Decoding Reach Direction in Early "Visual" Cortex of Congenitally Blind Individuals.

Motor actions, such as reaching or grasping, can be decoded from fMRI activity of early visual cortex (EVC) in sighted humans. This effect can depend on vision or visual imagery, or alternatively, could be driven by mechanisms independent of visual experience. Here, we show that the actions of reaching in different directions can be reliably decoded from fMRI activity of EVC in congenitally blind humans (both sexes). Thus, neither visual experience nor visual imagery is necessary for EVC to represent action-related information. We also demonstrate that, within EVC of blind humans, the accuracy of reach direction decoding is highest in areas typically representing foveal vision and gradually decreases in areas typically representing peripheral vision. We propose that this might indicate the existence of a predictive, hard-wired mechanism of aligning action and visual spaces. This mechanism might send action-related information primarily to the high-resolution foveal visual areas, which are critical for guiding and online correction of motor actions. Finally, we show that, beyond EVC, the decoding of reach direction in blind humans is most accurate in dorsal stream areas known to be critical for visuo-spatial and visuo-motor integration in the sighted. Thus, these areas can develop space and action representations even in the lifelong absence of vision. Overall, our findings in congenitally blind humans match previous research on the action system in the sighted, and suggest that the development of action representations in the human brain might be largely independent of visual experience.SIGNIFICANCE STATEMENT Early visual cortex (EVC) was traditionally thought to process only visual signals from the retina. Recent studies proved this account incomplete, and showed EVC involvement in many activities not directly related to incoming visual information, such as memory, sound, or action processing. Is EVC involved in these activities because of visual imagery? Here, we show robust reach direction representation in EVC of humans born blind. This demonstrates that EVC can represent actions independently of vision and visual imagery. Beyond EVC, we found that reach direction representation in blind humans is strongest in dorsal brain areas, critical for action processing in the sighted. This suggests that the development of action representations in the human brain is largely independent of visual experience.

Superior visual rhythm discrimination in expert musicians is most likely not related to cross-modal recruitment of the auditory cortex.

Training can influence behavioral performance and lead to brain reorganization. In particular, training in one modality, for example, auditory, can improve performance in another modality, for example, visual. Previous research suggests that one of the mechanisms behind this phenomenon could be the cross-modal recruitment of the sensory areas, for example, the auditory cortex. Studying expert musicians offers a chance to explore this process. Rhythm is an aspect of music that can be presented in various modalities. We designed an fMRI experiment in which professional pianists and non-musicians discriminated between two sequences of rhythms presented auditorily (series of sounds) or visually (series of flashes). Behavioral results showed that musicians performed in both visual and auditory rhythmic tasks better than non-musicians. We found no significant between-group differences in fMRI activations within the auditory cortex. However, we observed that musicians had increased activation in the right Inferior Parietal Lobe when compared to non-musicians. We conclude that the musicians' superior visual rhythm discrimination is not related to cross-modal recruitment of the auditory cortex; instead, it could be related to activation in higher-level, multimodal areas in the cortex.

Visuospatial Cognitive Dysfunction in Patients with Vestibular Loss.

OBJECTIVE: To characterize visuospatial and nonvisuospatial cognitive domains affected by vestibular loss and determine whether patient-reported outcomes measures (PROMs) correlate with performance on neuropsychological tests. STUDY DESIGN: Cross-sectional study. SETTING: University-based tertiary medical center. PATIENTS: Sixty-nine age-matched subjects: 25 patients with bilateral vestibular loss (BVL), 14 patients with unilateral vestibular loss (UVL), and 30 normal controls (NC). INTERVENTIONS: Neuropsychological tests used to assess visuospatial and auditory short-term and working memory, number magnitude representation, executive function, and attention. Validated PROMs used to evaluate quality of life and subjective cognitive impairment. MAIN OUTCOME MEASURES: Performance on neuropsychological tests and scores on PROM surveys. RESULTS: BVL and UVL patients performed significantly worse than NC subjects on tasks requiring visuospatial representation compared with NC subjects ( p < 0.01). BVL patients demonstrated decreased performance on spatial representation tasks compared with UVL and NC subjects ( p < 0.05 and p < 0.05, respectively). All subject groups performed similarly on tasks assessing nonvisuospatial cognitive domains, such as auditory short-term and working memory, executive function, and attention. PROMs did not seem to correlate with performance on neuropsychological tasks. CONCLUSION: Patients with vestibular loss exhibit impairments in tasks requiring visuospatial representation but perform similarly to NC subjects in tasks of auditory working memory, executive function, or attention. Currently available questionnaires may be insufficient to screen patients for cognitive deficits.

Rethinking the representation of sound.

Blindness triggers a reorganization of the visual and auditory cortices in the brain.

Preference for animate domain sounds in the fusiform gyrus of blind individuals is modulated by shape-action mapping.

In high-level visual areas in the human brain, preference for inanimate objects is observed regardless of stimulation modality (visual/auditory/tactile) and individual's visual experience (sighted/blind) whereas preference for animate entities seems robust mainly in the visual modality. Here, we test a hypothesis explaining this domain difference: Object representations can be activated through nonvisual stimulation when their shapes are systematically related to action system representations, a quality typical of most inanimate objects but of only specific animate entities. We studied functional magnetic resonance imaging activations in congenitally blind and sighted individuals listening to animal, object, and human sounds. In blind individuals, the typical location of the fusiform face area preferentially responded to human facial expression sounds clearly related to specific facial actions and resulting face shapes but not to speech or animal sounds. No univariate preference for any sound category was observed in the fusiform gyrus in sighted individuals, but the expected multivoxel effects were present. We conclude that nonvisual signals can activate shape representations of those stimuli-inanimate or animate-for which shape and action computations are transparently related. However, absence of potentially competing visual inputs seems necessary for this effect to be clearly detectable in the case of animate representation.

Temporal Dynamics of Brain White Matter Plasticity in Sighted Subjects during Tactile Braille Learning: A Longitudinal Diffusion Tensor Imaging Study.

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.

Early deafness leads to re-shaping of functional connectivity beyond the auditory cortex.

Early sensory deprivation, such as deafness, shapes brain development in multiple ways. Deprived auditory areas become engaged in the processing of stimuli from the remaining modalities and in high-level cognitive tasks. Yet, structural and functional changes were also observed in non-deprived brain areas, which may suggest the whole-brain network changes in deaf individuals. To explore this possibility, we compared the resting-state functional network organization of the brain in early deaf adults and hearing controls and examined global network segregation and integration. Relative to hearing controls, deaf adults exhibited decreased network segregation and an altered modular structure. In the deaf, regions of the salience network were coupled with the fronto-parietal network, while in the hearing controls, they were coupled with other large-scale networks. Deaf adults showed weaker connections between auditory and somatomotor regions, stronger coupling between the fronto-parietal network and several other large-scale networks (visual, memory, cingulo-opercular and somatomotor), and an enlargement of the default mode network. Our findings suggest that brain plasticity in deaf adults is not limited to changes in the auditory cortex but additionally alters the coupling between other large-scale networks and the development of functional brain modules. These widespread functional connectivity changes may provide a mechanism for the superior behavioral performance of the deaf in visual and attentional tasks.

Brain plasticity dynamics during tactile Braille learning in sighted subjects: Multi-contrast MRI approach.

A growing body of empirical evidence supports the notion of diverse neurobiological processes underlying learning-induced plasticity changes in the human brain. There are still open questions about how brain plasticity depends on cognitive task complexity, how it supports interactions between brain systems and with what temporal and spatial trajectory. We investigated brain and behavioural changes in sighted adults during 8-months training of tactile Braille reading whilst monitoring brain structure and function at 5 different time points. We adopted a novel multivariate approach that includes behavioural data and specific MRI protocols sensitive to tissue properties to assess local functional and structural and myelin changes over time. Our results show that while the reading network, located in the ventral occipitotemporal cortex, rapidly adapts to tactile input, sensory areas show changes in grey matter volume and intra-cortical myelin at different times. This approach has allowed us to examine and describe neuroplastic mechanisms underlying complex cognitive systems and their (sensory) inputs and (motor) outputs differentially, at a mesoscopic level.

Functional reorganization of the reading network in the course of foreign language acquisition.

During foreign language acquisition neural representations of native language and foreign language assimilate. In the reading network, this assimilation leads to a shift from effortful processing to automated reading. Longitudinal studies can track this transition and reveal dynamics that might not become apparent in behavior. Here, we report results from a longitudinal functional magnetic resonance imaging (fMRI) study, which tracked functional changes in the reading network of beginning learners of Greek over one year. We deliberately chose Greek as foreign language that would have similar orthographic transparency but a different alphabet than the native language (Polish). fMRI scans with lexical and semantic decision tasks were performed at five different time points (every ~3 months). Classical language areas (the left inferior frontal gyrus, the left precentral gyrus, and the bilateral supplementary motor cortex), and cognitive control areas (left inferior parietal lobe and bilateral anterior cingulate cortex) showed stronger activation after the first months of instruction as compared to the activation before instruction. This pattern occured in both tasks. Task-related activity in the reading network remained constant throughout the remaining 6 months of learning and was also present in a follow-up scan 3 months after the end of the course. A similar pattern was demonstrated by the analysis of convergence between foreign and native languages occurring within the first months of learning. Additionally, in the lexical task, the extent of spatial overlap, between foreign and native language in Broca's area increased constantly from the beginning till the end of training. Our findings support the notion that reorganization of language networks is achieved after a relatively short time of foreign language instruction. We also demonstrate that cognitive control areas are recruited in foreign language reading at low proficiency levels. No apparent changes in the foreign or native reading network occur after the initial 3 months of learning. This suggests that task demand might be more important than proficiency in regulating the resources needed for efficient foreign language reading.

Multimodal imaging of brain reorganization in hearing late learners of sign language.

The neural plasticity underlying language learning is a process rather than a single event. However, the dynamics of training-induced brain reorganization have rarely been examined, especially using a multimodal magnetic resonance imaging approach, which allows us to study the relationship between functional and structural changes. We focus on sign language acquisition in hearing adults who underwent an 8-month long course and five neuroimaging sessions. We assessed what neural changes occurred as participants learned a new language in a different modality-as reflected by task-based activity, connectivity changes, and co-occurring structural alterations. Major changes in the activity pattern appeared after just 3 months of learning, as indicated by increases in activation within the modality-independent perisylvian language network, together with increased activation in modality-dependent parieto-occipital, visuospatial and motion-sensitive regions. Despite further learning, no alterations in activation were detected during the following months. However, enhanced coupling between left-lateralized occipital and inferior frontal regions was observed as the proficiency increased. Furthermore, an increase in gray matter volume was detected in the left inferior frontal gyrus which peaked at the end of learning. Overall, these results showed complexity and temporal distinctiveness of various aspects of brain reorganization associated with learning of new language in different sensory modality.

Decoding Natural Sounds in Early "Visual" Cortex of Congenitally Blind Individuals.

Complex natural sounds, such as bird singing, people talking, or traffic noise, induce decodable fMRI activation patterns in early visual cortex of sighted blindfolded participants [1]. That is, early visual cortex receives non-visual and potentially predictive information from audition. However, it is unclear whether the transfer of auditory information to early visual areas is an epiphenomenon of visual imagery or, alternatively, whether it is driven by mechanisms independent from visual experience. Here, we show that we can decode natural sounds from activity patterns in early "visual" areas of congenitally blind individuals who lack visual imagery. Thus, visual imagery is not a prerequisite of auditory feedback to early visual cortex. Furthermore, the spatial pattern of sound decoding accuracy in early visual cortex was remarkably similar in blind and sighted individuals, with an increasing decoding accuracy gradient from foveal to peripheral regions. This suggests that the typical organization by eccentricity of early visual cortex develops for auditory feedback, even in the lifelong absence of vision. The same feedback to early visual cortex might support visual perception in the sighted [1] and drive the recruitment of this area for non-visual functions in blind individuals [2, 3].

Functional hierarchy for tactile processing in the visual cortex of sighted adults.

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.

Letter and Speech Sound Association in Emerging Readers With Familial Risk of Dyslexia.

In alphabetic scripts, learning letter-sound (LS) association (i.e., letter knowledge) is a strong predictor of later reading skills. LS integration is related to left superior temporal cortex (STC) activity and its disruption was previously observed in dyslexia (DYS). Whether disruption in LS association is a cause of reading impairment or a consequence of decreased exposure to print remains unclear. Using fMRI, we compared activation for letters, speech sounds and LS association in emerging readers with (FHD+, N = 50) and without (FHD-, N = 35) familial history of DYS, out of whom 17 developed DYS 2 years later. Despite having similar reading skills, FHD+ and FHD- groups showed opposite pattern of activation in left STC: In FHD- children activation was higher for incongruent compared to congruent, whereas in FHD+ it was higher for congruent LS pairs. Higher activation to congruent LS pairs was also characteristic of future DYS. The magnitude of incongruency effect in left STC was positively related to early reading skills, but only in FHD- children and (retrospectively) in typical readers. We show that alterations in brain activity during LS association can be detected at very early stages of reading acquisition, suggesting their causal involvement in later reading impairments. Increased response of left STC to incongruent LS pairs in FHD- group might reflect an early stage of automatizing LS associations, where the brain responds actively to conflicting pairs. The absence of such response in FHD+ children could lead to failures in suppressing incongruent information during reading acquisition, which could result in future reading problems.

Structural reorganization of the early visual cortex following Braille training in sighted adults.

Training can induce cross-modal plasticity in the human cortex. A well-known example of this phenomenon is the recruitment of visual areas for tactile and auditory processing. It remains unclear to what extent such plasticity is associated with changes in anatomy. Here we enrolled 29 sighted adults into a nine-month tactile Braille-reading training, and used voxel-based morphometry and diffusion tensor imaging to describe the resulting anatomical changes. In addition, we collected resting-state fMRI data to relate these changes to functional connectivity between visual and somatosensory-motor cortices. Following Braille-training, we observed substantial grey and white matter reorganization in the anterior part of early visual cortex (peripheral visual field). Moreover, relative to its posterior, foveal part, the peripheral representation of early visual cortex had stronger functional connections to somatosensory and motor cortices even before the onset of training. Previous studies show that the early visual cortex can be functionally recruited for tactile discrimination, including recognition of Braille characters. Our results demonstrate that reorganization in this region induced by tactile training can also be anatomical. This change most likely reflects a strengthening of existing connectivity between the peripheral visual cortex and somatosensory cortices, which suggests a putative mechanism for cross-modal recruitment of visual areas.

Universal Visual Features Might Be Necessary for Fluent Reading. A Longitudinal Study of Visual Reading in Braille and Cyrillic Alphabets.

It has been hypothesized that efficient reading is possible because all reading scripts have been matched, through cultural evolution, to the natural capabilities of the visual cortex. This matching has resulted in all scripts being made of line-junctions, such as T, X, or L. Our aim was to test a critical prediction of this hypothesis: visual reading in an atypical script that is devoid of line-junctions (such as the Braille alphabet read visually) should be much less efficient than reading in a "normal" script (e.g., Cyrillic). Using a lexical decision task, we examined Visual Braille reading speed and efficiency in sighted Braille teachers. As a control, we tested learners of a natural visual script, Cyrillic. Both groups participated in a two semester course of either visual Braille or Russian while their reading speed and accuracy was tested at regular intervals. The results show that visual Braille reading is slow, prone to errors and highly serial, even in Braille readers with years of prior reading experience. Although subjects showed some improvements in their visual Braille reading accuracy and speed following the course, the effect of word length on reading speed (typically observed in beginning readers) was remained very sizeable through all testing sessions. These results are in stark contrast to Cyrillic, a natural script, where only 3 months of learning were sufficient to achieve relative proficiency. Taken together, these results suggest that visual features such as line junctions and their combinations might be necessary for efficient reading.

Task-specific reorganization of the auditory cortex in deaf humans.

The principles that guide large-scale cortical reorganization remain unclear. In the blind, several visual regions preserve their task specificity; ventral visual areas, for example, become engaged in auditory and tactile object-recognition tasks. It remains open whether task-specific reorganization is unique to the visual cortex or, alternatively, whether this kind of plasticity is a general principle applying to other cortical areas. Auditory areas can become recruited for visual and tactile input in the deaf. Although nonhuman data suggest that this reorganization might be task specific, human evidence has been lacking. Here we enrolled 15 deaf and 15 hearing adults into an functional MRI experiment during which they discriminated between temporally complex sequences of stimuli (rhythms). Both deaf and hearing subjects performed the task visually, in the central visual field. In addition, hearing subjects performed the same task in the auditory modality. We found that the visual task robustly activated the auditory cortex in deaf subjects, peaking in the posterior-lateral part of high-level auditory areas. This activation pattern was strikingly similar to the pattern found in hearing subjects performing the auditory version of the task. Although performing the visual task in deaf subjects induced an increase in functional connectivity between the auditory cortex and the dorsal visual cortex, no such effect was found in hearing subjects. We conclude that in deaf humans the high-level auditory cortex switches its input modality from sound to vision but preserves its task-specific activation pattern independent of input modality. Task-specific reorganization thus might be a general principle that guides cortical plasticity in the brain.

Braille in the Sighted: Teaching Tactile Reading to Sighted Adults.

Blind people are known to have superior perceptual abilities in their remaining senses. Several studies suggest that these enhancements are dependent on the specific experience of blind individuals, who use those remaining senses more than sighted subjects. In line with this view, sighted subjects, when trained, are able to significantly progress in relatively simple tactile tasks. However, the case of complex tactile tasks is less obvious, as some studies suggest that visual deprivation itself could confer large advantages in learning them. It remains unclear to what extent those complex skills, such as braille reading, can be learnt by sighted subjects. Here we enrolled twenty-nine sighted adults, mostly braille teachers and educators, in a 9-month braille reading course. At the beginning of the course, all subjects were naive in tactile braille reading. After the course, almost all were able to read whole braille words at a mean speed of 6 words-per-minute. Subjects with low tactile acuity did not differ significantly in braille reading speed from the rest of the group, indicating that low tactile acuity is not a limiting factor for learning braille, at least at this early stage of learning. Our study shows that most sighted adults can learn whole-word braille reading, given the right method and a considerable amount of motivation. The adult sensorimotor system can thus adapt, to some level, to very complex tactile tasks without visual deprivation. The pace of learning in our group was comparable to congenitally and early blind children learning braille in primary school, which suggests that the blind's mastery of complex tactile tasks can, to a large extent, be explained by experience-dependent mechanisms.

Massive cortical reorganization in sighted Braille readers.

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.

Three-dimensional grammar in the brain: Dissociating the neural correlates of natural sign language and manually coded spoken language.

In several countries natural sign languages were considered inadequate for education. Instead, new sign-supported systems were created, based on the belief that spoken/written language is grammatically superior. One such system called SJM (system jezykowo-migowy) preserves the grammatical and lexical structure of spoken Polish and since 1960s has been extensively employed in schools and on TV. Nevertheless, the Deaf community avoids using SJM for everyday communication, its preferred language being PJM (polski jezyk migowy), a natural sign language, structurally and grammatically independent of spoken Polish and featuring classifier constructions (CCs). Here, for the first time, we compare, with fMRI method, the neural bases of natural vs. devised communication systems. Deaf signers were presented with three types of signed sentences (SJM and PJM with/without CCs). Consistent with previous findings, PJM with CCs compared to either SJM or PJM without CCs recruited the parietal lobes. The reverse comparison revealed activation in the anterior temporal lobes, suggesting increased semantic combinatory processes in lexical sign comprehension. Finally, PJM compared with SJM engaged left posterior superior temporal gyrus and anterior temporal lobe, areas crucial for sentence-level speech comprehension. We suggest that activity in these two areas reflects greater processing efficiency for naturally evolved sign language.