Correction: A self-training program for sensory substitution devices.

[This corrects the article DOI: 10.1371/journal.pone.0250281.].

Activation of human visual area V6 during egocentric navigation with and without visual experience.

V6 is a retinotopic area located in the dorsal visual stream that integrates eye movements with retinal and visuo-motor signals. Despite the known role of V6 in visual motion, it is unknown whether it is involved in navigation and how sensory experiences shape its functional properties. We explored the involvement of V6 in egocentric navigation in sighted and in congenitally blind (CB) participants navigating via an in-house distance-to-sound sensory substitution device (SSD), the EyeCane. We performed two fMRI experiments on two independent datasets. In the first experiment, CB and sighted participants navigated the same mazes. The sighted performed the mazes via vision, while the CB performed them via audition. The CB performed the mazes before and after a training session, using the EyeCane SSD. In the second experiment, a group of sighted participants performed a motor topography task. Our results show that right V6 (rhV6) is selectively involved in egocentric navigation independently of the sensory modality used. Indeed, after training, rhV6 of CB is selectively recruited for auditory navigation, similarly to rhV6 in the sighted. Moreover, we found activation for body movement in area V6, which can putatively contribute to its involvement in egocentric navigation. Taken together, our findings suggest that area rhV6 is a unique hub that transforms spatially relevant sensory information into an egocentric representation for navigation. While vision is clearly the dominant modality, rhV6 is in fact a supramodal area that can develop its selectivity for navigation in the absence of visual experience.

A self-training program for sensory substitution devices.

Sensory Substitution Devices (SSDs) convey visual information through audition or touch, targeting blind and visually impaired individuals. One bottleneck towards adopting SSDs in everyday life by blind users, is the constant dependency on sighted instructors throughout the learning process. Here, we present a proof-of-concept for the efficacy of an online self-training program developed for learning the basics of the EyeMusic visual-to-auditory SSD tested on sighted blindfolded participants. Additionally, aiming to identify the best training strategy to be later re-adapted for the blind, we compared multisensory vs. unisensory as well as perceptual vs. descriptive feedback approaches. To these aims, sighted participants performed identical SSD-stimuli identification tests before and after ~75 minutes of self-training on the EyeMusic algorithm. Participants were divided into five groups, differing by the feedback delivered during training: auditory-descriptive, audio-visual textual description, audio-visual perceptual simultaneous and interleaved, and a control group which had no training. At baseline, before any EyeMusic training, participants SSD objects' identification was significantly above chance, highlighting the algorithm's intuitiveness. Furthermore, self-training led to a significant improvement in accuracy between pre- and post-training tests in each of the four feedback groups versus control, though no significant difference emerged among those groups. Nonetheless, significant correlations between individual post-training success rates and various learning measures acquired during training, suggest a trend for an advantage of multisensory vs. unisensory feedback strategies, while no trend emerged for perceptual vs. descriptive strategies. The success at baseline strengthens the conclusion that cross-modal correspondences facilitate learning, given SSD algorithms are based on such correspondences. Additionally, and crucially, the results highlight the feasibility of self-training for the first stages of SSD learning, and suggest that for these initial stages, unisensory training, easily implemented also for blind and visually impaired individuals, may suffice. Together, these findings will potentially boost the use of SSDs for rehabilitation.

Mesoscopic Neural Representations in Spatial Navigation.

Recent evidence suggests that mesoscopic neural oscillations measured via intracranial electroencephalography exhibit spatial representations, which were previously only observed at the micro- and macroscopic level of brain organization. Specifically, theta (and gamma) oscillations correlate with movement, speed, distance, specific locations, and goal proximity to boundaries. In entorhinal cortex (EC), they exhibit hexadirectional modulation, which is putatively linked to grid cell activity. Understanding this mesoscopic neural code is crucial because information represented by oscillatory power and phase may complement the information content at other levels of brain organization. Mesoscopic neural oscillations help bridge the gap between single-neuron and macroscopic brain signals of spatial navigation and may provide a mechanistic basis for novel biomarkers and therapeutic targets to treat diseases causing spatial disorientation.

Grid-like hexadirectional modulation of human entorhinal theta oscillations.

The entorhinal cortex contains a network of grid cells that play a fundamental part in the brain's spatial system, supporting tasks such as path integration and spatial memory. In rodents, grid cells are thought to rely on network theta oscillations, but such signals are not evident in all species, challenging our understanding of the physiological basis of the grid network. We analyzed intracranial recordings from neurosurgical patients during virtual navigation to identify oscillatory characteristics of the human entorhinal grid network. The power of entorhinal theta oscillations showed six-fold modulation according to the virtual heading during navigation, which is a hypothesized signature of grid representations. Furthermore, modulation strength correlated with spatial memory performance. These results demonstrate the connection between theta oscillations and the human entorhinal grid network and show that features of grid-like neuronal representations can be identified from population electrophysiological recordings.

Task Selectivity as a Comprehensive Principle for Brain Organization.

How do the anatomically consistent functional selectivities of the brain emerge? A new study by Bola and colleagues reveals task selectivity in auditory rhythm-selective areas in congenitally deaf adults perceiving visual rhythm sequences. Here, we contextualize this result with accumulating evidence from animal and human studies supporting sensory-independent task specializations as a comprehensive principle shaping brain (re)organization.

Waist-up protection for blind individuals using the EyeCane as a primary and secondary mobility aid.

BACKGROUND: One of the most stirring statistics in relation to the mobility of blind individuals is the high rate of upper body injuries, even when using the white-cane. OBJECTIVE: We here addressed a rehabilitation- oriented challenge of providing a reliable tool for blind people to avoid waist-up obstacles, namely one of the impediments to their successful mobility using currently available methods (e.g., white-cane). METHODS: We used the EyeCane, a device we developed which translates distances from several angles to haptic and auditory cues in an intuitive and unobtrusive manner, serving both as a primary and secondary mobility aid. We investigated the rehabilitation potential of such a device in facilitating visionless waist-up body protection. RESULTS: After ∼5 minutes of training with the EyeCane blind participants were able to successfully detect and avoid obstacles waist-high and up. This was significantly higher than their success when using the white-cane alone. As avoidance of obstacles required participants to perform an additional cognitive process after their detection, the avoidance rate was significantly lower than the detection rate. CONCLUSION: Our work has demonstrated that the EyeCane has the potential to extend the sensory world of blind individuals by expanding their currently accessible inputs, and has offered them a new practical rehabilitation tool.

Perception of Graphical Virtual Environments by Blind Users via Sensory Substitution.

Graphical virtual environments are currently far from accessible to blind users as their content is mostly visual. This is especially unfortunate as these environments hold great potential for this population for purposes such as safe orientation, education, and entertainment. Previous tools have increased accessibility but there is still a long way to go. Visual-to-audio Sensory-Substitution-Devices (SSDs) can increase accessibility generically by sonifying on-screen content regardless of the specific environment and offer increased accessibility without the use of expensive dedicated peripherals like electrode/vibrator arrays. Using SSDs virtually utilizes similar skills as when using them in the real world, enabling both training on the device and training on environments virtually before real-world visits. This could enable more complex, standardized and autonomous SSD training and new insights into multisensory interaction and the visually-deprived brain. However, whether congenitally blind users, who have never experienced virtual environments, will be able to use this information for successful perception and interaction within them is currently unclear.We tested this using the EyeMusic SSD, which conveys whole-scene visual information, to perform virtual tasks otherwise impossible without vision. Congenitally blind users had to navigate virtual environments and find doors, differentiate between them based on their features (Experiment1:task1) and surroundings (Experiment1:task2) and walk through them; these tasks were accomplished with a 95% and 97% success rate, respectively. We further explored the reactions of congenitally blind users during their first interaction with a more complex virtual environment than in the previous tasks-walking down a virtual street, recognizing different features of houses and trees, navigating to cross-walks, etc. Users reacted enthusiastically and reported feeling immersed within the environment. They highlighted the potential usefulness of such environments for understanding what visual scenes are supposed to look like and their potential for complex training and suggested many future environments they wished to experience.

Reading in the dark: neural correlates and cross-modal plasticity for learning to read entire words without visual experience.

Cognitive neuroscience has long attempted to determine the ways in which cortical selectivity develops, and the impact of nature vs. nurture on it. Congenital blindness (CB) offers a unique opportunity to test this question as the brains of blind individuals develop without visual experience. Here we approach this question through the reading network. Several areas in the visual cortex have been implicated as part of the reading network, and one of the main ones among them is the VWFA, which is selective to the form of letters and words. But what happens in the CB brain? On the one hand, it has been shown that cross-modal plasticity leads to the recruitment of occipital areas, including the VWFA, for linguistic tasks. On the other hand, we have recently demonstrated VWFA activity for letters in contrast to other visual categories when the information is provided via other senses such as touch or audition. Which of these tasks is more dominant? By which mechanism does the CB brain process reading? Using fMRI and visual-to-auditory sensory substitution which transfers the topographical features of the letters we compare reading with semantic and scrambled conditions in a group of CB. We found activation in early auditory and visual cortices during the early processing phase (letter), while the later phase (word) showed VWFA and bilateral dorsal-intraparietal activations for words. This further supports the notion that many visual regions in general, even early visual areas, also maintain a predilection for task processing even when the modality is variable and in spite of putative lifelong linguistic cross-modal plasticity. Furthermore, we find that the VWFA is recruited preferentially for letter and word form, while it was not recruited, and even exhibited deactivation, for an immediately subsequent semantic task suggesting that despite only short sensory substitution experience orthographic task processing can dominate semantic processing in the VWFA. On a wider scope, this implies that at least in some cases cross-modal plasticity which enables the recruitment of areas for new tasks may be dominated by sensory independent task specific activation.

Integration and binding in rehabilitative sensory substitution: Increasing resolution using a new Zooming-in approach.

PURPOSE: To visually perceive our surroundings we constantly move our eyes and focus on particular details, and then integrate them into a combined whole. Current visual rehabilitation methods, both invasive, like bionic-eyes and non-invasive, like Sensory Substitution Devices (SSDs), down-sample visual stimuli into low-resolution images. Zooming-in to sub-parts of the scene could potentially improve detail perception. Can congenitally blind individuals integrate a 'visual' scene when offered this information via different sensory modalities, such as audition? Can they integrate visual information -perceived in parts - into larger percepts despite never having had any visual experience? METHODS: We explored these questions using a zooming-in functionality embedded in the EyeMusic visual-to-auditory SSD. Eight blind participants were tasked with identifying cartoon faces by integrating their individual components recognized via the EyeMusic's zooming mechanism. RESULTS: After specialized training of just 6-10 hours, blind participants successfully and actively integrated facial features into cartooned identities in 79±18% of the trials in a highly significant manner, (chance level 10% ; rank-sum P <  1.55E-04). CONCLUSIONS: These findings show that even users who lacked any previous visual experience whatsoever can indeed integrate this visual information with increased resolution. This potentially has important practical visual rehabilitation implications for both invasive and non-invasive methods.

Navigation using sensory substitution in real and virtual mazes.

Under certain specific conditions people who are blind have a perception of space that is equivalent to that of sighted individuals. However, in most cases their spatial perception is impaired. Is this simply due to their current lack of access to visual information or does the lack of visual information throughout development prevent the proper integration of the neural systems underlying spatial cognition? Sensory Substitution devices (SSDs) can transfer visual information via other senses and provide a unique tool to examine this question. We hypothesize that the use of our SSD (The EyeCane: a device that translates distance information into sounds and vibrations) can enable blind people to attain a similar performance level as the sighted in a spatial navigation task. We gave fifty-six participants training with the EyeCane. They navigated in real life-size mazes using the EyeCane SSD and in virtual renditions of the same mazes using a virtual-EyeCane. The participants were divided into four groups according to visual experience: congenitally blind, low vision & late blind, blindfolded sighted and sighted visual controls. We found that with the EyeCane participants made fewer errors in the maze, had fewer collisions, and completed the maze in less time on the last session compared to the first. By the third session, participants improved to the point where individual trials were no longer significantly different from the initial performance of the sighted visual group in terms of errors, time and collision.

A number-form area in the blind.

Distinct preference for visual number symbols was recently discovered in the human right inferior temporal gyrus (rITG). It remains unclear how this preference emerges, what is the contribution of shape biases to its formation and whether visual processing underlies it. Here we use congenital blindness as a model for brain development without visual experience. During fMRI, we present blind subjects with shapes encoded using a novel visual-to-music sensory-substitution device (The EyeMusic). Greater activation is observed in the rITG when subjects process symbols as numbers compared with control tasks on the same symbols. Using resting-state fMRI in the blind and sighted, we further show that the areas with preference for numerals and letters exhibit distinct patterns of functional connectivity with quantity and language-processing areas, respectively. Our findings suggest that specificity in the ventral 'visual' stream can emerge independently of sensory modality and visual experience, under the influence of distinct connectivity patterns.

The "EyeCane", a new electronic travel aid for the blind: Technology, behavior & swift learning.

PURPOSE: Independent mobility is one of the most pressing problems facing people who are blind. We present the EyeCane, a new mobility aid aimed at increasing perception of environment beyond what is provided by the traditional White Cane for tasks such as distance estimation, navigation and obstacle detection. METHODS: The "EyeCane" enhances the traditional White Cane by using tactile and auditory output to increase detectable distance and angles. It circumvents the technical pitfalls of other devices, such as weight, short battery life, complex interface schemes, and slow learning curve. It implements multiple beams to enables detection of obstacles at different heights, and narrow beams to provide active sensing that can potentially increase the user's spatial perception of the environment. Participants were tasked with using the EyeCane for several basic tasks with minimal training. RESULTS: Blind and blindfolded-sighted participants were able to use the EyeCane successfully for distance estimation, simple navigation and simple obstacle detection after only several minutes of training. CONCLUSIONS: These results demonstrate the EyeCane's potential for mobility rehabilitation. The short training time is especially important since available mobility training resources are limited, not always available, and can be quite expensive and/or entail long waiting periods.

EyeMusic: Introducing a "visual" colorful experience for the blind using auditory sensory substitution.

PURPOSE: Sensory-substitution devices (SSDs) provide auditory or tactile representations of visual information. These devices often generate unpleasant sensations and mostly lack color information. We present here a novel SSD aimed at addressing these issues. METHODS: We developed the EyeMusic, a novel visual-to-auditory SSD for the blind, providing both shape and color information. Our design uses musical notes on a pentatonic scale generated by natural instruments to convey the visual information in a pleasant manner. A short behavioral protocol was utilized to train the blind to extract shape and color information, and test their acquired abilities. Finally, we conducted a survey and a comparison task to assess the pleasantness of the generated auditory stimuli. RESULTS: We show that basic shape and color information can be decoded from the generated auditory stimuli. High performance levels were achieved by all participants following as little as 2-3 hours of training. Furthermore, we show that users indeed found the stimuli pleasant and potentially tolerable for prolonged use. CONCLUSIONS: The novel EyeMusic algorithm provides an intuitive and relatively pleasant way for the blind to extract shape and color information. We suggest that this might help facilitating visual rehabilitation because of the added functionality and enhanced pleasantness.

Sensory substitution: closing the gap between basic research and widespread practical visual rehabilitation.

Sensory substitution devices (SSDs) have come a long way since first developed for visual rehabilitation. They have produced exciting experimental results, and have furthered our understanding of the human brain. Unfortunately, they are still not used for practical visual rehabilitation, and are currently considered as reserved primarily for experiments in controlled settings. Over the past decade, our understanding of the neural mechanisms behind visual restoration has changed as a result of converging evidence, much of which was gathered with SSDs. This evidence suggests that the brain is more than a pure sensory-machine but rather is a highly flexible task-machine, i.e., brain regions can maintain or regain their function in vision even with input from other senses. This complements a recent set of more promising behavioral achievements using SSDs and new promising technologies and tools. All these changes strongly suggest that the time has come to revive the focus on practical visual rehabilitation with SSDs and we chart several key steps in this direction such as training protocols and self-train tools.

The effect of extended sensory range via the EyeCane sensory substitution device on the characteristics of visionless virtual navigation.

Mobility training programs for helping the blind navigate through unknown places with a White-Cane significantly improve their mobility. However, what is the effect of new assistive technologies, offering more information to the blind user, on the underlying premises of these programs such as navigation patterns? We developed the virtual-EyeCane, a minimalistic sensory substitution device translating single-point-distance into auditory cues identical to the EyeCane's in the real world. We compared performance in virtual environments when using the virtual-EyeCane, a virtual-White-Cane, no device and visual navigation. We show that the characteristics of virtual-EyeCane navigation differ from navigation with a virtual-White-Cane or no device, and that virtual-EyeCane users complete more levels successfully, taking shorter paths and with less collisions than these groups, and we demonstrate the relative similarity of virtual-EyeCane and visual navigation patterns. This suggests that additional distance information indeed changes navigation patterns from virtual-White-Cane use, and brings them closer to visual navigation.

Increasing accessibility to the blind of virtual environments, using a virtual mobility aid based on the "EyeCane": feasibility study.

Virtual worlds and environments are becoming an increasingly central part of our lives, yet they are still far from accessible to the blind. This is especially unfortunate as such environments hold great potential for them for uses such as social interaction, online education and especially for use with familiarizing the visually impaired user with a real environment virtually from the comfort and safety of his own home before visiting it in the real world. We have implemented a simple algorithm to improve this situation using single-point depth information, enabling the blind to use a virtual cane, modeled on the "EyeCane" electronic travel aid, within any virtual environment with minimal pre-processing. Use of the Virtual-EyeCane, enables this experience to potentially be later used in real world environments with identical stimuli to those from the virtual environment. We show the fast-learned practical use of this algorithm for navigation in simple environments.

Cross-sensory transfer of sensory-motor information: visuomotor learning affects performance on an audiomotor task, using sensory-substitution.

Visual-to-auditory sensory-substitution devices allow users to perceive a visual image using sound. Using a motor-learning task, we found that new sensory-motor information was generalized across sensory modalities. We imposed a rotation when participants reached to visual targets, and found that not only seeing, but also hearing the location of targets via a sensory-substitution device resulted in biased movements. When the rotation was removed, aftereffects occurred whether the location of targets was seen or heard. Our findings demonstrate that sensory-motor learning was not sensory-modality-specific. We conclude that novel sensory-motor information can be transferred between sensory modalities.

The brain as a flexible task machine: implications for visual rehabilitation using noninvasive vs. invasive approaches.

PURPOSE OF REVIEW: The exciting view of our brain as highly flexible task-based and not sensory-based raises the chances for visual rehabilitation, long considered unachievable, given adequate training in teaching the brain how to see. Recent advances in rehabilitation approaches, both noninvasive, like sensory substitution devices (SSDs) which present visual information using sound or touch, and invasive, like visual prosthesis, may potentially be used to achieve this goal, each alone, and most preferably together. RECENT FINDINGS: Visual impairments and said solutions are being used as a model for answering fundamental questions ranging from basic cognitive neuroscience, showing that several key visual brain areas are actually highly flexible, modality-independent and, as was recently shown, even visual experience-independent task machines, to technological and behavioral developments, allowing blind persons to 'see' using SSDs and other approaches. SUMMARY: SSDs can be potentially used as a research tool for assessing the brain's functional organization; as an aid for the blind in daily visual tasks; to visually train the brain prior to invasive procedures, by taking advantage of the 'visual' cortex's flexibility and task specialization even in the absence of vision; and to augment postsurgery functional vision using a unique SSD-prostheses hybrid. Taken together the reviewed results suggest a brighter future for visual neuro-rehabilitation.