Acta Psychologica 146 (2014) 58–62
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Does visual experience influence the spatial distribution of auditory attention?☆ Elodie Lerens, Laurent Renier ⁎ Université catholique de Louvain, Institute of Neuroscience (IoNS), Avenue Hippocrate, 54, UCL B1.54.09, 1200, Brussels, Belgium
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Article history: Received 4 July 2013 Received in revised form 26 November 2013 Accepted 5 December 2013 Available online 28 December 2013 PsycINFO codes: 2326 Auditory & Speech Perception 2346 Attention 3299 Vision & Hearing & Sensory Disorders Keywords: Visual deprivation Early blindness Auditory perception Brain plasticity Attention Compensatory mechanisms
a b s t r a c t Sighted individuals are less accurate and slower to localize sounds coming from the peripheral space than sounds coming from the frontal space. This specific bias in favour of the frontal auditory space seems reduced in early blind individuals, who are particularly better than sighted individuals at localizing sounds coming from the peripheral space. Currently, it is not clear to what extent this bias in the auditory space is a general phenomenon or if it applies only to spatial processing (i.e. sound localization). In our approach we compared the performance of early blind participants with that of sighted subjects during a frequency discrimination task with sounds originating either from frontal or peripheral locations. Results showed that early blind participants discriminated faster than sighted subjects both peripheral and frontal sounds. In addition, sighted subjects were faster at discriminating frontal sounds than peripheral ones, whereas early blind participants showed equal discrimination speed for frontal and peripheral sounds. We conclude that the spatial bias observed in sighted subjects reflects an unbalance in the spatial distribution of auditory attention resources that is induced by visual experience. © 2013 The Authors. Published by Elsevier B.V. All rights reserved.
1. Introduction Does visual experience determine the spatial distribution of attention resources in the auditory modality? We know from animal studies that vision plays a role in calibrating the spatial representation of the auditory sense (Knudsen & Knudsen, 1985, 1989; Withington, Binns, Ingham, & Thornton, 1994). Studies in visually deprived animals also clearly demonstrated how visual experience affects performance in the auditory modality (Rauschecker, 1995). While sighted human and non-human primates localize less accurately (and more slowly) sounds coming from the peripheral space as compared to the frontal one (Oldfield & Parker, 1984; Recanzone & Beckerman, 2004; TederSälejärvi, Hillyard, Röder, & Neville, 1999), such disadvantage for peripheral sounds seems reduced in congenitally blind individuals (Röder et al., 1999; Voss et al., 2004). Visually deprived animals and humans are better than sighted subjects at localizing sounds coming from the peripheral space (Chen, Zhang, & Zhou, 2006; Rauschecker & ☆ This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-No Derivative Works License, which permits noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited. ⁎ Corresponding author at: Avenue Hippocrate, 54, UCL-B1.54.09, 1200 Brussels, Belgium, Tel.: +32 2 764 54 56; fax: +32 2 764 94 22. E-mail address: [email protected] (L. Renier).
Kniepert, 1994; Röder et al., 1999; Voss et al., 2004) and from the back space (Després, Candas, & Dufour, 2005; Voss et al., 2004), whereas equal performance levels are observed for frontal sounds (Després et al., 2005; Röder et al., 1999; Voss et al., 2004; Zwiers, Van Opstal, & Cruysberg, 2001a, 2001b). Interestingly, a similar effect of the auditory experience on the spatial distribution of attention between the central and the peripheral visual fields was reported in studies in early deaf individuals (Bavelier, Dye, & Hauser, 2006; Bavelier et al., 2000; Proksch & Bavelier, 2002). To date, no study has investigated the potential effect of sound source location on non-spatial processing either in sighted or in early blind individuals. General attention mechanisms could mediate this effect of the sound source location on the stimulus processing abilities (e.g. stimulus localization or discrimination). The present study aimed to test the effects of visual experience on auditory discrimination abilities in the frontal and the peripheral space. We hypothesized that sighted participants would be affected by an attention bias that leads them to most efficiently (i.e. more accurately and/or more rapidly) process the sounds originating from frontal locations, whereas early blind participants would have equivalent performance levels across the sound source locations. A secondary goal was to test to what extent blind individuals are better than sighted ones when simultaneously attending to multiple potential sound sources versus only one sound source. Since blind
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E. Lerens, L. Renier / Acta Psychologica 146 (2014) 58–62
individuals need to be more attentive than sighted individuals to multiple auditory stimulations from their surrounding environment, we hypothesized that they would typically perform better than sighted individuals in situations involving multiple stimulation sources than in situations involving a single one. 2. Methods 2.1. Subjects Twelve early and totally blind individuals (EB) and 12 sighted controls (SC), matched for gender (10 men), age (EB: 38 ± 12; SC: 37.5 ± 16) and self-rated musical experience (evaluated on a “5 level” scale that took into account both expertise (how well) and musical practice amount (0: no musical notion, 1: some musical notions associated with an old or current practice of a musical instrument, 2: good musical notions associated with a regular practice of a musical instrument, 3: professional player, 4: absolute pitch, EB: 1.8 ± 1.3, SC: 1.8 ± 1.1)), took part to the experiment. The musical experience was evaluated to test its potential effect on frequency discrimination, since increased tonal processing capabilities in musicians have been reported in the literature (Micheyl, Delhommeau, Perrot, & Oxenham, 2006; Pitt, 1994). The participants were totally blind due to congenital or early (before the age of three) peripheral deficits (see Table 1 for additional details). No participant reported neurological, psychiatric illness or auditory impairment. All participants signed an informed consent. This experiment was approved by the ethics committee of the school of medicine of the Université catholique de Louvain. 2.2. Stimuli and materials Stimuli consisted of three broadband noises of 60 dB of intensity created using “Adobe Audition” and filtered with three different bandpasses: 2500–4500 Hz for the target, 1500–3500 Hz for the distractor 1 and 500–2500 Hz for the distractor 2. The stimuli duration was 100 milliseconds (ms) including 10 ms rise and 10 ms fall. The stimuli were presented via three speakers located on a half-circle placed at a distance of 70 cm from the centre of the head (see Fig. 1(A)). The first speaker was located in front of the participant and corresponded to the frontal location. The second speaker was located at the extreme Table 1 Characteristics of the blind participants. Participants Age Sex Musical experience
Blindness onset
Cause of blindness
EBa 1
26
Mb
4
congenital
EB 2
39
Fc
0
congenital
EB 3
60
M
2
EB 4
35
M
2
infancy (b2 years) congenital
Genetic eye disorder (abnormal retina development) Retinopathy of prematurity Bilateral retinoblastoma
EB 5 EB 6 EB 7 EB 8 EB 9
31 35 48 52 27
M M M M M
2 1 4 1 2
congenital congenital congenital congenital congenital
EB 10 EB 11
55 24
M M
2 0
congenital infancy (b3 years)
EB 12
34
F
1
congenital
Genetic eye disorder (abnormal retina development) Optic Leber neuropathy Optic Leber neuropathy Genetic eye disorder* Bilateral retinoblastoma Genetic eye disorder (abnormal retina development) Retinal degeneration Genetic eye disorder (abnormal retina development) Retinopathy of prematurity
Note: EB: early blind; M: male; F: female; (*) no additional details available.
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left of the participant, corresponding to − 90°azimuth and the third speaker was located at the extreme right of the participant, corresponding to +90° azimuth, both being considered as peripheral locations. We used one speaker per location (i.e. frontal, peripheral right and peripheral left) instead of a set of numerous close speakers for each attended location as used in previous studies (e.g. Röder et al., 1999) since our goal was to evaluate the effect of the speaker location on frequency discrimination and not to determine the ability to finely discriminate between close spatial locations. 2.3. Procedure Participants were instructed to perform an auditory target detection task; they had to press a button as quickly as possible at the target presentation regardless of the speaker it originated from. Three different conditions were administered in a counterbalanced order: two experimental conditions and one control condition. In the first experimental condition, called “wide spatial distribution”, targets and distractors came sequentially and pseudo-randomly from the frontal and the peripheral (right and left) speakers. The participants had to pay attention to the three sound source locations. In the second condition, called “focused spatial distribution”, targets and distractors always came from the same speaker (either from the front, the right or the left) in each sub-condition. In this condition, the speaker location was announced to the participants at the beginning of each sub-condition, so that they could focus on it. For the two experimental conditions, a total of 1650 stimuli were presented with a ratio of 1/3 of targets, 1/3 of distractors 1 and 1/3 of distractors 2. The targets and the distractors were presented sequentially in a pseudo-random order with the only constraint that two targets were never presented consecutively (Fig. 1(B)). Different interstimulus intervals were used (ISIs: 500, 700, 900, 1100, 1300 ms). The control condition consisted in an auditory detection task during which the target appeared pseudo-randomly at one of the three locations. The subjects had to press the button as quickly as possible at the stimulus presentation. No distractor was presented during this condition. In the control condition, one hundred targets appeared pseudo-randomly either from the front, the right or the left speaker. The rest of the procedure in the control condition was identical to the experimental conditions. The entire testing took place in a sound attenuated room. The speakers were positioned at ear level and the head was wedged with a cushion in order to maintain it in the same orientation throughout the experiment. Sighted participants were blindfolded throughout the experiment. Before the experiment, the target and the two distractors were presented to the participants. Then the participants underwent a brief familiarization session (20 trials for each condition). Stimulations and responses recording were controlled using Matlab (Mathworks Inc. Sherborn MA, USA). Participants delivered their responses via a mouse of high temporal accuracy (Razer, model number: RZ01-0015). Breaks of few minutes were introduced every 8 min to reduce any potential decrease of attention. 3. Data analyses For the experimental conditions, we performed two separate 2 (groups: EB vs SC) ×2 (spatial distribution of the stimuli: “wide spatial distribution” vs “focused spatial distribution”) ×2 (sound source locations: front vs periphery) analyses of variance (ANOVAs): on the reaction times (RTs) for the hits (targets correctly detected) and on the target omissions rates. In addition, simple effects were tested on the RTs using Student t-tests. The false alarm (FA) rates were too low (1.2% on average) in all conditions to allow discriminating between conditions and groups and were therefore not further analyzed. We carried out a Pearson correlation analysis in order to test the relation between the musical experience and RTs. The RTs and the target omissions rates of the control condition were evaluated with two separate 2 (EB vs SC) × 2 (front vs periphery) ANOVAs.
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Fig. 1. Experimental setup and procedure (A) Participants seated in a sound attenuated room with the three speakers located at a distance of 70 cm to the center of the subject's head. One speaker was placed in front of the subject (0°) and two speakers were located at 90°azimuth to the left (−90°) and to the right (90°) of the mid-sagittal plane of the participant. The head was wedged with a cushion in order to maintain it in the same orientation throughout the experiment. (B) Example of a time course for the condition “wide spatial distribution” of the stimuli. Targets and distractors came sequentially from the three different speakers and were separated by variable inter-stimuli intervals. Participants had to detect the targets independently to their spatial origin.
4. Results On average the subjects correctly performed the task in all conditions as relatively few omissions (3.3%) and false alarms (1.2%) were recorded. The ANOVA performed on the RTs revealed an effect of the group [F(1,22) = 11.24, p b 0.005], no effect of the target location [F(1,22) = 1.3, p = 0.26] and no effect of the spatial distribution of the stimuli [F(1,22) = 0.53, p = 0.47]. EB participants were faster (mean in milliseconds ± SEM: 307 ± 10) than SC participants (364 ± 13). An interaction between the group and the target location was present [F(1,22) = 8.23, p b 0.01] (see Fig. 2A). Student t-test revealed a difference between the front and the periphery in SC participants only [SC: t(11) = − 3.18, p b 0.01]; sighted participants were faster to detect frontal targets than peripheral ones unlike early blind participants. No other double interaction was observed (all ps N 0.1), but a triple interaction between the group, the spatial distribution of the stimuli and the target location was present [F(1,22) = 5.64, p b 0.05] indicating that the interaction between group and target location was not equivalent in the two spatial distribution conditions. When we decomposed the triple interaction, we observed an interaction between the group and the target location in the “focused spatial distribution” (F(1,22) = 7.58, p b 0.05) and not in the “wide spatial distribution” (F(1,22) = 2.8, p = 0.108). Analyses of the simple effects of the target location within each group and each spatial distribution condition showed a significant effect of the target location in both spatial distribution conditions in SC subjects only (all ps b 0.05 in SC subjects and all ps N 0.1 in EB subjects). Analyses of the simple effects of the group within each target location and each spatial distribution condition revealed a significant effect
of the group in all conditions (all ps b 0.005) except for frontal targets in the “focused spatial distribution” where only a trend was present (p = 0.079). This slightly reduced group difference for the frontal targets in the “focused spatial distribution” as compared to all other conditions probably explains the double interaction between group and target location observed in the “focused spatial distribution” and not in the “wide spatial distribution”, hence explaining the triple interaction. The ANOVA performed on target omission rates revealed a marginal group effect [F(1,22) = 3.46, p = 0.076], a target location effect [F(1,22) = 6, p b 0.05] and a marginal effect of the spatial distribution of the stimuli [F (1,22) = 3.59, p = 0.071]. EB participants tended to make fewer omissions than SC participants (EB: 0.9% ± 0.4, SC: 5.6% ± 2.5). There were fewer omissions for the frontal targets (2% ± 0.9) than for the peripheral ones (4.4% ± 1.7). There was a trend towards fewer omissions for the “focused spatial distribution” (2% ± 0.8) than for the “wide spatial distribution” (4.4% ± 1.8). There was a marginal interaction between the group and the target location [F(1,22) = 3.46, p = 0.076; EB: front: 0.6 ± 1.2, periphery: 1.2 ± 2.4; SC: front: 3.5 ± 1.2, periphery: 7.7 ± 2.4] (see Fig. 2B). No other interaction was significant (all ps N 0.05). The correlation analysis between the RTs and the musical experience level was not significant (r = − 0.26; p = 0.22 in the whole group, r = − 0.459; p = 0.133 in EB participants and r = − 0.255; p = 0.424 in SC participants). For the control condition, the ANOVA performed on the RTs revealed no group effect [F(1,22) = 1.7, p = 0.21; EB = 202 ± 9, SC = 222 ± 12], a target location effect [F(1,22) = 4.5, p b 0.05] and no interaction between the target location and the group [F(1,22) = 0.12, p = 0.74]. The RTs for the frontal targets were shorter than for the
Fig. 2. Performance of early blind subjects and sighted control participants as a function of the spatial location of the targets (frontal speaker vs. peripheral ones) (A) Mean reaction times (RT) in milliseconds (ms) as a function of the group (blind vs sighted) and the target location (front vs periphery). The RTs of the blind participants were shorter than the RTs of the sighted controls (p b 0.005) and there was an interaction between the group and the target source location (p b 0.01). (B) Mean omissions rates (%) as a function of the group (blind vs sighted) and the target location (front vs periphery). There was a marginal group effect (p = 0.076) and an effect of the target source location was present (p b 0.05). A marginal interaction between the group and the target location was also observed (p = 0.076). Error bars are standard errors of the mean (SEM). Results for the “focused spatial distribution” and “wide spatial distribution” were plotted together since there was no effect of the spatial distribution of the stimuli (p N 0.1).
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peripheral ones (Front = 209 ± 7, Periphery = 215 ± 9). The ANOVA performed on target omissions rates revealed no significant effect (all ps N 0.05). 5. Discussion 5.1. Visual experience constrains the spatial distribution of auditory attention The present study is one of the first attempts to investigate the effect of sound source location on non-spatial processing either in sighted or in early blind individuals. Sighted participants discriminated frontal targets faster than peripheral ones while early blind participants performed equally fast for frontal and peripheral targets. This difference between early blind and sighted subjects in the performance profile may depend on a difference in the spatial distribution of attention in the two groups, this difference being supposedly induced by visual experience. A possible explanation to this effect of visual experience on the spatial distribution of attention would be that sighted individuals spontaneously orient their head towards the source of the sounds that may have a potential interest or value for them (e.g. a speaker, television), in order to complement their auditory perception with visual information (e.g. images, lipreading). Consequently, they may develop a greater expertise for processing frontal stimuli more efficiently than peripheral ones. We noticed that some of our blind volunteers do not orient spontaneously their head toward what they are listening to (e.g. the speaker) even if some of them learned to do it when they are speaking to someone. Consequently, early blind individuals would not develop a specific practice-related expertise for more efficiently processing frontal sounds than peripheral ones; they would rather process frontal and peripheral sounds indifferently. It is worth noting that a similar frontal advantage in sighted subjects was previously observed in studies that used localization tasks (Teder-Sälejärvi et al., 1999) while this frontal advantage was reduced in early blind subjects in similar tasks (Després et al., 2005; Röder et al., 1999; Voss et al., 2004). Interestingly, Teder-Sälejärvi and Hillyard (1998) and Teder-Sälejärvi et al. (1999) reported that when the participants explicitly paid attention to a specific part of the surrounding space, the localization performance (i.e. accuracy and speed) improved for this location. This illustrates how inducing a change in the spatial distribution of attention (i.e. orienting it toward a specific location) affects auditory processing abilities across spatial locations. In the visual domain, studies in deafness offer an interesting example of how auditory deprivation influences the spatial distribution of visual attention between the central/foveal and the peripheral visual fields (Bavelier et al., 2000, 2006; Dye, Hauser, & Bavelier, 2009; Proksch & Bavelier, 2002). It is particularly worth noting that in both cases (blindness and deafness), sensory deprivation leads to a relative favouring of the peripheral space as compared to what is observed in sighted or hearing persons. Peripheral vision or peripheral audition is less accurate than central/foveal vision or frontal audition. Sighted and hearing individuals may use the convergence of the two senses, audition and vision, to be efficient in the peripheral space. Without vision or audition to compensate that specific weakness in the peripheral space, sensory deprived individuals would typically improve their peripheral vision or audition. 5.2. Improved auditory discrimination in early blindness The present study showed that early blind participants were faster (and tend to be more accurate) than sighted controls to detect an auditory target among distractor sounds. This group difference was observed for sounds originating both from frontal and peripheral location(s) and in conditions involving both a single and multiple sound source location(s). In accordance with Wan, Wood, Reutens, and Wilson (2010a), the improvement of the sound frequency
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discrimination ability in early blind participants was found independently of musical experience since each individual blind subject was matched for this aspect to a control participant and that performance did not correlate with musical experience. In addition, the improvement observed in early blind participants did not depend on a difference in simple reaction time since no group difference was observed for the RTs in the control condition. This suggests that this compensatory mechanism involves higher level processes such as frequency discrimination and attention. These results are consistent with previous studies that reported supra-normal sound frequency discrimination and categorization abilities in early blind individuals (Gougoux et al., 2004; Hamilton, Pascual-Leone, & Schlaug, 2004; Voss, Lepore, Gougoux, & Zatorre, 2011; Wan et al., 2010a), while they had equal performances for low demand attention tasks (Collignon, Renier, Bruyer, Tranduy, & Veraart, 2006; Kujala, Lehtokoski, Alho, Kekoni, & Risto, 1997; Kujala et al., 2005). In the absence of vision, blind individuals rely only on audition, tact and olfaction and therefore use them more intensively, which would result in the development of improved perceptual abilities (Alary et al., 2009; Beaulieu-Lefebvre, Schneider, Kupers, & Ptito, 2011; Cuevas, Plaza, Rombaux, De Volder, & Renier, 2009; Goldreich & Kanics, 2003; Gougoux et al., 2004; Lessard, Paré, Lepore, & Lassonde, 1998; Lewald, 2013; Norman & Bartholomew, 2011; Pascual-Leone, Amedi, Fregni, & Merabet, 2005; Rauschecker, 1995; Renier, De Volder, & Rauschecker, in press; Wan, Wood, Reutens, & Wilson, 2010b; Wong, Gnanakumaran, & Goldreich, 2011). In the present study, we also tested whether the improvement in early blind individuals was more pronounced in conditions involving multiple sound sources as compared to conditions involving only one source. Contrary to our initial hypothesis, the stimuli spatial distribution (i.e. 1 vs 3 sound source(s)) did not have any particular effect on either the early blind or the sighted control participants, except that both groups tended to make fewer omissions in the “focused spatial distribution” than in the “wide spatial distribution”. We cannot exclude that the difference in difficulty levels between both conditions was insufficient for any effect of this factor to be observed. 5.3. Conclusions The present study indicates that visual experience influences the way we distribute our auditory attention around us. A bias leading to a favouring of the frontal space at the expense of the peripheral one was present in sighted individuals and absent in early blind individuals during auditory discrimination. Acknowledgments We wish to thank Anne G. De Volder, who is a senior research associate at the Belgian National Funds for Scientific Research (FNRS). E. Lerens was supported by the National Fund for Scientific Research (Belgium). L. Renier is a Postdoctoral Researcher supported by the Brussels Institute for Research and Innovation (INNOVIRIS, Belgium). This study was supported by FRSM grant #3.4502.08 (Belgium). References Alary, F., Duquette, M., Goldstein, R., Elaine Chapman, C., Voss, P., La Buissonnière-Ariza, V., et al. (2009). Tactile acuity in the blind: A closer look reveals superiority over the sighted in some but not all cutaneous tasks. Neuropsychologia, 47(10), 2037–2043. Bavelier, D., Dye, M. W. G., & Hauser, P. C. (2006). Do deaf individuals see better? Trends in Cognitive Sciences, 10, 512–518. Bavelier, D., Tomann, A., Hutton, C., Mitchell, T., Corina, D., Liu, G., et al. (2000). Visual attention to the periphery is enhanced in congenitally deaf individuals. Journal of Neuroscience, 20, 1–6. Beaulieu-Lefebvre, M., Schneider, F. C., Kupers, R., & Ptito, M. (2011). Odor perception and odor awareness in congenital blindness. Brain Research Bulletin, 84(3), 206–209. Chen, Q., Zhang, M., & Zhou, X. (2006). Spatial and nonspatial peripheral auditory processing in congenitally blind people. NeuroReport, 17, 1449–1452.
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Acta Psychologica journal homepage: www.elsevier.com/ locate/actpsy
Does visual experience influence the spatial distribution of auditory attention?☆ Elodie Lerens, Laurent Renier ⁎ Université catholique de Louvain, Institute of Neuroscience (IoNS), Avenue Hippocrate, 54, UCL B1.54.09, 1200, Brussels, Belgium
a r t i c l e
i n f o
Article history: Received 4 July 2013 Received in revised form 26 November 2013 Accepted 5 December 2013 Available online 28 December 2013 PsycINFO codes: 2326 Auditory & Speech Perception 2346 Attention 3299 Vision & Hearing & Sensory Disorders Keywords: Visual deprivation Early blindness Auditory perception Brain plasticity Attention Compensatory mechanisms
a b s t r a c t Sighted individuals are less accurate and slower to localize sounds coming from the peripheral space than sounds coming from the frontal space. This specific bias in favour of the frontal auditory space seems reduced in early blind individuals, who are particularly better than sighted individuals at localizing sounds coming from the peripheral space. Currently, it is not clear to what extent this bias in the auditory space is a general phenomenon or if it applies only to spatial processing (i.e. sound localization). In our approach we compared the performance of early blind participants with that of sighted subjects during a frequency discrimination task with sounds originating either from frontal or peripheral locations. Results showed that early blind participants discriminated faster than sighted subjects both peripheral and frontal sounds. In addition, sighted subjects were faster at discriminating frontal sounds than peripheral ones, whereas early blind participants showed equal discrimination speed for frontal and peripheral sounds. We conclude that the spatial bias observed in sighted subjects reflects an unbalance in the spatial distribution of auditory attention resources that is induced by visual experience. © 2013 The Authors. Published by Elsevier B.V. All rights reserved.
1. Introduction Does visual experience determine the spatial distribution of attention resources in the auditory modality? We know from animal studies that vision plays a role in calibrating the spatial representation of the auditory sense (Knudsen & Knudsen, 1985, 1989; Withington, Binns, Ingham, & Thornton, 1994). Studies in visually deprived animals also clearly demonstrated how visual experience affects performance in the auditory modality (Rauschecker, 1995). While sighted human and non-human primates localize less accurately (and more slowly) sounds coming from the peripheral space as compared to the frontal one (Oldfield & Parker, 1984; Recanzone & Beckerman, 2004; TederSälejärvi, Hillyard, Röder, & Neville, 1999), such disadvantage for peripheral sounds seems reduced in congenitally blind individuals (Röder et al., 1999; Voss et al., 2004). Visually deprived animals and humans are better than sighted subjects at localizing sounds coming from the peripheral space (Chen, Zhang, & Zhou, 2006; Rauschecker & ☆ This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-No Derivative Works License, which permits noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited. ⁎ Corresponding author at: Avenue Hippocrate, 54, UCL-B1.54.09, 1200 Brussels, Belgium, Tel.: +32 2 764 54 56; fax: +32 2 764 94 22. E-mail address: [email protected] (L. Renier).
Kniepert, 1994; Röder et al., 1999; Voss et al., 2004) and from the back space (Després, Candas, & Dufour, 2005; Voss et al., 2004), whereas equal performance levels are observed for frontal sounds (Després et al., 2005; Röder et al., 1999; Voss et al., 2004; Zwiers, Van Opstal, & Cruysberg, 2001a, 2001b). Interestingly, a similar effect of the auditory experience on the spatial distribution of attention between the central and the peripheral visual fields was reported in studies in early deaf individuals (Bavelier, Dye, & Hauser, 2006; Bavelier et al., 2000; Proksch & Bavelier, 2002). To date, no study has investigated the potential effect of sound source location on non-spatial processing either in sighted or in early blind individuals. General attention mechanisms could mediate this effect of the sound source location on the stimulus processing abilities (e.g. stimulus localization or discrimination). The present study aimed to test the effects of visual experience on auditory discrimination abilities in the frontal and the peripheral space. We hypothesized that sighted participants would be affected by an attention bias that leads them to most efficiently (i.e. more accurately and/or more rapidly) process the sounds originating from frontal locations, whereas early blind participants would have equivalent performance levels across the sound source locations. A secondary goal was to test to what extent blind individuals are better than sighted ones when simultaneously attending to multiple potential sound sources versus only one sound source. Since blind
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individuals need to be more attentive than sighted individuals to multiple auditory stimulations from their surrounding environment, we hypothesized that they would typically perform better than sighted individuals in situations involving multiple stimulation sources than in situations involving a single one. 2. Methods 2.1. Subjects Twelve early and totally blind individuals (EB) and 12 sighted controls (SC), matched for gender (10 men), age (EB: 38 ± 12; SC: 37.5 ± 16) and self-rated musical experience (evaluated on a “5 level” scale that took into account both expertise (how well) and musical practice amount (0: no musical notion, 1: some musical notions associated with an old or current practice of a musical instrument, 2: good musical notions associated with a regular practice of a musical instrument, 3: professional player, 4: absolute pitch, EB: 1.8 ± 1.3, SC: 1.8 ± 1.1)), took part to the experiment. The musical experience was evaluated to test its potential effect on frequency discrimination, since increased tonal processing capabilities in musicians have been reported in the literature (Micheyl, Delhommeau, Perrot, & Oxenham, 2006; Pitt, 1994). The participants were totally blind due to congenital or early (before the age of three) peripheral deficits (see Table 1 for additional details). No participant reported neurological, psychiatric illness or auditory impairment. All participants signed an informed consent. This experiment was approved by the ethics committee of the school of medicine of the Université catholique de Louvain. 2.2. Stimuli and materials Stimuli consisted of three broadband noises of 60 dB of intensity created using “Adobe Audition” and filtered with three different bandpasses: 2500–4500 Hz for the target, 1500–3500 Hz for the distractor 1 and 500–2500 Hz for the distractor 2. The stimuli duration was 100 milliseconds (ms) including 10 ms rise and 10 ms fall. The stimuli were presented via three speakers located on a half-circle placed at a distance of 70 cm from the centre of the head (see Fig. 1(A)). The first speaker was located in front of the participant and corresponded to the frontal location. The second speaker was located at the extreme Table 1 Characteristics of the blind participants. Participants Age Sex Musical experience
Blindness onset
Cause of blindness
EBa 1
26
Mb
4
congenital
EB 2
39
Fc
0
congenital
EB 3
60
M
2
EB 4
35
M
2
infancy (b2 years) congenital
Genetic eye disorder (abnormal retina development) Retinopathy of prematurity Bilateral retinoblastoma
EB 5 EB 6 EB 7 EB 8 EB 9
31 35 48 52 27
M M M M M
2 1 4 1 2
congenital congenital congenital congenital congenital
EB 10 EB 11
55 24
M M
2 0
congenital infancy (b3 years)
EB 12
34
F
1
congenital
Genetic eye disorder (abnormal retina development) Optic Leber neuropathy Optic Leber neuropathy Genetic eye disorder* Bilateral retinoblastoma Genetic eye disorder (abnormal retina development) Retinal degeneration Genetic eye disorder (abnormal retina development) Retinopathy of prematurity
Note: EB: early blind; M: male; F: female; (*) no additional details available.
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left of the participant, corresponding to − 90°azimuth and the third speaker was located at the extreme right of the participant, corresponding to +90° azimuth, both being considered as peripheral locations. We used one speaker per location (i.e. frontal, peripheral right and peripheral left) instead of a set of numerous close speakers for each attended location as used in previous studies (e.g. Röder et al., 1999) since our goal was to evaluate the effect of the speaker location on frequency discrimination and not to determine the ability to finely discriminate between close spatial locations. 2.3. Procedure Participants were instructed to perform an auditory target detection task; they had to press a button as quickly as possible at the target presentation regardless of the speaker it originated from. Three different conditions were administered in a counterbalanced order: two experimental conditions and one control condition. In the first experimental condition, called “wide spatial distribution”, targets and distractors came sequentially and pseudo-randomly from the frontal and the peripheral (right and left) speakers. The participants had to pay attention to the three sound source locations. In the second condition, called “focused spatial distribution”, targets and distractors always came from the same speaker (either from the front, the right or the left) in each sub-condition. In this condition, the speaker location was announced to the participants at the beginning of each sub-condition, so that they could focus on it. For the two experimental conditions, a total of 1650 stimuli were presented with a ratio of 1/3 of targets, 1/3 of distractors 1 and 1/3 of distractors 2. The targets and the distractors were presented sequentially in a pseudo-random order with the only constraint that two targets were never presented consecutively (Fig. 1(B)). Different interstimulus intervals were used (ISIs: 500, 700, 900, 1100, 1300 ms). The control condition consisted in an auditory detection task during which the target appeared pseudo-randomly at one of the three locations. The subjects had to press the button as quickly as possible at the stimulus presentation. No distractor was presented during this condition. In the control condition, one hundred targets appeared pseudo-randomly either from the front, the right or the left speaker. The rest of the procedure in the control condition was identical to the experimental conditions. The entire testing took place in a sound attenuated room. The speakers were positioned at ear level and the head was wedged with a cushion in order to maintain it in the same orientation throughout the experiment. Sighted participants were blindfolded throughout the experiment. Before the experiment, the target and the two distractors were presented to the participants. Then the participants underwent a brief familiarization session (20 trials for each condition). Stimulations and responses recording were controlled using Matlab (Mathworks Inc. Sherborn MA, USA). Participants delivered their responses via a mouse of high temporal accuracy (Razer, model number: RZ01-0015). Breaks of few minutes were introduced every 8 min to reduce any potential decrease of attention. 3. Data analyses For the experimental conditions, we performed two separate 2 (groups: EB vs SC) ×2 (spatial distribution of the stimuli: “wide spatial distribution” vs “focused spatial distribution”) ×2 (sound source locations: front vs periphery) analyses of variance (ANOVAs): on the reaction times (RTs) for the hits (targets correctly detected) and on the target omissions rates. In addition, simple effects were tested on the RTs using Student t-tests. The false alarm (FA) rates were too low (1.2% on average) in all conditions to allow discriminating between conditions and groups and were therefore not further analyzed. We carried out a Pearson correlation analysis in order to test the relation between the musical experience and RTs. The RTs and the target omissions rates of the control condition were evaluated with two separate 2 (EB vs SC) × 2 (front vs periphery) ANOVAs.
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Fig. 1. Experimental setup and procedure (A) Participants seated in a sound attenuated room with the three speakers located at a distance of 70 cm to the center of the subject's head. One speaker was placed in front of the subject (0°) and two speakers were located at 90°azimuth to the left (−90°) and to the right (90°) of the mid-sagittal plane of the participant. The head was wedged with a cushion in order to maintain it in the same orientation throughout the experiment. (B) Example of a time course for the condition “wide spatial distribution” of the stimuli. Targets and distractors came sequentially from the three different speakers and were separated by variable inter-stimuli intervals. Participants had to detect the targets independently to their spatial origin.
4. Results On average the subjects correctly performed the task in all conditions as relatively few omissions (3.3%) and false alarms (1.2%) were recorded. The ANOVA performed on the RTs revealed an effect of the group [F(1,22) = 11.24, p b 0.005], no effect of the target location [F(1,22) = 1.3, p = 0.26] and no effect of the spatial distribution of the stimuli [F(1,22) = 0.53, p = 0.47]. EB participants were faster (mean in milliseconds ± SEM: 307 ± 10) than SC participants (364 ± 13). An interaction between the group and the target location was present [F(1,22) = 8.23, p b 0.01] (see Fig. 2A). Student t-test revealed a difference between the front and the periphery in SC participants only [SC: t(11) = − 3.18, p b 0.01]; sighted participants were faster to detect frontal targets than peripheral ones unlike early blind participants. No other double interaction was observed (all ps N 0.1), but a triple interaction between the group, the spatial distribution of the stimuli and the target location was present [F(1,22) = 5.64, p b 0.05] indicating that the interaction between group and target location was not equivalent in the two spatial distribution conditions. When we decomposed the triple interaction, we observed an interaction between the group and the target location in the “focused spatial distribution” (F(1,22) = 7.58, p b 0.05) and not in the “wide spatial distribution” (F(1,22) = 2.8, p = 0.108). Analyses of the simple effects of the target location within each group and each spatial distribution condition showed a significant effect of the target location in both spatial distribution conditions in SC subjects only (all ps b 0.05 in SC subjects and all ps N 0.1 in EB subjects). Analyses of the simple effects of the group within each target location and each spatial distribution condition revealed a significant effect
of the group in all conditions (all ps b 0.005) except for frontal targets in the “focused spatial distribution” where only a trend was present (p = 0.079). This slightly reduced group difference for the frontal targets in the “focused spatial distribution” as compared to all other conditions probably explains the double interaction between group and target location observed in the “focused spatial distribution” and not in the “wide spatial distribution”, hence explaining the triple interaction. The ANOVA performed on target omission rates revealed a marginal group effect [F(1,22) = 3.46, p = 0.076], a target location effect [F(1,22) = 6, p b 0.05] and a marginal effect of the spatial distribution of the stimuli [F (1,22) = 3.59, p = 0.071]. EB participants tended to make fewer omissions than SC participants (EB: 0.9% ± 0.4, SC: 5.6% ± 2.5). There were fewer omissions for the frontal targets (2% ± 0.9) than for the peripheral ones (4.4% ± 1.7). There was a trend towards fewer omissions for the “focused spatial distribution” (2% ± 0.8) than for the “wide spatial distribution” (4.4% ± 1.8). There was a marginal interaction between the group and the target location [F(1,22) = 3.46, p = 0.076; EB: front: 0.6 ± 1.2, periphery: 1.2 ± 2.4; SC: front: 3.5 ± 1.2, periphery: 7.7 ± 2.4] (see Fig. 2B). No other interaction was significant (all ps N 0.05). The correlation analysis between the RTs and the musical experience level was not significant (r = − 0.26; p = 0.22 in the whole group, r = − 0.459; p = 0.133 in EB participants and r = − 0.255; p = 0.424 in SC participants). For the control condition, the ANOVA performed on the RTs revealed no group effect [F(1,22) = 1.7, p = 0.21; EB = 202 ± 9, SC = 222 ± 12], a target location effect [F(1,22) = 4.5, p b 0.05] and no interaction between the target location and the group [F(1,22) = 0.12, p = 0.74]. The RTs for the frontal targets were shorter than for the
Fig. 2. Performance of early blind subjects and sighted control participants as a function of the spatial location of the targets (frontal speaker vs. peripheral ones) (A) Mean reaction times (RT) in milliseconds (ms) as a function of the group (blind vs sighted) and the target location (front vs periphery). The RTs of the blind participants were shorter than the RTs of the sighted controls (p b 0.005) and there was an interaction between the group and the target source location (p b 0.01). (B) Mean omissions rates (%) as a function of the group (blind vs sighted) and the target location (front vs periphery). There was a marginal group effect (p = 0.076) and an effect of the target source location was present (p b 0.05). A marginal interaction between the group and the target location was also observed (p = 0.076). Error bars are standard errors of the mean (SEM). Results for the “focused spatial distribution” and “wide spatial distribution” were plotted together since there was no effect of the spatial distribution of the stimuli (p N 0.1).
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peripheral ones (Front = 209 ± 7, Periphery = 215 ± 9). The ANOVA performed on target omissions rates revealed no significant effect (all ps N 0.05). 5. Discussion 5.1. Visual experience constrains the spatial distribution of auditory attention The present study is one of the first attempts to investigate the effect of sound source location on non-spatial processing either in sighted or in early blind individuals. Sighted participants discriminated frontal targets faster than peripheral ones while early blind participants performed equally fast for frontal and peripheral targets. This difference between early blind and sighted subjects in the performance profile may depend on a difference in the spatial distribution of attention in the two groups, this difference being supposedly induced by visual experience. A possible explanation to this effect of visual experience on the spatial distribution of attention would be that sighted individuals spontaneously orient their head towards the source of the sounds that may have a potential interest or value for them (e.g. a speaker, television), in order to complement their auditory perception with visual information (e.g. images, lipreading). Consequently, they may develop a greater expertise for processing frontal stimuli more efficiently than peripheral ones. We noticed that some of our blind volunteers do not orient spontaneously their head toward what they are listening to (e.g. the speaker) even if some of them learned to do it when they are speaking to someone. Consequently, early blind individuals would not develop a specific practice-related expertise for more efficiently processing frontal sounds than peripheral ones; they would rather process frontal and peripheral sounds indifferently. It is worth noting that a similar frontal advantage in sighted subjects was previously observed in studies that used localization tasks (Teder-Sälejärvi et al., 1999) while this frontal advantage was reduced in early blind subjects in similar tasks (Després et al., 2005; Röder et al., 1999; Voss et al., 2004). Interestingly, Teder-Sälejärvi and Hillyard (1998) and Teder-Sälejärvi et al. (1999) reported that when the participants explicitly paid attention to a specific part of the surrounding space, the localization performance (i.e. accuracy and speed) improved for this location. This illustrates how inducing a change in the spatial distribution of attention (i.e. orienting it toward a specific location) affects auditory processing abilities across spatial locations. In the visual domain, studies in deafness offer an interesting example of how auditory deprivation influences the spatial distribution of visual attention between the central/foveal and the peripheral visual fields (Bavelier et al., 2000, 2006; Dye, Hauser, & Bavelier, 2009; Proksch & Bavelier, 2002). It is particularly worth noting that in both cases (blindness and deafness), sensory deprivation leads to a relative favouring of the peripheral space as compared to what is observed in sighted or hearing persons. Peripheral vision or peripheral audition is less accurate than central/foveal vision or frontal audition. Sighted and hearing individuals may use the convergence of the two senses, audition and vision, to be efficient in the peripheral space. Without vision or audition to compensate that specific weakness in the peripheral space, sensory deprived individuals would typically improve their peripheral vision or audition. 5.2. Improved auditory discrimination in early blindness The present study showed that early blind participants were faster (and tend to be more accurate) than sighted controls to detect an auditory target among distractor sounds. This group difference was observed for sounds originating both from frontal and peripheral location(s) and in conditions involving both a single and multiple sound source location(s). In accordance with Wan, Wood, Reutens, and Wilson (2010a), the improvement of the sound frequency
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discrimination ability in early blind participants was found independently of musical experience since each individual blind subject was matched for this aspect to a control participant and that performance did not correlate with musical experience. In addition, the improvement observed in early blind participants did not depend on a difference in simple reaction time since no group difference was observed for the RTs in the control condition. This suggests that this compensatory mechanism involves higher level processes such as frequency discrimination and attention. These results are consistent with previous studies that reported supra-normal sound frequency discrimination and categorization abilities in early blind individuals (Gougoux et al., 2004; Hamilton, Pascual-Leone, & Schlaug, 2004; Voss, Lepore, Gougoux, & Zatorre, 2011; Wan et al., 2010a), while they had equal performances for low demand attention tasks (Collignon, Renier, Bruyer, Tranduy, & Veraart, 2006; Kujala, Lehtokoski, Alho, Kekoni, & Risto, 1997; Kujala et al., 2005). In the absence of vision, blind individuals rely only on audition, tact and olfaction and therefore use them more intensively, which would result in the development of improved perceptual abilities (Alary et al., 2009; Beaulieu-Lefebvre, Schneider, Kupers, & Ptito, 2011; Cuevas, Plaza, Rombaux, De Volder, & Renier, 2009; Goldreich & Kanics, 2003; Gougoux et al., 2004; Lessard, Paré, Lepore, & Lassonde, 1998; Lewald, 2013; Norman & Bartholomew, 2011; Pascual-Leone, Amedi, Fregni, & Merabet, 2005; Rauschecker, 1995; Renier, De Volder, & Rauschecker, in press; Wan, Wood, Reutens, & Wilson, 2010b; Wong, Gnanakumaran, & Goldreich, 2011). In the present study, we also tested whether the improvement in early blind individuals was more pronounced in conditions involving multiple sound sources as compared to conditions involving only one source. Contrary to our initial hypothesis, the stimuli spatial distribution (i.e. 1 vs 3 sound source(s)) did not have any particular effect on either the early blind or the sighted control participants, except that both groups tended to make fewer omissions in the “focused spatial distribution” than in the “wide spatial distribution”. We cannot exclude that the difference in difficulty levels between both conditions was insufficient for any effect of this factor to be observed. 5.3. Conclusions The present study indicates that visual experience influences the way we distribute our auditory attention around us. A bias leading to a favouring of the frontal space at the expense of the peripheral one was present in sighted individuals and absent in early blind individuals during auditory discrimination. Acknowledgments We wish to thank Anne G. De Volder, who is a senior research associate at the Belgian National Funds for Scientific Research (FNRS). E. Lerens was supported by the National Fund for Scientific Research (Belgium). L. Renier is a Postdoctoral Researcher supported by the Brussels Institute for Research and Innovation (INNOVIRIS, Belgium). This study was supported by FRSM grant #3.4502.08 (Belgium). References Alary, F., Duquette, M., Goldstein, R., Elaine Chapman, C., Voss, P., La Buissonnière-Ariza, V., et al. (2009). Tactile acuity in the blind: A closer look reveals superiority over the sighted in some but not all cutaneous tasks. Neuropsychologia, 47(10), 2037–2043. Bavelier, D., Dye, M. W. G., & Hauser, P. C. (2006). Do deaf individuals see better? Trends in Cognitive Sciences, 10, 512–518. Bavelier, D., Tomann, A., Hutton, C., Mitchell, T., Corina, D., Liu, G., et al. (2000). Visual attention to the periphery is enhanced in congenitally deaf individuals. Journal of Neuroscience, 20, 1–6. Beaulieu-Lefebvre, M., Schneider, F. C., Kupers, R., & Ptito, M. (2011). Odor perception and odor awareness in congenital blindness. Brain Research Bulletin, 84(3), 206–209. Chen, Q., Zhang, M., & Zhou, X. (2006). Spatial and nonspatial peripheral auditory processing in congenitally blind people. NeuroReport, 17, 1449–1452.
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