matter plasticity remain unexplored. We investigated white matter microstructural changes using diffusion tensor imaging at five different time points in 26 sighted female adults during 8 months of training on tactile braille reading. Our results show that training-induced white matter plasticity occurs both within and beyond the trained sensory modality, as reflected by fractional anisotropy (FA) increases in somatosensory and visual cortex, respectively. The observed changes followed distinct time courses, with gradual linear FA increase along the training in the somatosensory cortex and sudden visual cortex cross-modal plasticity occurring after braille input became linguistically meaningful. WM changes observed in these areas returned to baseline after the cessation of learning in line with the supply-demand model of plasticity. These results also indicate that the temporal dynamics of microstructural plasticity in different cortical regions might be modulated by the nature of computational demands. We provide additional evidence that observed FA training-induced changes are behaviorally relevant to tactile reading. Together, these results demonstrate that WM plasticity is a highly dynamic process modulated by the introduction of novel experiences.SIGNIFICANCE STATEMENT Throughout the lifetime the human brain is shaped by various experiences. Training-induced reorganization in white matter (WM) microstructure has been reported, but we know little about its temporal dynamics. To fill this gap, we scanned sighted subjects five times during tactile braille reading training. We observed different dynamics of WM plasticity in the somatosensory and visual cortices implicated in braille reading. The former showed a continuous increase in WM tissue anisotropy along with tactile training, while microstructural changes in the latter were observed only after the participants learned to read braille words. Our results confirm the supply-demand model of brain plasticity and provide evidence that WM reorganization depends on distinct computational demands and functional roles of regions involved in the trained skill.

Neuroimaging studies have provided evidence that the orthographic properties of linguistic stimuli are processed within the visual word form area (VWFA) localised in the left inferotemporal cortex (Cohen & Dehaene, 2004). It is not, however, clear in the literature whether this region responds preferentially to words, distinguishing them from pseudowords, or whether the pseudowords are distinguished from letter-strings on the basis of their orthographic regularity, or again, whether the VWFA distinguishes letters from numbers or from visual stimuli such as chequerboards. Very recently, it has been claimed that there is no evidence that the ill-named VWFA changes its responsiveness during or after reading acquisition (Price & Devlin, 2004). In order to simulate a condition of pre-reading ability in adult readers, we performed this study, in which we compared processing of Greek words and legal pseudowords in mother-tongue Greeks (skilled readers) and monolingual Italian individuals (naive readers) who had no familiarity with the Greek alphabet. ERPs were recorded while volunteers were engaged in a task involving the identification and response to target letters contained within Greek words or pseudowords. The response speed was identical in the two groups (550 vs. 557 ms). ERP data showed that at 165 ms post-stimulus (N1 component) the left lateral-occipital scalp area, probably corresponding to the left ventral occipitotemporal sulcus, discriminates letters of a familiar alphabet, while an unknown alphabet also activates the homologous right-hemispheric region more than 100 ms later. This suggests that the VWFA discriminates nonalphabetic symbols from letter-strings. An analysis of the N2 component showed an increase in the activation of the same region at about 285 ms post-stimulus during the processing of words rather than pseudowords in skilled readers, thus supporting the view that the VWFA discriminates words on the basis of their familiarity. The data seem to suggest that the VWFA is alphabet-specific and that it is based on the shaping of visual area activity during acquisition of the ability to read a given symbolic code. Experiments were conducted with the understanding and the consent of each participant, and with approval from the Ethical Committee of the Italian Consiglio Nazionale delle Ricerche.

A number of recent studies consistently show an area, known as the visual word form area (VWFA), in the left fusiform gyrus that is selectively responsive for visual words in alphabetic scripts as well as in logographic scripts, such as Chinese characters. However, given the large difference between Chinese characters and alphabetic scripts in terms of their orthographic rules, it is not clear at a fine spatial scale, whether Chinese characters engage the same VWFA in the occipito-temporal cortex as alphabetic scripts. We specifically compared Chinese with Korean script, with Korean script serving as a good example of alphabetic writing system, but matched to Chinese in the overall square shape. Sixteen proficient early Chinese-Korean bilinguals took part in the fMRI experiment. Four types of stimuli (Chinese characters, Korean characters, line drawings and unfamiliar Chinese faces) were presented in a block-design paradigm. By contrasting characters (Chinese or Korean) to faces, presumed VWFAs could be identified for both Chinese and Korean characters in the left occipito-temporal sulcus in each subject. The location of peak response point in these two VWFAs were essentially the same. Further analysis revealed a substantial overlap between the VWFA identified for Chinese and that for Korean. At the group level, there was no significant difference in amplitude of response to Chinese and Korean characters. Spatial patterns of response to Chinese and Korean are similar. In addition to confirming that there is an area in the left occipito-temporal cortex that selectively responds to scripts in both Korean and Chinese in early Chinese-Korean bilinguals, our results show that these two scripts engage essentially the same VWFA, even at the level of fine spatial patterns of activation across voxels. These results suggest that similar populations of neurons are engaged in processing the different scripts within the same VWFA in early bilinguals.

A Ventral Visual Stream Reading Center Independent of Visual Experience

Action Video Games Make Dyslexic Children Read Better