Audiotactile integration is reduced in congenital blindness in a spatial ventriloquism task

In the ventriloquism effect, the presentation of spatially discrepant visual information biases the localization of simultaneously presented sounds. Recently, an analogous spatial influence of touch on audition has been observed. By manipulating hand posture, it has been demonstrated that this audiotactile ventriloquist effect predominantly operates in an external frame of reference. In the present study, we examined the contribution of developmental vision to audiotactile interactions as indicated by the ventriloquism effect. Congenitally blind, late blind and sighted adults were asked to report the perceived location of sounds presented from a left, a central or a right location. Auditory stimuli were either delivered alone or concurrently with touches at the left or the right hand. The hands were located to the right and to the left of the lateral speakers and participants either adopted an uncrossed or a crossed hand posture. While sighted controls and late blind participants similarly mislocalized auditory stimuli toward the concurrent tactile stimuli in bimodal trials, the congenitally blind showed a reduced ventriloquism effect. All groups showed a reduced audiotactile ventriloquism effect in the crossed hand condition. However, the magnitude of the reduction was significantly larger in the group of congenitally blind than in the group of sighted controls. These results suggest reduced audio-tactile interactions in spatial processing following a lack of visual input from birth.     

Early visual deprivation alters multisensory processing in peripersonal space

Multisensory peripersonal space develops in a maturational process that is thought to be influenced by early sensory experience. We investigated the role of vision in the effective development of audiotactile interactions in peripersonal space. Early blind (EB), late blind (LB) and sighted control (SC) participants were asked to lateralize auditory, tactile and audiotactile stimuli. The experiment was conducted with the hands uncrossed or crossed over the body midline in order to alter the relationship between personal and peripersonal spatial representations. First, we observed that the crossed posture results in a greater detrimental effect for tactile performance in sighted subjects but a greater deficit in auditory performance in early blind ones. This result is interpreted as evidence for a visually driven developmental process that automatically remaps tactile and proprioceptive spatial representation into an external framework. Second, we demonstrate that improved reaction times observed in the bimodal conditions in SC and LB exceeds that predicted by probability summation in both conditions of postures, indicating neural integration of different sensory information. In EB, nonlinear summation was obtained in the uncrossed but not in the crossed posture. We argue that the default use of an anatomically anchored reference system in EB prevents effective audiotactile interactions in the crossed posture due to the poorly aligned spatial coordinates of these two modalities in such conditions. Altogether, these results provide compelling evidence for the critical role of early vision in the development of multisensory perception and action control in peripersonal space.     

Event-related potential evidence for the use of external coordinates in the preparation of tactile attention by the early blind

Recent studies have suggested that visual experience in childhood is crucial for the automatic activation of an external spatial reference frame in tactile perception. These findings are largely based on behavioural work, with limited exploration using event-related potentials (ERPs). The present study examined the role of external spatial frameworks on tactile perception by recording ERP correlates of both preparatory processes and somatosensory processing during a tactile attention task for a group of early blind participants and age-matched sighted controls who carried out the task in darkness. Participants had to shift attention to one hand or the other as indicated by an auditory cue presented at the start of each trial, in order to detect infrequent tactile targets delivered to the attended hand. Spatial information about the external environment was acquired in advance during tactile exploration of the testing booth. ERPs measured during the cue-target interval indicated a conflict between anatomical and external spatial reference frames for both early blind and sighted participants, as marked by the delayed onset of the anterior directing attention negativity, although the delay was more pronounced in the sighted. A delay was also observed, irrespective of visual experience, on the onset of attentional modulations of somatosensory ERPs elicited by tactile stimuli. Although these results confirm that neither concurrent nor developmental vision is necessary for the default use of an external spatial framework in tactile attention, they suggest that the relative impact of an external vs. an anatomical spatial coordinate system may be affected by visual experience.     

Shifts of attention in the early blind: an erp study of attentional control processes in the absence of visual spatial information

To investigate the role of visual spatial information in the control of spatial attention, event-related brain potentials (ERPs) were recorded during a tactile attention task for a group of totally blind participants who were either congenitally blind or had lost vision during infancy, and for an age-matched, sighted control group who performed the task in the dark. Participants had to shift attention to the left or right hand (as indicated by an auditory cue presented at the start of each trial) in order to detect infrequent tactile targets delivered to this hand. Effects of tactile attention on the processing of tactile events, as reflected by attentional modulations of somatosensory ERPs to tactile stimuli, were very similar for early blind and sighted participants, suggesting that the capacity to selectively process tactile information from one hand versus the other does not differ systematically between the blind and the sighted. ERPs measured during the cue-target interval revealed an anterior directing attention negativity (ADAN) that was present for the early blind group as well as for the sighted control group. In contrast, the subsequent posterior late direction attention negativity (LDAP) was absent in both groups. These results suggest that these two components reflect functionally distinct attentional control mechanisms which differ in their dependence on the availability of visually coded representations of external space.     

Temporal cues trick the visual and auditory cortices mimicking spatial cues in blind individuals

In the absence of vision, spatial representation may be altered. When asked to compare the relative distances between three sounds (i.e., auditory spatial bisection task), blind individuals demonstrate significant deficits and do not show an event‐related potential response mimicking the visual C1 reported in sighted people. However, we have recently demonstrated that the spatial deficit disappears if coherent time and space cues are presented to blind people, suggesting that they may use time information to infer spatial maps. In this study, we examined whether the modification of temporal cues during space evaluation altered the recruitment of the visual and auditory cortices in blind individuals. We demonstrated that the early (50–90 ms) occipital response, mimicking the visual C1, is not elicited by the physical position of the sound, but by its virtual position suggested by its temporal delay. Even more impressively, in the same time window, the auditory cortex also showed this pattern and responded to temporal instead of spatial coordinates.     

Vertical sound localization in blind humans

It is widely held that early-blind people compensate their visual loss by a general sharpening of spatial hearing. The present study reports a possible exception to this view: when the vertical position (elevation) of a sound source had to be localized, four out of six early-blind subjects exhibited systematic deviations in pointing, while two early-blind subjects were as accurate as sighted controls. On the other hand, blind and sighted individuals were able to judge relative positions of different sound locations with similar precision. These results suggest that visual experience may be used to accurately calibrate the relation between the vertical coordinates of auditory space and body, but is not needed to develop sufficiently high resolution of spatial hearing.     

Auditory-tactile speech perception in congenitally blind and sighted adults

The present study investigated whether manual tactile information from a speaker's face modulates the intelligibility of speech when audio-tactile perception is compared with audio-only perception. Since more elaborated auditory and tactile skills have been reported in the blind, two groups of congenitally blind and sighted adults were compared. Participants performed a forced-choice syllable decision task across three conditions: audio-only and congruent/incongruent audio-tactile conditions. For the auditory modality, the syllables were embedded or not in noise while, for the tactile modality, participants felt in synchrony a mouthed syllable by placing a hand on the face of a talker. In the absence of acoustic noise, syllables were almost perfectly recognized in all conditions. On the contrary, with syllables embedded with acoustic noise, more correct responses were reported in case of congruent mouthing compared to no mouthing, and in case of no mouthing compared to incongruent mouthing. Interestingly, no perceptual differences were observed between blind and sighted adults. These findings demonstrate that manual tactile information relevant to recovering speech gestures modulates auditory speech perception in case of degraded acoustic information and that audio-tactile interactions occur similarly in blind and sighted untrained listeners.     

Congenital blindness leads to enhanced vibrotactile perception

Previous studies have shown that in comparison with the sighted, blind individuals display superior non-visual perceptual abilities and differ in brain organisation. In this study, we investigated the performance of blind and sighted participants on a vibrotactile discrimination task. Thirty-three blind participants were classified into one of three groups (congenital, early, late), depending on the age at which they became blind. Consistent with previous neuroimaging data, individuals blinded after late childhood (14 years) showed no advantage over sighted participants. Both the congenitally- and early-blind participants were better than the sighted. The congenitally blind participants were even more accurate than the early-blind participants; a distinction that has not been drawn previously. Duration of blindness did not predict task performance and the effect of onset age persisted after duration of daily Braille reading was accounted for. We conclude that complete visual deprivation early in life leads to heightened tactile acuity.     

Dynamic modulation of visual detection by auditory cues in spatial neglect

One of the most constant findings of studies about selective attention is that detection of visual stimuli is enhanced when a visual cue is presented at the position of the upcoming target. In healthy participants, comparable benefits were reported when the cue was presented in a different modality than the target. The aim of this study was to examine spatial and temporal dynamics of visual attention following auditory cues in patients with spatial neglect. Twelve healthy subjects and five patients with left-sided neglect were asked to react to a small vertical line presented randomly at one of four positions. The target appeared 150 or 1000 ms after an auditory cue that was either static (continuous 380 Hz tone presented to the left or right ear) or dynamic (380 Hz tone moving from the left to the right ear or vice versa). The reaction time pattern of healthy participants was unaffected by the different tones. In contrast, reaction times of neglect patients were significantly faster to left targets following a dynamic tone moving from right to left in comparison to a tone moving from left to right. Interestingly, static unilateral tones modulated visual attention of neglect patients to a lesser degree than dynamic tones. The modulation of visual attention by dynamic auditory cues was of short duration and disappeared after 1000 ms. These results demonstrate a fast automatic shift of spatial attention in the direction of a moving tone, suggesting strong dynamic links between visual and auditory attention in patients with a severe spatial deficit.     

Comparison of blind and sighted participants' performance in a letter recognition working memory task

The performance in letter recognition of 21 blind participants was compared with that of 16 age-matched sighted participants in an n-back working memory task. Blind participants were tested tactually with series of raised letters and Braille characters, and sighted participants tactually with series of raised letters and visually with series of letters presented on a computer screen. With this approach, we wanted to compare the tactual performances by trained (blind) and non-trained (sighted) participants, and tactual and visual performances by trained (blind and sighted, respectively) participants. Increments of mnemonic load increased the number of incorrect responses significantly in all n-back tasks. As expected, the blind participants outperformed the sighted ones statistically significantly in the tactile raised letters n-back task. The sighted participants produced significantly fewer incorrect responses in the visual task than the blind participants in the raised letters task, whereas there was no such difference between sighted subjects' visual performance and blind subjects' tactile performance in the Braille task. These results demonstrate the degree and limits to which everyday practice develops perceptual skills either in persons without sensory deficits (vision and visual environment), or persons with severe sensory loss (blindness and tactile environment). The performance level of blind persons relying on their tactile skills is just about the same as that of sighted subjects relying on their visual skills.     

Opposing effects of head position on sound localization in blind and sighted human subjects

Up to now, there is an unsolved contradiction between the view that the development of an auditory spatial representation needs calibration by vision and the psychophysical demonstration of quite precise sound localization in early blind humans. The present study provides a link between these two competing conceptions. Two experiments were conducted with congenitally or early blind subjects and sighted controls. In the first experiment, subjects pointed with their head to actual sound sources located in the azimuthal plane. In the second experiment, lateralization of dichotic sound stimuli, presented via headphones, was investigated with variation of head-to-trunk position. The results showed opposing systematic errors of sound localization or lateralization, depending on head position, made by blind and sighted subjects. These differences suggest that audiomotor feedback replaces vision so as to calibrate auditory space in blind individuals. That is, in contrast to the widespread opinion of compensation of visual loss by a general sharpening of audition, compensatory plasticity in the blind may specifically be related to enhanced processing of proprioceptive and vestibular information with the auditory spatial input.     

Auditory localization and precedence effect: An exploratory study in infants and toddlers with visual impairment and normal vision

The precedence effect is a spatial hearing phenomenon implicated in sound localization on reverberant environments. It occurs when a pair of sounds, with a brief delay between them, is presented from different directions; listeners give greater perceptual weight to localization cues coming from the first-arriving sound, called lead, and suppress localization cues from the later-arriving reflection, called lag. Developmental studies with sighted infants show that the first responses to precedence effect stimuli are observed at 4–5 months of life. In this exploratory study, we use the minimum audible angle (MAA) paradigm in conjunction with the observer-based psychophysical procedure to test the ability of infants and toddlers, with visual impairment and normal vision, to discriminate changes in the azimuthal position of sounds configured under precedence effect conditions. The results indicated that similar and, in some conditions, higher performances were obtained by blind toddlers when compared to sighted children of similar age, and revealed that the observer-based psychophysical procedure is a valuable method to measure auditory localization acuity in infants and toddlers with visual impairment. The video records showed auditory orienting behaviors specific of the blind children group.     

The extent of visual deficit and auditory spatial compensation: evidence from self-positioning from auditory cues

Blindfolded sighted, myopic, amblyopic, adventitiously blind and congenitally blind humans performed a self-positioning task during which they were stimulated only by auditory cues. Results showed that visually deprived subjects used auditory cues to position themselves in their environment with a greater accuracy than normal-sighted subjects. In addition, the magnitude of auditory spatial compensation was found to be strongly related to the extent of the visual deficit.     

Attention and sensory interactions within the occipital cortex in the early blind: an fMRI study

Visual deprivation early in life results in occipital cortical responsiveness across a broad range of perceptual and cognitive tasks. In the reorganized occipital cortex of early blind (EB) individuals, the relative lack of specificity for particular sensory stimuli and tasks suggests that attention effects may play a prominent role in these areas. We wished to establish whether occipital cortical areas in the EB were responsive to stimuli across sensory modalities (auditory, tactile) and whether these areas maintained or altered their activity as a function of selective attention. Using a three-stimulus oddball paradigm and event-related functional magnetic resonance imaging, auditory and tactile tasks presented separately demonstrated that several occipital regions of interest (ROIs) in the EB, but not sighted controls (SCs), responded to targets and task-irrelevant distracter stimuli of both modalities. When auditory and tactile stimuli were presented simultaneously with subjects alternating attention between sensory streams, only the calcarine sulcus continued to respond to stimuli in both modalities. In all other ROIs, responses to auditory targets were as large or larger than those observed in the auditory-alone condition, but responses to tactile targets were attenuated or abolished by the presence of unattended auditory stimuli. Both auditory and somatosensory cortices responded consistently to auditory and tactile targets, respectively. These results reveal mechanisms of orienting and selective attention within the visual cortex of EB individuals and suggest that mechanisms of enhancement and suppression interact asymmetrically on auditory and tactile streams during bimodal sensory presentation.     

Ventral and dorsal visual pathways support auditory motion processing in the blind: evidence from electrical neuroimaging

Blindness induces processes of neural plasticity, resulting in recruitment of the deafferentated visual areas for non‐visual sensory functions. These processes are related to superior abilities of blind compared with sighted individuals for specific auditory and tactile tasks. Recently, an exceptional performance of the blind has been demonstrated for auditory motion perception, with a minimum audible movement angle that was half that of sighted controls (J. Lewald (2013) Neuropsychologia, 51 , 181–186). The present study revealed an electrophysiological correlate of this finding by analysing the so‐called motion‐onset response, a prominent auditory‐evoked potential to the onset of motion. The cN1 component of this response, appearing about 170 ms after motion onset, was two times higher in amplitude for blind compared with matched sighted control subjects. At the time of the cN1, electrical neuroimaging using sLORETA revealed stronger activation in blind than sighted subjects primarily in ventral visual areas (V1v, V2v, VP, V4v) of the right occipital lobe. Activation was also obtained in middle temporal area V5. These findings suggest that blindness results in stronger involvement of both non‐motion areas of the ventral visual stream and motion areas of the dorsal visual stream in processing of auditory motion at the same point in time after motion onset. This argues against the view that visual motion areas, such as area V5, are preferentially recruited for auditory motion analysis in the blind. Rather, cross‐modal reorganization of cortical areas induced by blindness seems to be largely independent of the specific visual functions of the same areas in sighted persons.     

Activation of the hippocampal complex during tactile maze solving in congenitally blind subjects

Despite their lack of vision, congenitally blind subjects are able to build and manipulate cognitive maps for spatial navigation. It is assumed that they thereby rely more heavily on echolocation, proprioceptive signals and environmental cues such as ambient temperature and audition to compensate for their lack of vision. Little is known, however, about the neural mechanisms underlying spatial navigation in blind individuals in settings where these cues are absent. We therefore measured behavioural performance and blood oxygenation-level dependant (BOLD) responses using functional magnetic resonance imaging (fMRI) in congenitally blind and blindfolded sighted participants while they navigated through a tactile multiple T-maze. Both groups learned the maze task at a similar pace. In blind participants, tactile maze navigation was associated with increased BOLD responses in the right hippocampus and parahippocampus, occipital cortex and fusiform gyrus. Blindfolded sighted controls did not show increased BOLD responses in these areas; instead they activated the caudate nucleus and thalamus. Both groups activated the precuneus during tactile maze navigation. We conclude that cross-modal plastic processes allow for the recruitment of the hippocampal complex and visual cortex in congenital blindness.     

The Extent of Task Specificity for Visual and Tactile Sequences in the Auditory Cortex of the Deaf and Hard of Hearing

It has been proposed that the auditory cortex in the deaf humans might undergo task-specific reorganization. However, evidence remains scarce as previous experiments used only two very specific tasks (temporal processing and face perception) in visual modality. Here, congenitally deaf/hard of hearing and hearing women and men were enrolled in an fMRI experiment as we sought to fill this evidence gap in two ways. First, we compared activation evoked by a temporal processing task performed in two different modalities, visual and tactile. Second, we contrasted this task with a perceptually similar task that focuses on the spatial dimension. Additional control conditions consisted of passive stimulus observation. In line with the task specificity hypothesis, the auditory cortex in the deaf was activated by temporal processing in both visual and tactile modalities. This effect was selective for temporal processing relative to spatial discrimination. However, spatial processing also led to significant auditory cortex recruitment which, unlike temporal processing, occurred even during passive stimulus observation. We conclude that auditory cortex recruitment in the deaf and hard of hearing might involve interplay between task-selective and pluripotential mechanisms of cross-modal reorganization. Our results open several avenues for the investigation of the full complexity of the cross-modal plasticity phenomenon.SIGNIFICANCE STATEMENT Previous studies suggested that the auditory cortex in the deaf may change input modality (sound to vision) while keeping its function (e.g., rhythm processing). We investigated this hypothesis by asking deaf or hard of hearing and hearing adults to discriminate between temporally and spatially complex sequences in visual and tactile modalities. The results show that such function-specific brain reorganization, as has previously been demonstrated in the visual modality, also occurs for tactile processing. On the other hand, they also show that for some stimuli (spatial) the auditory cortex activates automatically, which is suggestive of a take-over by a different kind of cognitive function. The observed differences in processing of sequences might thus result from an interplay of task-specific and pluripotent plasticity.     

Exceptional ability of blind humans to hear sound motion: Implications for the emergence of auditory space

Blind people may compensate for their visual loss by the increased use of auditory spatial information, thus showing normal or even supra-normal ability to localize sources of sound. However, the problem of how blind persons develop and maintain an internal concept of the topography of the auditory space in the absence of calibration by visual information is still unsolved. The present study demonstrated a substantial superiority of blind subjects in perception of auditory motion: The minimum audible movement angle of blind subjects (mean 3°) was about half the value found in matched sighted controls, whereas no such advantage was demonstrable for localization of stationary sound. There were no significant differences between early or congenitally blind subjects and late blind subjects, suggesting that long-term visual deprivation per se, independently of the point in time of its onset, was relevant for the superiority in auditory motion perception. The results were compatible with the hypothesis that in the absence of visual input the calibration of the auditory space is performed by audiomotor feedback, that is, by the evaluation of systematic changes of auditory spatial cues resulting from head and body movements. It is reasonable to assume that with blindness the neuronal circuits specifically concerned with the analysis of auditory motion are more intensely trained than in sighted people. It seems possible that the higher demand of motion analysis associated with blindness is related to processes of reorganization in the brain, as have been previously reported to occur also in areas known to be involved in auditory and/or visual motion analysis in sighted persons.     

Effects of vestibular rotatory accelerations on covert attentional orienting in vision and touch

Peripheral vestibular organs feed the central nervous system with inputs favoring the correct perception of space during head and body motion. Applying temporal order judgments (TOJs) to pairs of simultaneous or asynchronous stimuli presented in the left and right egocentric space, we evaluated the influence of leftward and rightward vestibular rotatory accelerations given around the vertical head-body axis on covert attentional orienting. In a first experiment, we presented visual stimuli in the left and right hemifield. In a second experiment, tactile stimuli were presented to hands lying on their anatomical side or in a crossed position across the sagittal body midline. In both experiments, stimuli were presented while normal subjects suppressed or did not suppress the vestibulo-ocular response (VOR) evoked by head-body rotation. Independently of VOR suppression, visual and tactile stimuli presented on the side of rotation were judged to precede simultaneous stimuli presented on the side opposite the rotation. When limbs were crossed, attentional facilitatory effects were only observed for stimuli presented to the right hand lying in the left hemispace during leftward rotatory trials with VOR suppression. This result points to spatiotopic rather than somatotopic influences of vestibular inputs, suggesting that cross-modal effects of these inputs on tactile ones operate on a representation of space that is updated following arm crossing. In a third control experiment, we demonstrated that temporal prioritization of stimuli presented on the side of rotation was not determined by response bias linked to spatial compatibility between the directions of rotation and the directional labels used in TOJs (i.e., "left" or "right" first). These findings suggest that during passive rotatory head-body accelerations, covert attention is shifted toward the direction of rotation and the direction of the fast phases of the VOR.     

Neural correlates of olfactory processing in congenital blindness

Adaptive neuroplastic changes have been well documented in congenitally blind individuals for the processing of tactile and auditory information. By contrast, very few studies have investigated olfactory processing in the absence of vision. There is ample evidence that the olfactory system is highly plastic and that blind individuals rely more on their sense of smell than the sighted do. The olfactory system in the blind is therefore likely to be susceptible to cross-modal changes similar to those observed for the tactile and auditory modalities. To test this hypothesis, we used functional magnetic resonance imaging to measure changes in the blood-oxygenation level-dependent signal in congenitally blind and blindfolded sighted control subjects during a simple odor detection task. We found several group differences in task-related activations. Compared to sighted controls, congenitally blind subjects more strongly activated primary (right amygdala) and secondary (right orbitofrontal cortex and bilateral hippocampus) olfactory areas. In addition, widespread task-related activations were found throughout the whole extent of the occipital cortex in blind but not in sighted participants. The stronger recruitment of the occipital cortex during odor detection demonstrates a preferential access of olfactory stimuli to this area when vision is lacking from birth. This finding expands current knowledge about the supramodal function of the visually deprived occipital cortex in congenital blindness, linking it also to olfactory processing in addition to tactile and auditory processing.