General Enhancement of Spatial Hearing in Congenitally Blind People

Abstract

Vision is thought to support the development of spatial abilities in the other senses. If this is true, how does spatial hearing develop in people lacking visual experience? We comprehensively addressed this question by investigating auditory-localization abilities in 17 congenitally blind and 17 sighted individuals using a psychophysical minimum-audible-angle task that lacked sensorimotor confounds. Participants were asked to compare the relative position of two sound sources located in central and peripheral, horizontal and vertical, or frontal and rear spaces. We observed unequivocal enhancement of spatial-hearing abilities in congenitally blind people, irrespective of the field of space that was assessed. Our results conclusively demonstrate that visual experience is not a prerequisite for developing optimal spatial-hearing abilities and that, in striking contrast, the lack of vision leads to a general enhancement of auditory-spatial skills.

Keywords

blindness auditory localization spatial hearing minimum audible angle open data open materials

Vision conveys spatial information in the most reliable fashion when compared with the other senses. For instance, auditory or tactile information is typically remapped toward visual positions if inputs from separate senses are spatially misaligned (Botvinick & Cohen, 1998; Howard & Templeton, 1966), short-term prismatic adaptation to spatially conflicting visual and auditory stimuli biases subsequent auditory localization toward the source of misaligned visual inputs when the prisms are removed (Recanzone, 1998), and owls reared with prismatic deviation show permanent biases in auditory localization (Knudsen, 2002). Actually, one of the primary roles of spatial hearing might be to orient our vision toward the sound source for foveation and then use our motor system to visually guide appropriate action plans based on the precise location of the target using visual coordinates (Arnott & Alain, 2011; Gruters et al., 2018). Taken together, these studies suggest that vision is important in teaching the auditory system how to translate auditory-localization cues into representations of space (Knudsen, 2002).

Does the prominent role of vision for space perception prevent people who are lacking visual experience from developing normal spatial-hearing skills? Some studies have supported the idea that congenitally blind people perform worse than sighted controls when involved in a horizontal auditory spatial-bisection task (Gori, Sandini, Martinoli, & Burr, 2014) or when they have to localize sounds arranged along the vertical midsagittal plane (Lewald, 2002; Zwiers, Van Opstal, & Cruysberg, 2001). Similarly, work in visually deprived animals has shown less precise sound-localization skills in darkness-reared animals and abnormalities in the topography and precision of the spatial tuning of their superior colliculus (Knudsen, Esterly, & Du Lac, 1991). In striking contrast, other studies have shown that congenitally blind people have improved localization acuity in the horizontal plane, particularly for peripheral sounds (King & Parsons, 1999; Rauschecker & Kniepert, 1994; Röder et al., 1999; Voss, Lassonde, & Gougoux, 2004) or during monaural auditory localization (Lessard, Paré, Lepore, & Lassonde, 1998), presumably because of a more beneficial use of spectral auditory cues (Doucet et al., 2005).

These controversial results illustrate that the role of visual experience in calibrating the development of spatial hearing remains poorly understood (Collignon, Voss, Lassonde, & Lepore, 2009; Gori et al., 2014). Addressing this question, however, is crucial for understanding how vision supports the development of spatial abilities in the remaining senses (Collignon et al., 2009). In the present study, we therefore aimed to revisit this debate by comprehensively investigating whether and how the lack of visual experience affects spatial-hearing abilities. Unlike previous studies, the present study focused on auditory-localization skills, which we investigated using a purely perceptual psychophysical minimum-audible-angle task (Mills, 1958) free of sensorimotor confounds. Moreover, sound-localization abilities were assessed in central and peripheral, horizontal and vertical, and frontal and rear portions of space. This allowed us to obtain, for the first time, a fine-grained psychophysical mapping of the global surrounding space of congenitally blind and sighted listeners. Of specific interest, we included a condition in which auditory sources were located in the rear space, which offered the unique opportunity to assess auditory-localization skills when neither the blind nor sighted participants could rely on direct sensory feedback to calibrate their spatial-hearing abilities.

Method

Participants

Seventeen congenitally blind participants (8 women; age: M = 32.6 years, SD = 7.5) and 17 age- and gender-matched sighted control participants (8 women; age: M = 31.4 years, SD = 6.2) took part in the study. All blind participants had lost their sight at birth or before 3 years of age.

Sighted participants had normal or corrected-to-normal vision. All participants reported normal hearing and no physical, neurological, or mental problems. Our sample size was determined by the availability of a maximum number of congenitally blind participants during the period of testing of this experiment (~7 months). Congenitally blind participants were recruited only if they fulfilled these well-controlled criteria for inclusion: congenital visual impairment, never experienced more than rudimentary sensitivity to brightness (no patterned vision), blindness induced by peripheral deficits (eyes or optic tracks), no neurological or psychological comorbidity, and no sensory problems other than visual deficits (see Table S1 in the Supplemental Material available online for further details).

To the best of our knowledge, all previous studies focusing on auditory-perceptual skills in blind individuals involved smaller sample sizes (between 5 and 15 participants). Furthermore, data were collected from a large number of conditions covering a variety of auditory locations with each participant. In the present study, the experimental design relied on within-subjects analysis (e.g., each psychometric curve was first extracted at the single-subject level), and goodness of fit of the psychophysical curves was evaluated through a bootstrapping procedure (500 samples). We did not conduct a formal a priori power analysis.

Participants were blindfolded and instructed to keep their eyes closed throughout the experiment. All procedures were approved by the research ethics boards of the Center for Mind/Brain Sciences and the University of Trento and conducted in accordance with the Declaration of Helsinki. All participants gave informed consent prior to the study and were financially compensated for their time.

Apparatus and stimuli

The experiment was performed in a semianechoic room. Sounds were delivered through 61 loudspeakers mounted on two semicircular horizontal and vertical planes with a radius of 1.1 m (see Fig. 1). Participants were seated in the center of the apparatus with their head on a chin rest to ensure that the speakers on the horizontal plane were at ear level and those on the vertical plane were aligned with their midsagittal plane. Each arm of the apparatus consisted of 31 loudspeakers in steps of 4° (the central speaker was shared between the two arms).

Fig. 1.

Illustration of the sound apparatus and experimental design. The apparatus consisted of 61 loudspeakers mounted on two semicircular horizontal and vertical planes, or “arms.” On each trial, a reference sound was played from a speaker on one side of an arm (designated as the central speaker, or “C”). This was followed by a target sound, which was randomly played from one of 10 adjacent speakers (ranging from ±5 to ±1 to the left or right of the central speaker). Participants were instructed to indicate the location of the target sound relative to the reference sound (“right” or “left” on the horizontal arm; “up” or “down” on the vertical arm).

Auditory stimuli were 100-ms pink-noise bursts (center frequency, f₀, of 960 Hz; rise/fall time 6 ms), presented at 65 dB-A sound-pressure level, as measured from the participant’s head position with a free-field measuring microphone (Koolertron audiometer, Shenzhen, China). Throughout the session, constant pink noise was presented at 41.8 dB-A from two loudspeakers positioned behind the acoustical apparatus. The pink noise had two purposes. First, such background noise created an ecologically valid noisy environment that masked any localized sound that could have emanated from any electrical apparatus located in the room. Second, background noise may make auditory localization more complex compared with a purely silent environment and therefore may prevent ceiling effects that could have reduced the power of our design to reveal between-group differences (Voss, Lepore, Gougoux, & Zatorre, 2011; for a review, see Collignon et al., 2009, but cf. Christensen, Lindén, Nakamura, & Barkat, 2019), which may partially explain disparities across studies. Participants responded via a keyboard placed on their right-hand side, positioned in such a way as to minimize lower sounds obstruction. The loudspeakers (4-ohm impedance with 7-W amplifier) were connected to a PCI-PXI I/O module (National Instruments, Austin, TX) designed for precise control of audiovisual-stimulus delivery with millisecond resolution. Stimuli delivery and response recording were controlled using MATLAB (Version 2014b; The MathWorks, Natick, MA). All participants were blindfolded throughout the experiment. Sighted participants were not allowed to see the apparatus before or during the experiment, in order to prevent any visual information from influencing their responses.

We relied on a two-alternative forced-choice task (up vs. down or left vs. right), avoiding any confounds linked to the use of pointing responses and therefore measuring perceptual spatial-hearing abilities directly. Because blind people cannot use visual feedback, they rarely point toward sound sources in everyday life. Moreover, visual impairment is associated with changes in the development of motor behavior involving the upper limbs (Cappagli, Cocchi, & Gori, 2017; Pardhan, Gonzalez-Alvarez, & Subramanian, 2011). Therefore, one cannot rule out the possibility that in the previous studies that required participants to point toward sound with their arms and hands, blind people performed worse than sighted people simply because of changes in goal-directed hand movements and not because of changes in their spatial-hearing abilities¹ (Finocchietti, Cappagli, & Gori, 2015; Lewald, 2002, 2013; Vercillo, Tonelli, & Gori, 2018; Voss, Tabry, & Zatorre, 2015; Zwiers et al., 2001).

Procedure

Prior to entering the room, the participants were blindfolded. When in the room, the participants sat in the center of the apparatus with their head positioned on a chin rest. The height of the chin rest was fixed, and each participant could adjust the height of the chair for comfort. This procedure was adopted to ensure that all loudspeakers along the horizontal and vertical planes were equally distant from participants’ ears (see Fig. 1). The distance between the participant and the apparatus was 1.10 m. A response panel (15.5 cm × 9.5 cm) was positioned in front of the chin rest.

During the experimental session, the sounds were played from a single plane (i.e., horizontal or vertical) at a time, with the starting plane being counterbalanced across participants). Prior to starting the task, the experimenter informed the participant which plane the sounds would be presented from. Within each plane, three different portions of space (each consisting of 11 adjacent loudspeakers) were successively assessed in a random order. Along the horizontal plane, sounds could be presented from the left, central, or right area (centered on the loudspeakers at −36°, 0°, and +36°, respectively), whereas along the vertical plane, sounds could be presented from the upper, central, or lower area (centered at +36° above the center, 0°, and −36° below the center, respectively; see Fig. 1). The participant was alerted to the upcoming stimulated area by a 100-ms beep from the corresponding area that preceded the presentation of the actual set of experimental trials (10 for each area). Moreover, the position of the participant with regard to the acoustical apparatus was manipulated six times across the session, so that the participant performed the task faced toward or away from the acoustical apparatus.

On each trial, a reference sound and a target sound, each lasting 100 ms, were presented successively with a 150-ms interval between them, followed by a 1,200-ms response gap. If a response was not provided during the response-gap period, the trial was counted as a miss, and the following trial automatically started. The reference sound was always played from the central speaker of the corresponding area; the target sound was randomly played from one of the 10 adjacent speakers (ranging from ±5 to ±1 with regard to the center reference). Participants were instructed to indicate the location of the target (second) sound relative to the reference (first) sound by pressing the left or right button for sounds presented along the horizontal plane and the up or down button for sounds presented along the vertical plane. Each speaker location (10) of each area of space (six: three vertical and three horizontal) was stimulated. In total, participants were presented with 1,200 trials (10 repetitions × 10 speaker locations × 2 participant positions × 2 planes × 3 areas). Before the experimental session, participants completed a short training session in both the vertical and horizontal planes. Between the experimental blocks, participants were allowed to take a break. In total, the session lasted for about 70 min. Scripts to run the experiment, analysis scripts, and data are available at this project’s Open Science Framework page (https://osf.io/tav35/).

Data analysis

To test for the effect of spatial arrangement of sounds on auditory-localization performance, we fitted psychometric curves to the proportion of “right” or “up” responses for the horizontal and vertical axes, respectively. For each participant, the proportion of “right” or “up” responses was calculated as a function of the location of the target sound relative to the reference sound (i.e., ±5 to ±1), separately for each condition. Condition here is defined as a combination of three factors: plane (horizontal vs. vertical), position (front vs. back), and area (left, center, right for the horizontal plane; up, center, down for the vertical plane). For each condition, the proportion of “right” or “up” responses was fitted using the cumulative normal function, through maximum likelihood estimation (fitting procedures were performed in R using the quickpsy package; Linares & Lopez-Moliner, 2016; R Core Team, 2017). In addition, the goodness of fit for each participant and each condition was assessed by using bootstrapping (500 samples) to calculate the p value of the deviance. First, the psychometric function (i.e., the fit) was used for generating 500 bootstrap samples, and for each sample, the best fit and the deviance were calculated. The distribution of the deviances was used to calculate the probability of obtaining a value of the deviance larger than the deviance evaluated for the original data (the fit was considered as poor if the p value was less than .05). For spatial-location discrimination, the one threshold score per participant and per condition (the difference in space required to shift the performance from 50% to 75%) and point of subjective equality (PSE; the mean of psychometric function) were extracted from the fitted function. We identified two types of outlying values, and we excluded them from further analyses (8.3% in total). The first type is constituted by the conditions for which poor goodness of fit, evaluated through the bootstrapping procedure, resulted from the psychophysical models (5.9%). The second type of outlying value was any participant threshold value that deviated more than 3 standard deviations from the mean of that condition (2.4% of the data).

The threshold values extracted from the psychometric curves were submitted to a linear mixed-effects model (LMM), as computed through the lme function in R (nlme package, Pinheiro & R Core Team, 2014, in combination with the lmerTest package, Kuznetsova, Brockhoff, & Christensen, 2017). An LMM was performed on the whole data set, with plane, position, and group as fixed effects and subject as a random effect. To consider the high variability in the vertical-plane threshold values compared with the horizontal plane, we allowed the option of different variances for each level of plane. Then two LMMs were computed on the thresholds reported for the horizontal and vertical planes separately, with area, position, and group as fixed effects and subject as a random effect. We assumed that response distribution would differ across participants, but in this case they all had the same slope, so all the LMMs included only random intercepts. We computed the test of significance of the different factors (Satterthwaite degrees-of-freedom-approximation method) for each of the LMMs in order to evaluate the global effects of the predictors. False-discovery-rate (FDR) correction was applied for multiple post hoc comparisons (see also Supplemental Analyses and Table S2 in the Supplemental Material for post hoc tests of interactions). Note that because of the complexity of calculating true degrees of freedom in LMMs, we used the Satterthwaite approximation approach, and the denominator degrees of freedom were determined by the grouping level at which the term was estimated (Pinheiro & Bates, 2000, Chapter 2.4). A similar approach to the threshold values was adopted to analyze PSE measures. PSE analysis and visualization (including individual participant estimates of PSE) are presented in the Supplemental Material (see Supplemental Analyses and Fig. S1).

To further analyze our data without modeling them with curve fitting, we created three generalized linear mixed models (GLMMs) directly on the proportion of correct responses. Using the R function glmer (package lme4), we modeled the experimental stimulus (i.e., loudspeakers placed in 10 equally spaced locations) as a continuous predictor; the proportion of correct responses as a response variable; area, position, and group as fixed effects; and subject as a random effect. Such a GLMM procedure with probit link function provides group-level and individual-level estimates of slope and PSE (Moscatelli et al., 2012). We not only replicated our main results but also actually observed a gain in the statistical power of our main group differences (see Supplemental Analyses and Fig. S2 in the Supplemental Material). All codes relevant to analysis of the main and supplemental findings are available at this project’s Open Science Framework page (https://osf.io/tav35/).

Results

Results for the two groups are shown in Figure 2, separately for each experimental condition. The individual threshold and PSE values across horizontal and vertical conditions are shown in Figure S1 as scatterplots.

Fig. 2.

Results for congenitally blind (CB) and sighted control (SC) participants in the minimum-audible-angle task. Curve-fitting representation is at the group level for illustration purposes only. For each position participants took relative to the apparatus (front, i.e., facing the apparatus, and back, i.e., having their backs to the apparatus), the main graphs show the proportion of “right” responses for each of the three areas in the horizontal plane (left, center, right) and the proportion of “up” responses for each of the three areas in the vertical plane (up, center, down). The x-axes represent the location of each speaker relative to the center (C): far left (L5) to far right (R5) for the horizontal plane and farthest down (D5) and farthest up (U5) for the vertical plane. The insets within each main graph show the individual threshold values (circles) in degrees of angle for the CB and SC participants. The horizontal bars represent group means, and the error bars indicate standard deviations. The filled triangles for the CB group indicate the two early-blind participants who were not fully blind at birth.

Thresholds

In the first LMM, we analyzed the auditory-localization performance of congenitally blind and sighted participants by considering plane, position, and group as fixed effects and subject as a random effect (marginal R² = .72; conditional R² = .84). In the model, within-plane spatial areas (e.g., left, center, and right) were concatenated in order to create a plane predictor. This analysis revealed a significant effect of group, F(1, 32) = 6.44, p = .016, indicating lower overall thresholds (i.e., superior auditory-localization performance) of congenitally blind compared with sighted participants. The effect of position was also significant, F(1, 332) = 20.8, p < .001, showing better performance when participants were facing the speakers. A significant main effect of plane, F(1, 332) = 43.35, p < .001, showed that the auditory-localization task was easier in the horizontal plane compared with the vertical plane. The plane-by-group interaction was significant, F(1, 332) = 14.84, p < .001, demonstrating that despite the performance of the two groups differing significantly both in the horizontal plane, t(31.9) = −2.25, p = .03, and the vertical plane, t(199.2) = −4.57, p < .001, the group difference was stronger in the vertical plane (p values for two pairwise t tests were FDR corrected). A significant interaction between plane and head, F(1, 332) = 5.81, p = .017, suggested that although performance for both the horizontal and vertical planes decreased when participants had their backs to the apparatus, localization was affected the most in the vertical plane—horizontal plane: t(160.1) = −4.02, p < .001; vertical plane: t(173.3) = −3.19, p = .002 (p values for two pairwise t tests were FDR corrected).

To further investigate the effect of spatial areas (e.g., left, center, and right in the horizontal plane) in auditory localization, the threshold values were entered into two LMMs for each plane separately. Group, position, and area predictors were entered as fixed effects and subjects was entered as a random effect (marginal R² = .20; conditional R² = .56). In the model for the horizontal data, the global main effects of group, position, and area were significant. The main effect of group showed that the congenitally blind participants were overall more proficient than the sighted control participants, F(1, 32) = 5.45, p = .026. The main effect of position, F(1, 147) = 19.89, p < .001, showed an advantage for localizing sounds coming from the front. Post hoc comparisons on the main effect of area, F(2, 147) = 13.76, p < .001, showed that the discrimination thresholds were overall significantly lower for the central area compared with the two peripheral ones—left vs. center, t(147.7) = 4.85, p < .001; center vs. right, t(147.6) = 4.14, p < .001; left vs. right, t(147.3) = 0.7, p = .49 (p values for three pairwise t tests were FDR corrected). The interaction between area and group, F(2, 147) = 3.18, p = .045, indicated that congenitally blind participants were more accurate at localizing sounds in the peripheral areas compared with the sighted control participants—left area: t(56.7) = −2.47, p = .028; center area: t(57.83) = −0.71, p = .5; right area: t(55.8) = −2.84, p = .023 (p values for three pairwise t tests were FDR corrected).

The LMM computed on the vertical data (marginal R² = .22; conditional R² = .67) also showed a significant global effect of group, F(1, 32) = 7.23, p = .01, revealing overall better performance in congenitally blind participants. We also observed a main effect of position, F(1, 137) = 19.68, p < .001, with better localization for sounds coming from the front. Post hoc comparisons on the main effect of area, F(2, 137) = 7.58, p < .001, showed that the thresholds were higher overall when sounds were localized in the upper area compared with the center area, t(133.8) = 4.01, p < .001, and the upper area compared with the down area, t(134.2) = −3.9, p < .001, with no differences between the center and down areas, t(133.4) = −0.15, p = 0.8 (p values for three pairwise t tests were FDR corrected). The significant interaction between position and area, F(2, 137) = 7.6, p < .001, is due to the absence of a difference between front and rear space in the down area—center area: t(134.9) = −2.45, p = .023; up area: t(135.6) = −5.26, p < .001 (p values for three pairwise t tests were FDR corrected).

Point of subjective equality

The PSE is the test location that is perceived to be the equal of the reference stimulus location for each space. LMM analyses on PSEs were carried out separately for each plane. In summary, the results revealed a higher tendency to respond “left” when sounds were presented in the left area of horizontal space, a bias that was more pronounced in the congenitally blind participants (Cattaneo et al., 2011; see Supplemental Analyses in the Supplemental Material).

Discussion

Several studies have suggested that vision may support the development of spatial abilities in the remaining senses (Knudsen, 2002) and that, therefore, the lack of vision since birth may prevent the optimal development of spatial-hearing skills (Gori et al., 2014). In striking contrast with this view, our results are unequivocal in showing that early visual deprivation triggers a general enhancement of auditory-spatial abilities. We therefore conclude that vision is not essential to calibrate the development of auditory-spatial abilities and that enhanced reliance on auditory cues in early-blind people induces an improvement in auditory-localization skills (Collignon et al., 2009).

Our findings contrast those of previous studies showing an impairment of spatial-hearing abilities in the early blind (Finocchietti et al., 2015; Gori et al., 2014; Lewald, 2002, 2013; Vercillo, Burr, & Gori, 2016; Voss et al., 2015; Zwiers et al., 2001). This discrepancy might be explained by considering the experimental paradigms used in those conflicting studies. First, several studies showing deficits in blind participants compared with sighted control participants have relied on a spatial-bisection task (Gori et al., 2014; Vercillo et al., 2016). Spatial-bisection tasks might be impaired in early-blind participants for two reasons that are independent of pure perceptual auditory-spatial skills. First, spatial-bisection tasks induce a mandatory conflict between space and time because shorter and longer (spatial) distances have the same (temporal) duration. Because of their acute auditory skills (as demonstrated here), early-blind people may be especially sensitive to such spatiotemporal incongruencies, resulting in altered performance (Gori, Amadeo, & Campus, 2018). Second, spatial-bisection tasks require a metric representation of external space (Vercillo et al., 2018). Indeed, early-blind people have qualitative alterations in their perception of external space (Crollen et al., 2017), which may explain their specific difficulties in resolving spatial-bisection tasks independently of their intrinsic spatial-hearing abilities (Collignon et al., 2009). Supporting this view, one recent study found that severe deficits of early-blind participants in localizing brief auditory stimuli with respect to external acoustic landmarks (using a spatial-bisection task) were simply alleviated when participants had to localize the exact same sounds with respect to their own hand (using a body-centered reference frame; Vercillo et al., 2018). These results suggest that the spatial deficit of early-blind individuals in the spatial-bisection task is not due to impaired spatial-hearing abilities but is rather the by-product of an altered representation of metric relationships in external space (Crollen, Spruyt, Mahau, Bottini, & Collignon, 2019; Vercillo et al., 2018). In contrast, the minimum-audible-angle task can be proficiently performed by relying on a mere topographical representation of sounds; it therefore assesses the capability to perceptually localize sounds in space without being confounded by advanced metric computations in the external space.

Another crucial difference between our paradigm and previous studies (i.e., studies that showed poorer performance in congenitally blind participants) is related to the method used to provide a response regarding the location of sounds. Several previous studies have required participants to point toward the source of sounds, either with their hand or their head (Finocchietti et al., 2015; Lewald, 2013; Vercillo et al., 2018; Voss et al., 2015; Zwiers et al., 2001), an action particularly unnatural for blind participants, who rarely point toward the source of events in the absence of visuomotor guidance. Moreover, visual impairment is associated with changes in the development of motor behavior using upper limbs (Pardhan et al., 2011). Furthermore, pointing prompts the use of an allocentric representation of space, which, as explained above, is not the default reference frame used by blind individuals (Crollen et al., 2019; Vercillo et al., 2018). Consequently, higher performance by sighted (vs. blind) individuals might artificially emerge in tasks that require pointing as a response to the location of sounds; these studies therefore would not assess pure perceptual auditory-localization abilities per se.

Although early visual deprivation enhances auditory-localization abilities overall, this perceptual enhancement is particularly marked for sounds presented in the peripheral areas (King & Parsons, 1999; Rauschecker & Kniepert, 1994; Röder et al., 1999; Voss et al., 2004). Such preferential enhancement in the auditory periphery could simply be related to the fact that sounds are more difficult to localize in the periphery, therefore opening more possibilities for experience-dependent improvement and the expression of between-group differences. Second, preferential enhancement in the periphery may be related to the fact that anatomical projections from the auditory cortex to the primary visual cortex in primates preferentially map onto the visual periphery (Falchier, Clavagnier, Barone, & Kennedy, 2002). The absence of vision might result in a strengthening of these connections, thus underlying the behaviorally observable enhancement of peripheral sensory-field representation. Another possibility is that peripheral sounds, in addition to interaural-level difference cues and interaural-temporal difference cues, rely more strongly on information provided by spectral cues (Middlebrooks & Green, 1991). The more proficient localization of peripheral stimuli would thus be explained by the superiority of congenitally blind participants at processing spectral cues (Doucet et al., 2005; Lessard et al., 1998).

Assessing spatial-hearing abilities in the rear space offers the unique opportunity to probe the relationship between visual experiences and auditory-localization skills under a condition in which neither of the two groups could rely on any direct sensory feedback during development. As expected, our results confirmed that for sighted participants, localizing sounds derived from sources straight in front of them is much easier than localizing sounds behind them (Middlebrooks & Green, 1991). More precisely, sighted participants were particularly impaired when localizing sounds located in the upper portion of rear space (Middlebrooks & Green, 1991; Oldfield & Parker, 1984). Interestingly, this difference between frontal and rear sounds was less prominent in congenitally blind participants, who again showed better performance than sighted participants. This result is instrumental in showing that the difference between blind and sighted people manifests not only in frontal regions (where sighted people typically have direct visual cues to calibrate the exact position of sound sources in external spaces) but also in situations in which both groups do not have such instantaneous visual calibration.

Blind individuals rely more on their spatial-hearing ability in navigating their environment, so it is likely that perceptual training sharpens their auditory-spatial skills. Such perceptual-training effects may also induce, and potentially be supported by, changes in the neurobiology of spatial-hearing abilities. The enhanced auditory skills could stem from either plasticity within the auditory regions or the recruitment of functionally related occipital regions that lack typical or intrinsic visual input. Previous studies have shown that regions typically dedicated to visuospatial processing (e.g., the right dorsal occipitoparietal cortex) show enhanced responses when congenitally blind people, compared with sighted people, localize sounds in space (Collignon et al., 2011). A study using transcranial magnetic stimulation found that focally and transiently disrupting the activity of the right-hemisphere middle and superior occipital gyri significantly altered auditory-spatial localization abilities in early-blind participants, while leaving pitch and intensity perception unaffected (Collignon, Lassonde, Lepore, Bastien, & Veraart, 2007). Finally, superior auditory-localization abilities of early-blind individuals have been shown to correlate with enhanced recruitment of the occipital cortex (Gougoux, Zatorre, Lassonde, Voss, & Lepore, 2005). However, elucidating how brain plasticity links to enhanced auditory-spatial skills in blind people might be more complex than a simple linear relationship between spatial-hearing performance and occipital reorganization because recent studies have shown that the lack of vision triggers a large-scale reorganization (increased and decreased involvement) in the network dedicated to spatial hearing (Collignon et al., 2009; Dormal, Rezk, Yakobov, Lepore, & Collignon, 2016). Further studies are therefore needed to relate the superiority of congenitally blind people in auditory localization to the underlying neuroplastic mechanisms in brain networks.

Supplemental Material

BattalOccelli_OpenPracticesDisclosure-v5.1_project – Supplemental material for General Enhancement of Spatial Hearing in Congenitally Blind People

Supplemental material, BattalOccelli_OpenPracticesDisclosure-v5.1_project for General Enhancement of Spatial Hearing in Congenitally Blind People by Ceren Battal, Valeria Occelli, Giorgia Bertonati, Federica Falagiarda and Olivier Collignon in Psychological Science

Supplemental Material

Battal_Supplemental_Material_rev – Supplemental material for General Enhancement of Spatial Hearing in Congenitally Blind People

Supplemental material, Battal_Supplemental_Material_rev for General Enhancement of Spatial Hearing in Congenitally Blind People by Ceren Battal, Valeria Occelli, Giorgia Bertonati, Federica Falagiarda and Olivier Collignon in Psychological Science

Footnotes

Acknowledgements

O. Collignon is a research associate at the Fond National de la Recherche Scientifique de Belgique (FRS-FNRS). We are grateful to M. Barilari, S. Cattoir, and S. Benetti for their help with data acquisition, P. Chiesa for his continuing support with the auditory hardware, J. A. Greenwood for his methodological and statistical input, and G. Costa for the illustration in Figure 1.

Transparency

Action Editor: Philippe G. Schyns

Editor: D. Stephen Lindsay

Author Contributions

The first two authors contributed equally to this work. C. Battal and O. Collignon developed the study concept and design. G. Bertonati and C. Battal acquired the data. F. Falagiarda and C. Battal analyzed the data under the supervision of O. Collignon. V. Occelli, C. Battal, and O. Collignon drafted the manuscript, and all authors approved the final version for submission.

ORCID iD

Ceren Battal

Supplemental Material

Additional supporting information can be found at

Notes

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