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.

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.DOI: http://dx.doi.org/10.7554/eLife.10762.001

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.

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.

Summary 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 ].

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.

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.

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.