Davide Bottari

Enhanced reactivity to visual stimuli in deaf individuals

PURPOSE Several studies have reported faster response time to visual stimuli in profoundly deaf individuals. This result is often linked to the processing of peripheral targets, and it is assumed to occur in relation to attention orienting. We evaluated whether enhanced reactivity to visual events in profoundly deaf individuals can be explained by faster orienting of visual attention alone. METHODS We examined 11 deaf individuals and 11 hearing controls, in a simple detection task and in a shape discrimination task. While simple detection can be performed under distributed attention, shape discrimination requires orienting of spatial attention to the target. The same visual targets served for both tasks, presented at central or peripheral locations and corrected for cortical magnification. RESULTS The simple detection task revealed faster RTs in deaf than hearing controls, regardless of target location. Moreover, while hearing controls paid a cost in responding to peripheral than central targets, deaf participants performed equally well regardless of target eccentricity. In the shape discrimination task deaf never outperformed hearing controls. CONCLUSIONS These findings reveal that enhanced reactivity to visual stimuli in the deaf cannot be explained only by faster orienting of visual attention and can emerge for central as well as peripheral targets. Moreover, the persisting advantage for peripheral locations in the deaf, observed here under distributed attention, suggests that this spatially-selective effect could result from reorganised sensory processing rather than different attentional gradients.

Changes in early cortical visual processing predict enhanced reactivity in deaf individuals.

Individuals with profound deafness rely critically on vision to interact with their environment. Improvement of visual performance as a consequence of auditory deprivation is assumed to result from cross-modal changes occurring in late stages of visual processing. Here we measured reaction times and event-related potentials (ERPs) in profoundly deaf adults and hearing controls during a speeded visual detection task, to assess to what extent the enhanced reactivity of deaf individuals could reflect plastic changes in the early cortical processing of the stimulus. We found that deaf subjects were faster than hearing controls at detecting the visual targets, regardless of their location in the visual field (peripheral or peri-foveal). This behavioural facilitation was associated with ERP changes starting from the first detectable response in the striate cortex (C1 component) at about 80 ms after stimulus onset, and in the P1 complex (100–150 ms). In addition, we found that P1 peak amplitudes predicted the response times in deaf subjects, whereas in hearing individuals visual reactivity and ERP amplitudes correlated only at later stages of processing. These findings show that long-term auditory deprivation can profoundly alter visual processing from the earliest cortical stages. Furthermore, our results provide the first evidence of a co-variation between modified brain activity (cortical plasticity) and behavioural enhancement in this sensory-deprived population.

Visual temporal order judgment in profoundly deaf individuals

We investigated temporal processing in profoundly deaf individuals by testing their ability to make temporal order judgments (TOJs) for pairs of visual stimuli presented at central or peripheral visual eccentricities. Ten profoundly deaf participants judged which of the two visual stimuli appearing on opposite sides of central fixation was delivered first. Stimuli were presented either symmetrically, at central or peripheral locations, or asymmetrically (i.e. one central and the other peripheral) at varying stimulus onset asynchronies (SOAs) using the method of constant stimuli. Two groups of hearing controls were also tested in this task: 10 hearing controls auditory-deprived during testing and 12 hearing controls who were not subjected to any deprivation procedure. Temporal order thresholds (i.e. just noticeable differences) and points of subjective simultaneity for the two visual stimuli did not differ between groups. However, faster discrimination responses were systematically observed in the deaf than in either group of hearing controls, especially when the first of the two stimuli appeared at peripheral locations. Contrary to some previous findings, our results show that a life-long auditory deprivation does not alter temporal processing abilities in the millisecond range. In fact, we show that deaf participants obtain similar temporal thresholds to hearing controls, while also responding much faster. This enhanced reactivity is documented here for the first time in the context of a temporal processing task, and we suggest it may constitute a critical aspect of the functional changes occurring as a consequence of profound deafness.

Sensitive periods for the functional specialization of the neural system for human face processing

Significance Sensitive periods in human functional brain development were tested in humans who had been blind from birth and whose sight was restored as long as 14 y later. In investigating this rare population, our data demonstrate a general principle of brain development: rather than being born with highly specialized neural systems (e.g., for specific object categories such as faces), the functional differentiation of neural circuits seems to depend on early (visual) experience involving a decrease in responsiveness to certain events during sensitive periods. The functional tuning of neural systems seems necessary to achieve high processing proficiency. The aim of the study was to identify possible sensitive phases in the development of the processing system for human faces. We tested the neural processing of faces in 11 humans who had been blind from birth and had undergone cataract surgery between 2 mo and 14 y of age. Pictures of faces and houses, scrambled versions of these pictures, and pictures of butterflies were presented while event-related potentials were recorded. Participants had to respond to the pictures of butterflies (targets) only. All participants, even those who had been blind from birth for several years, were able to categorize the pictures and to detect the targets. In healthy controls and in a group of visually impaired individuals with a history of developmental or incomplete congenital cataracts, the well-known enhancement of the N170 (negative peak around 170 ms) event-related potential to faces emerged, but a face-sensitive response was not observed in humans with a history of congenital dense cataracts. By contrast, this group showed a similar N170 response to all visual stimuli, which was indistinguishable from the N170 response to faces in the controls. The face-sensitive N170 response has been associated with the structural encoding of faces. Therefore, these data provide evidence for the hypothesis that the functional differentiation of category-specific neural representations in humans, presumably involving the elaboration of inhibitory circuits, is dependent on experience and linked to a sensitive period. Such functional specialization of neural systems seems necessary to archive high processing proficiency.

Partial recovery of visual-spatial remapping of touch after restoring vision in a congenitally blind man.

In an initial processing step, sensory events are encoded in modality specific representations in the brain but seem to be automatically remapped into a supra-modal, presumably visual-external frame of reference. To test whether there is a sensitive phase in the first years of life during which visual input is crucial for the acquisition of this remapping process, we tested a single case of a congenitally blind man whose sight was restored after the age of two years. HS performed a tactile temporal order judgment task (TOJ) which required judging the temporal order of two tactile stimuli, one presented to each index finger. In addition, a visual-tactile cross-modal congruency task was run, in which spatially congruent and spatially incongruent visual distractor stimuli were presented together with tactile stimuli. The tactile stimuli had to be localized. Both tasks were performed with an uncrossed and a crossed hand posture. Similar to congenitally blind individuals HS did not show a crossing effect in the tactile TOJ task suggesting an anatomical rather than visual-external coding of touch. In the visual-tactile task, however, external remapping of touch was observed though incomplete compared to sighted controls. These data support the hypothesis of a sensitive phase for the acquisition of an automatic use of visual-spatial representations for coding tactile input. Nonetheless, these representations seem to be acquired to some extent after the end of congenital blindness but seem to be recruited only in the context of visual stimuli and are used with a reduced efficiency.

Hearing again with two ears: recovery of spatial hearing after bilateral cochlear implantation.

Bilateral cochlear implants (CI) offer a unique opportunity for the study of spatial hearing plasticity in humans. Here we studied the recovery of spatial hearing in two sequential bilateral CI recipients, adopting a longitudinal approach. Each recipient was tested in a sound-source identification task shortly after bilateral activation and at 1, 6, and 12 months follow-up. The results show fast recovery (1 month from CI activation) in the recipient who had substantial experience with auditory cues in adulthood. By contrast, the bilateral CI recipient who developed profound deafness in childhood, regained spatial hearing abilities only 12 months after CI activation. These findings provide the first direct evidence that recovery of auditory spatial abilities in bilateral CI recipients can occur shortly after activation of the two devices. In addition, they suggest that previous auditory experience can constrain the time course of this recovery.

Prominent reflexive eye-movement orienting associated with deafness

Profound deafness affects orienting of visual attention. Until now, research focused exclusively on covert attentional orienting, neglecting whether overt oculomotor behavior may also change in deaf people. Here we used the pro- and anti-saccade task to examine the relative contribution of reflexive and voluntary eye-movement control in profoundly deaf and hearing individuals. We observed a behavioral facilitation in reflexive compared to voluntary eye movements, indexed by faster saccade latencies and smaller error rates in pro- than anti-saccade trials, which was substantially larger in deaf than hearing participants. This provides the first evidence of plastic changes related to deafness in overt oculomotor behavior, and constitutes an ecologically relevant parallel to the modulations attributed to deafness in covert attention orienting. Our findings also have implications for designers of real and virtual environments for deaf people and reveal that experiments on deaf visual abilities must not ignore the prominent reflexive eye-movement orienting in this sensory-deprived population.

Change blindness in profoundly deaf individuals and cochlear implant recipients

We used a change blindness paradigm to examine visual abilities in the profoundly deaf when exogenous capture of attention is prevented and only endogenous attention shifts are possible. Nineteen profoundly deaf participants, 22 cochlear implant recipients and 18 hearing controls were asked to detect a change occurring between two consecutive visual scenes separated by a blank. Changes occurred on half of the trials, either at central or peripheral locations, and the task was performed under focused attention (at the centre or at the periphery) or under distributed attention. When allowed to focus attention, all groups showed comparable change sensitivity, with better performance for central than peripheral stimuli. However, in the distributed condition, only the profoundly deaf participants remained reliably more sensitive to changes occurring at central than peripheral locations. This finding contradicts the well-known visual performance enhancement typically observed for peripheral regions of the visual field in the profoundly deaf. We suggest that this discrepancy between our novel finding and the existing literature reflects the strictly endogenous nature of our change blindness paradigm. Our results point to a differential role of exogenous and endogenous attention components in the multisensory plasticity occurring after auditory deprivation and suggest that compensatory abilities in the deaf may be linked to exogenous capture of visual attention.

Audio-tactile integration in congenitally and late deaf cochlear implant users.

Several studies conducted in mammals and humans have shown that multisensory processing may be impaired following congenital sensory loss and in particular if no experience is achieved within specific early developmental time windows known as sensitive periods. In this study we investigated whether basic multisensory abilities are impaired in hearing-restored individuals with deafness acquired at different stages of development. To this aim, we tested congenitally and late deaf cochlear implant (CI) recipients, age-matched with two groups of hearing controls, on an audio-tactile redundancy paradigm, in which reaction times to unimodal and crossmodal redundant signals were measured. Our results showed that both congenitally and late deaf CI recipients were able to integrate audio-tactile stimuli, suggesting that congenital and acquired deafness does not prevent the development and recovery of basic multisensory processing. However, we found that congenitally deaf CI recipients had a lower multisensory gain compared to their matched controls, which may be explained by their faster responses to tactile stimuli. We discuss this finding in the context of reorganisation of the sensory systems following sensory loss and the possibility that these changes cannot be “rewired” through auditory reafferentation.

Spatial hearing with a single cochlear implant in late-implanted adults

We assessed sound localisation abilities of late-implanted adults fitted with a single cochlear implant (CI) and examined whether these abilities are affected by the duration of implant use. Ten prelingually and four postlingually deafened adults who received a unilateral CI were tested in a sound-source identification task. Above chance performance was observed in those prelingual CI recipients who had worn their implant for longer time (9 years on average), revealing some monaural sound localisation abilities in this population but only after extensive CI use. On the contrary, the four postlingual recipients performed equal or better with respect to the best prelingual participants despite shorter experience with the monaural implant (11 months on average). Our findings reveal that some sound localisation ability can emerge in prelingually deafened adults fitted with a single implant, at least in a controlled laboratory setting. This ability, however, appears to emerge only after several years of CI use. Furthermore, the results of four postlingually deafened adults suggest that early experience with auditory cues may result in more rapid acquisition of spatial hearing with a single CI.