Early visual experience refines the retinotopic organization within and across visual cortical regions.

Early visual areas are retinotopically organized in human and non-human primates. Population receptive field (pRF) size increases with eccentricity and from lower- to higher-level visual areas. Furthermore, the cortical magnification factor (CMF), a measure of how much cortical space is devoted to each degree of visual angle, is typically larger for foveal as opposed to peripheral regions of the visual field. Whether this fine-scale organization within and across visual areas depends on early visual experience has yet been unknown. Here, we employed 7T functional magnetic resonance imaging pRF mapping to assess the retinotopic organization of early visual regions (i.e., V1, V2, and V3) in eight sight recovery individuals with a history of congenital blindness until a maximum of 4 years of age. Compared with sighted controls, foveal pRF sizes in these individuals were larger, and pRF sizes did not show the typical increase with eccentricity and down the visual cortical processing stream (V1-V2-V3). Cortical magnification was overall diminished and decreased less from foveal to parafoveal visual field locations. Furthermore, cortical magnification correlated with visual acuity in sight recovery individuals. The results of this study suggest that early visual experience is essential for refining a presumably innate prototypical retinotopic organization in humans within and across visual areas, which seems to be crucial for acquiring full visual capabilities.

Sight restoration in congenitally blind humans does not restore visual brain structure.

It is unknown whether impaired brain structure after congenital blindness is reversible if sight is restored later in life. Using structural magnetic resonance imaging, visual cortical surface area and cortical thickness were assessed in a large group of 21 sight-recovery individuals who had been born blind and who months or years later gained sight through cataract removal surgery. As control groups, we included 27 normally sighted individuals, 10 individuals with permanent congenital blindness, and 11 sight-recovery individuals with a late onset of cataracts. Congenital cataract-reversal individuals had a lower visual cortical surface area and a higher visual cortical thickness than normally sighted controls. These results corresponded to those of congenitally permanently blind individuals suggesting that impaired brain structure did not recover. Crucially, structural brain alterations in congenital-cataract reversal individuals were associated with a lower post-surgery visual acuity. No significant changes in visual cortex structure were observed in sight-recovery individuals with late onset cataracts. The results demonstrate that impaired structural brain development due to visual deprivation from birth is not fully reversible and limits functional recovery. Additionally, they highlight the crucial importance of prevention measures in the context of other types of aberrant childhood environments including low socioeconomic status and adversity.

Typical resting-state activity of the brain requires visual input during an early sensitive period.

Sensory deprivation, following a total loss of one sensory modality e.g. vision, has been demonstrated to result in compensatory plasticity. It is yet not known to which extent neural changes, e.g. higher resting-state activity in visual areas (cross-modal plasticity) as a consequence of blindness, reverse, when sight is restored. Here, we used functional MRI to acquire blood oxygen level-dependent resting-state activity during an eyes open and an eyes closed state in congenital cataract-reversal individuals, developmental cataract-reversal individuals, congenitally permanently blind individuals and sighted controls. The amplitude of low frequency fluctuation of the blood oxygen level-dependent signal-a neural marker of spontaneous brain activity during rest-was analyzed. In accordance with previous reports, in normally sighted controls we observed an increase in amplitude of low-frequency fluctuation during rest with the eyes open compared with rest with eyes closed in visual association areas and in parietal cortex but a decrease in auditory and sensorimotor regions. In congenital cataract-reversal individuals, we found an increase of the amplitude of slow blood oxygen level-dependent fluctuations in visual cortex during rest with eyes open compared with rest with eyes closed too but this increase was larger in amplitude than in normally sighted controls. In contrast, congenital cataract-reversal individuals lagged a similar increase in parietal regions and did not show the typical decrease of amplitude of low-frequency fluctuation in auditory cortex. Congenitally blind individuals displayed an overall higher amplitude in slow blood oxygen level-dependent fluctuations in visual cortex compared with sighted individuals and compared with congenital cataract-reversal individuals in the eyes closed condition. Higher amplitude of low-frequency fluctuation in visual cortex of congenital cataract-reversal individuals than in normally sighted controls during eyes open might indicate an altered excitatory-inhibitory balance of visual neural circuits. By contrast, the lower parietal increase and the missing downregulation in auditory regions suggest a reduced influence of the visual system on multisensory and the other sensory systems after restoring sight in congenitally blind individuals. These results demonstrate a crucial dependence of visual and multisensory neural system functioning on visual experience during a sensitive phase in human brain development.

Improved balance performance accompanied by structural plasticity in blind adults after training.

Postural control requires the sensory integration of visual, vestibular, and proprioceptive signals. In the absence of vision, either by blindfolding or in blind individuals, balance performance is typically poorer than with sight. Previous research has suggested that despite showing compensatory vestibular and proprioceptive processing during upright standing, balance performance in blind individuals is overall lower than in sighted controls with eyes open. The present study tested whether balance training, which places demands on vestibular and proprioceptive self-motion perception, improves balance performance in blind adults, and whether we find similar structural correlates in cortical and subcortical brain areas as have been reported in sighted individuals. Fourteen congenitally or late blind adults were randomly assigned to either a balance or a relaxation group and exercised twice a week for 12 weeks. Assessments prior to and after training included balance tests and the acquisition of T1-weighted MRI images. The blind balance group significantly improved in dynamic, static, and functional balance performance compared to the blind relaxation group. The balance performance improvement did not differ from that of age- and gender matched sighted adults after balance training. Cortical thickness increased in the left parahippocampus and decreased in the inferior insula bilaterally in the blind balance group compared to the blind relaxation group. Thickness decreases in the insula were related to improved static and functional balance. Gray matter volume was reduced in the left hippocampus proper and increased in the right subiculum in the blind balance group. The present data suggest that impaired balance performance in blind adults can be significantly improved by a training inducing plasticity in brain regions associated with vestibular and proprioceptive self-motion processing.

Activation in the angular gyrus and in the pSTS is modulated by face primes during voice recognition.

The aim of the present study was to better understand the interaction of face and voice processing when identifying people. In a S1-S2 crossmodal priming fMRI experiment, the target (S2) was a disyllabic voice stimulus, whereas the modality of the prime (S1) was manipulated blockwise and consisted of the silent video of a speaking face in the crossmodal condition or of a voice stimulus in the unimodal condition. Primes and targets were from the same speaker (person-congruent) or from two different speakers (person-incongruent). Participants had to classify the S2 as either an old or a young person. Response times were shorter after a congruent than after an incongruent face prime. The right posterior superior temporal sulcus (pSTS) and the right angular gyrus showed a significant person identity effect (person-incongruent > person-congruent) in the crossmodal condition but not in the unimodal condition. In the unimodal condition, a person identity effect was observed in the bilateral inferior frontal gyrus. Our data suggest that both the priming with a voice and with a face result in a preactivated voice representation of the respective person, which eventually facilitates (person-congruent trials) or hampers (person-incongruent trials) the processing of the identity of a subsequent voice. This process involves activation in the right pSTS and in the right angular gyrus for voices primed by faces, but not for voices primed by voices. Hum Brain Mapp 38:2553-2565, 2017. © 2017 Wiley Periodicals, Inc.

Neural plasticity of voice processing: Evidence from event-related potentials in late-onset blind and sighted individuals.

PURPOSE: Intra- and crossmodal neuroplasticity have been reported to underlie superior voice processing skills in congenitally blind individuals. The present study used event-related potentials (ERPs) in order to test if such compensatory plasticity is limited to the developing brain. METHODS: Late blind individuals were compared to sighted controls in their ability to identify human voices. A priming paradigm was employed in which two successive voices (S1, S2) of the same (person-congruent) or different speakers (person-incongruent) were presented. Participants made an old-young decision on the S2. RESULTS: In both groups ERPs to the auditory S2 were more negative in person-incongruent than in person-congruent trials between 200-300 ms. A topographic analysis suggested a more posteriorly shifted distribution of the Person Match effect (person-incongruent minus person-congruent trials) in late blind individuals compared to sighted controls. CONCLUSION: In contrast to congenitally blind individuals, late blind individuals did not show an early Person Match effect in the time range of the N1, suggesting that crossmodal compensation is mediated by later processing steps rather than by changes at early perceptual levels.

Crossmodal plasticity in the fusiform gyrus of late blind individuals during voice recognition.

Blind individuals are trained in identifying other people through voices. In congenitally blind adults the anterior fusiform gyrus has been shown to be active during voice recognition. Such crossmodal changes have been associated with a superiority of blind adults in voice perception. The key question of the present functional magnetic resonance imaging (fMRI) study was whether visual deprivation that occurs in adulthood is followed by similar adaptive changes of the voice identification system. Late blind individuals and matched sighted participants were tested in a priming paradigm, in which two voice stimuli were subsequently presented. The prime (S1) and the target (S2) were either from the same speaker (person-congruent voices) or from two different speakers (person-incongruent voices). Participants had to classify the S2 as either coming from an old or a young person. Only in late blind but not in matched sighted controls, the activation in the anterior fusiform gyrus was modulated by voice identity: late blind volunteers showed an increase of the BOLD signal in response to person-incongruent compared with person-congruent trials. These results suggest that the fusiform gyrus adapts to input of a new modality even in the mature brain and thus demonstrate an adult type of crossmodal plasticity.

Short-term plasticity of visuo-haptic object recognition.

Functional magnetic resonance imaging (fMRI) studies have provided ample evidence for the involvement of the lateral occipital cortex (LO), fusiform gyrus (FG), and intraparietal sulcus (IPS) in visuo-haptic object integration. Here we applied 30 min of sham (non-effective) or real offline 1 Hz repetitive transcranial magnetic stimulation (rTMS) to perturb neural processing in left LO immediately before subjects performed a visuo-haptic delayed-match-to-sample task during fMRI. In this task, subjects had to match sample (S1) and target (S2) objects presented sequentially within or across vision and/or haptics in both directions (visual-haptic or haptic-visual) and decide whether or not S1 and S2 were the same objects. Real rTMS transiently decreased activity at the site of stimulation and remote regions such as the right LO and bilateral FG during haptic S1 processing. Without affecting behavior, the same stimulation gave rise to relative increases in activation during S2 processing in the right LO, left FG, bilateral IPS, and other regions previously associated with object recognition. Critically, the modality of S2 determined which regions were recruited after rTMS. Relative to sham rTMS, real rTMS induced increased activations during crossmodal congruent matching in the left FG for haptic S2 and the temporal pole for visual S2. In addition, we found stronger activations for incongruent than congruent matching in the right anterior parahippocampus and middle frontal gyrus for crossmodal matching of haptic S2 and in the left FG and bilateral IPS for unimodal matching of visual S2, only after real but not sham rTMS. The results imply that a focal perturbation of the left LO triggers modality-specific interactions between the stimulated left LO and other key regions of object processing possibly to maintain unimpaired object recognition. This suggests that visual and haptic processing engage partially distinct brain networks during visuo-haptic object matching.

Brain systems mediating voice identity processing in blind humans.

Blind people rely more on vocal cues when they recognize a person's identity than sighted people. Indeed, a number of studies have reported better voice recognition skills in blind than in sighted adults. The present functional magnetic resonance imaging study investigated changes in the functional organization of neural systems involved in voice identity processing following congenital blindness. A group of congenitally blind individuals and matched sighted control participants were tested in a priming paradigm, in which two voice stimuli (S1, S2) were subsequently presented. The prime (S1) and the target (S2) were either from the same speaker (person-congruent voices) or from two different speakers (person-incongruent voices). Participants had to classify the S2 as either a old or a young person. Person-incongruent voices (S2) compared with person-congruent voices elicited an increased activation in the right anterior fusiform gyrus in congenitally blind individuals but not in matched sighted control participants. In contrast, only matched sighted controls showed a higher activation in response to person-incongruent compared with person-congruent voices (S2) in the right posterior superior temporal sulcus. These results provide evidence for crossmodal plastic changes of the person identification system in the brain after visual deprivation.

Vision holds a greater share in visuo-haptic object recognition than touch.

The integration of visual and haptic input can facilitate object recognition. Yet, vision might dominate visuo-haptic interactions as it is more effective than haptics in processing several object features in parallel and recognizing objects outside of reaching space. The maximum likelihood approach of multisensory integration would predict that haptics as the less efficient sense for object recognition gains more from integrating additional visual information than vice versa. To test for asymmetries between vision and touch in visuo-haptic interactions, we measured regional changes in brain activity using functional magnetic resonance imaging while healthy individuals performed a delayed-match-to-sample task. We manipulated identity matching of sample and target objects: We hypothesized that only coherent visual and haptic object features would activate unified object representations. The bilateral object-specific lateral occipital cortex, fusiform gyrus, and intraparietal sulcus showed increased activation to crossmodal compared to unimodal matching but only for congruent object pairs. Critically, the visuo-haptic interaction effects in these regions depended on the sensory modality which processed the target object, being more pronounced for haptic than visual targets. This preferential response of visuo-haptic regions indicates a modality-specific asymmetry in crossmodal matching of visual and haptic object features, suggesting a functional primacy of vision over touch in visuo-haptic object recognition.

The superiority in voice processing of the blind arises from neural plasticity at sensory processing stages.

Blind people rely much more on voices compared to sighted individuals when identifying other people. Previous research has suggested a faster processing of auditory input in blind individuals than sighted controls and an enhanced activation of temporal cortical regions during voice processing. The present study used event-related potentials (ERPs) to single out the sub-processes of auditory person identification that change and allow for superior voice processing after congenital blindness. A priming paradigm was employed in which two successive voices (S1 and S2) of either the same (50% of the trials) or different actors were presented. Congenitally blind and matched sighted participants made an old-young decision on the S2. During the pre-experimental familiarization with the stimuli, congenitally blind individuals showed faster learning rates than sighted controls. Reaction times were shorter in person-congruent trials than in person-incongruent trials in both groups. ERPs to S2 stimuli in person-incongruent as compared to person-congruent trials were significantly enhanced at early processing stages (100-160 ms) in congenitally blind participants only. A later negative ERP effect (>200 ms) was found in both groups. The scalp topographies of the experimental effects were characterized by a central and parietal distribution in the sighted but a more posterior distribution in the congenitally blind. These results provide evidence for an improvement of early voice processing stages and a reorganization of the person identification system as a neural correlate of compensatory behavioral improvements following congenital blindness.

The left fusiform gyrus hosts trisensory representations of manipulable objects.

During object manipulation the brain integrates the visual, auditory, and haptic experience of an object into a unified percept. Previous brain imaging studies have implicated for instance the dorsal part of the lateral occipital complex in visuo-tactile and the posterior superior temporal sulcus in audio-visual integration of object-related inputs (Amedi et al., 2005). Yet it is still unclear which brain regions represent object-specific information of all three sensory modalities. To address this question, we performed two complementary functional magnetic resonance imaging experiments. In the first experiment, we identified brain regions which were consistently activated by unimodal visual, auditory, and haptic processing of manipulable objects relative to non-object control stimuli presented in the same modality. In the second experiment, we assessed regional brain activations when participants had to match object-related information that was presented simultaneously in two or all three modalities. Only a well-defined region in left fusiform gyrus (FG) showed an object-specific activation during unisensory processing in the visual, auditory, and tactile modalities. The same region was also consistently activated during multisensory matching of object-related information across all three senses. Taken together, our results suggest that this region is central to the recognition of manipulable objects. A putative role of this FG region is to unify object-specific information provided by the visual, auditory, and tactile modalities into trisensory object representations.

Crossmodal interaction of facial and vocal person identity information: an event-related potential study.

Hearing a voice and seeing a face are essential parts of person identification and social interaction. It has been suggested that both types of information do not only interact at late processing stages but rather interact at the level of perceptual encoding (<200 ms). The present study analysed when visual and auditory representations of person identity modulate the processing of voices. In unimodal trials, two successive voices (S1-S2) of the same or of two different speakers were presented. In the crossmodal condition, the S1 consisted of the face of the same or a different person with respect to the following voice stimulus. Participants had to decide whether the voice probe (S2) was from an elderly or a young person. Reaction times to the S2 were shorter when these stimuli were person-congruent, both in the uni- and crossmodal conditions. ERPs recorded to the person-incongruent as compared to the person-congruent trials (S2) were enhanced at early (100-140 ms) and later processing stages (270-530 ms) in the crossmodal condition. A similar later negative ERP effect (270-530 ms) was found in the unimodal condition as well. These results suggest that identity information conveyed by a face is capable to modulate the sensory processing of voice stimuli.

To switch or not to switch: brain potential indices of attentional control after task-relevant and task-irrelevant changes of stimulus features.

Attention is controlled by the interplay of sensory input and top-down processes. We compared attentional control processes during task switching and reorientation after distraction. The primary task was to discriminate laterally and centrally presented tones; these stimuli were composed of a frequent standard or an infrequent deviant pitch. In the distraction condition, pitch was irrelevant and could be ignored. In the switch condition, pitch changes were relevant: whenever a deviant tone was presented, participants had to discriminate its pitch and not its direction. The task in standard trials remained unchanged. In both conditions, deviants elicited mismatch negativity (MMN), P3a, P3b, and reorienting negativity (RON). We, therefore, suggest that distraction and switching are triggered by the same system of attentional control. In addition, remarkable differences were observable between the two conditions: In the switch condition the MMN was followed by a more pronounced N2b and P3a. The differences between these components support the idea that in the distraction condition, a switch of attention is only initiated but not completely performed.