Neuropsychologia 48 (2010) 344–348

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Early but not late-blindness leads to enhanced auditory perception Catherine Y. Wan a,b,∗ , Amanda G. Wood b,c , David C. Reutens b,d , Sarah J. Wilson a a

School of Behavioral Science, The University of Melbourne, Victoria 3010, Australia Department of Medicine, Southern Clinical School, Monash University, Victoria 3800, Australia c Murdoch Childrens Research Institute, Parkville, Victoria 3052, Australia d Centre for Advanced Imaging, University of Queensland, Queensland 4072, Australia b

a r t i c l e

i n f o

Article history: Received 27 November 2008 Received in revised form 10 August 2009 Accepted 13 August 2009 Available online 22 August 2009 Keywords: Blind Auditory perception Brain plasticity Onset age

a b s t r a c t The notion that blindness leads to superior non-visual abilities has been postulated for centuries. Compared to sighted individuals, blind individuals show different patterns of brain activation when performing auditory tasks. To date, no study has controlled for musical experience, which is known to influence auditory skills. The present study tested 33 blind (11 congenital, 11 early-blind, 11 late-blind) participants and 33 matched sighted controls. We showed that the performance of blind participants was better than that of sighted participants on a range of auditory perception tasks, even when musical experience was controlled for. This advantage was observed only for individuals who became blind early in life, and was even more pronounced for individuals who were blind from birth. Years of blindness did not predict task performance. Here, we provide compelling evidence that superior auditory abilities in blind individuals are not explained by musical experience alone. These results have implications for the development of sensory substitution devices, particularly for late-blind individuals. © 2009 Elsevier Ltd. All rights reserved.

1. Introduction Humans have a remarkable capacity to adapt to changes in environmental input, such as those associated with sensory deprivation. In the absence of visual input, blind individuals rely on sensory information from audition and touch to assist their navigation in environments that are generally designed for the sighted. It is not surprising, then, that blind individuals perform better than sighted individuals on attentional and spatial localization tasks (Lessard, Pare, Lepore, & Lassonde, 1998; Roder, Rosler, & Neville, 1999). Other research has demonstrated that blind individuals have superior speech perception (Hugdahl et al., 2004; Muchnik, Efrati, Nemeth, Malin, & Hildesheimer, 1991; Niemeyer & Starlinger, 1981) and verbal memory abilities (Amedi, Raz, Pianka, Malach, & Zohary, 2003; Roder & Rosler, 2003). Even short-term visual deprivation of sighted individuals may lead to enhanced sound localization (Lewald, 2007) and pitch discrimination abilities (Gibby, Gibby, & Townsend, 1970). The timing of blindness onset during development may determine the degree of sensory enhancement in the non-visual modalities (Neville & Bavelier, 2002). In the auditory domain, some studies indicate that early-blind individuals display superior per-

∗ Corresponding author at: Department of Neurology, Beth Israel Deaconess Medical Center and Harvard Medical School, 330 Brookline Avenue, Boston, MA 02215, United States. E-mail address: [email protected] (C.Y. Wan). 0028-3932/$ – see front matter © 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2009.08.016

formance compared to late-blind individuals (Gougoux et al., 2004; Voss, Gougoux, Zatorre, Lassonde, & Lepore, 2008), while others report these groups have similar abilities (Voss et al., 2004). Previous studies have tended to use different age ranges, with the lower limit for late-onset blindness varying from 5 years (Gougoux et al., 2004) to 18 years (Voss, Gougoux, Lassonde, Zatorre, & Lepore, 2006). With few exceptions (e.g., Kujala, Alho, et al., 1997), neuroimaging evidence suggests that individuals with early- and late-onset blindness show different degrees of cross-modal (occipital) activation during non-visual task processing (Buchel, Price, Frackowiak, & Friston, 1998; Burton, Diamond, & McDermott, 2003; Burton, Sinclair, & McLaren, 2004; Burton, Snyder, Diamond, & Raichle, 2002; Fieger, Roder, Teder-Salejarvi, Hillyard, & Neville, 2006). In particular, it has been suggested that 14–16 years represents an important cut-off (Cohen et al., 1999; Sadato, Okada, Honda, & Yonekura, 2002). Individuals deprived of any visual input from birth may be most susceptible to changes in brain function induced by blindness. However, previous studies have not compared individuals with no visual experience (congenitally blind) with those becoming blind after visual experience early in life (early-blind). A number of studies have investigated the ability of blind individuals to discriminate simple auditory stimuli. Early studies reported mixed findings (e.g., Sakurabayashi, Sato, & Uehara, 1956; Starlinger & Niemeyer, 1981), however, more recent research has supported superior pitch discrimination in blind individuals (Gougoux et al., 2004). None of these studies has attempted to control for differences in musical experience between blind and sighted

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Table 1 Demographic characteristics and musical ability of the blind participants (see text for details). Age at test

Years blind

Gender

Years musical training

Musical training category

31 22 63 36 26 26 33 21 55 19 35 33 (14)

31 22 63 36 26 26 33 21 55 19 35 33 (14)

M M M F F F M F F M F

12 16 18 2 18 7 6 16 0 10 20

4 5 5 2 5 3 3 5 1 4 5

11 5 1.4 1.5 13 12 8 9 13 12 1.5 7.9 (4.8)

52 40 48 36 53 38 25 48 48 43 35 42 (9)

41 35 47 35 40 26 17 39 35 31 34 34 (8)

M F F F M M M M M F M

5 4 6 2 7 2 16 6 0 4 0

3 3 3 2 3 2 5 3 1 3 1

14.5 24 20 54 27 33 33 25 18.5 31 17.5 27.0 (10.9)

44 39 48 59 54 46 50 50 38 40 42 46 (7)

29 15 28 5 27 13 17 25 20 9 25 19 (8)

M F F M M F F F F F M

5 1 12 0 2 1 6 7 2 2 10

3 2 4 1 2 2 3 3 2 2 4

ID

Cause of blindness

Age of blindness onset (years)

Con 1 Con 2 Con 3 Con 4 Con 5 Con 6 Con 7 Con 8 Con 9 Con 10 Con 11 Mean (SD)

Retinopathy of prematurity Retinopathy of prematurity Congenital cataracts Malformed eyes Retinopathy of prematurity Congenital detached retina Congenital cataracts Retinopathy of prematurity Retinopathy of prematurity Retinopathy of prematurity Retinoblastoma

0 0.3 0.3 0 0.2 0 0 0.2 0.2 0 0.2 0.1 (0.1)

Early 1 Early 2 Early 3 Early 4 Early 5 Early 6 Early 7 Early 8 Early 9 Early 10 Early 11 Mean (SD)

Retinitis pigmentosa Retinoblastoma Detached retina Retinoblastoma Retinitis pigmentosa Congenital glaucoma Detached retina Detached retina Detached retina Retinitis pigmentosa Retinopathy of prematurity

Late 1 Late 2 Late 3 Late 4 Late 5 Late 6 Late 7 Late 8 Late 9 Late 10 Late 11 Mean (SD)

Detached retina Cataracts Retinitis pigmentosa Impact injury Impact injury Retinitis pigmentosa Retinopathy of prematurity Retinopathy of prematurity Retinitis pigmentosa Detached retina Glaucoma

participants, which is a key variable in auditory research (e.g., Gaab & Schlaug, 2003; Pitt, 1994). Enhanced auditory abilities may be due to greater musical experience, rather than to differences related to vision loss per se. For example, the prevalence of absolute pitch may be higher in blind individuals (Hamilton, Pascual-Leone, & Schlaug, 2004) and blind musicians with absolute pitch may show different brain activation patterns compared to sighted musicians with absolute pitch (Gaab, Schulze, Ozdemir, & Schlaug, 2006; Ross, Olson, & Gore, 2003). The aim of the present study was to compare auditory perception skills in blind and sighted individuals, while controlling for factors that might influence these abilities. To ascertain whether visual deprivation (rather than practice) is primarily responsible for any observed differences, we systematically matched each blind participant with a sighted control on variables such as musical training and pitch naming ability (absolute pitch). We also directly compared individuals blinded at three phases in development (congenital, early-onset, late-onset) to investigate the developmental time frame for superior non-visual abilities following visual loss. 2. Methods 2.1. Participants This study was approved by the Human Research Ethics Committee at The University of Melbourne. A total of 33 blind and 33 sighted participants took part in the study (N = 66). The blind participants were recruited from community organizations. In all, blindness was caused by peripheral defects. When tested, participants had minimal (or no) light sensitivity, no pattern vision, no significant hearing loss (as assessed by an audiogram) and were free of neurological deficits. All participants were classified into one of three blindness groups: congenital, early-, and late-onset, depending on the age at which complete vision loss began (see Table 1). The con-

Current musical engagement

Presence of AP

Yes Yes

Yes

Yes

Yes

Yes

Yes Yes

Yes Yes

Yes

Yes

Yes

genital group comprised 11 individuals (aged 19–63 years) who were born blind or became blind soon after birth. The early-blind group comprised 11 individuals (aged 25–53 years) who became completely blind between the ages of 1.4 and 13 years. In light of the neuroimaging data from Cohen et al. (1999), we defined late-blindness as 14+ years of age. Thus, the late-blind group included 11 individuals (aged 38–59 years) who became completely blind between 14.5 and 54 years. For each blind participant, we recruited a sighted control matched for age, gender, nature and extent of musical training, current musical activity, and the presence of absolute pitch. Age was matched within a range of 5 years. There were no significant differences in age between blind and sighted participants across the three groups (p > 0.39). Musical training was recorded in terms of number of years. To simplify matching, we classified each participant into one of five training categories: (i) no training, (ii) a few months to less than 3 years, (iii) 4–8 years, (iv) 9–15 years and (v) over 15 years of training (see Table 1). Participants with extensive musical training (more than 15 years) had all received training before the age of 10 years. To test for absolute pitch, a 50-item pitch naming task was administered to each participant (Wilson, Lusher, Wan, Dudgeon, & Reutens, 2009). 2.2. Procedure Our study comprised three tasks that assessed different aspects of auditory processing: pitch discrimination, pitch-timbre categorization, and pitch working memory. All participants were blindfolded during testing. For all tasks, participants were given a practice session prior to testing. Response accuracy was emphasized over response speed. 2.2.1. Pitch discrimination The pitch discrimination task was based on the method of Bonnel et al. (2003). Stimuli were pairs of pure tones. Each trial comprised two 100 ms tones, which were presented consecutively, with an inter-tone interval of 300 ms and an attack and decay rate of 10 ms for each tone. One tone was the “standard” frequency (500, 750, 1000 or 1500 Hz), and the other “comparison” frequency was either 2%, 1%, 0.5%, or 0.25% higher than the standard. Each of the four difficulty levels was tested in 40 repetitions, resulting in a total of 160 trials. Participants were required to respond with a key press to indicate whether the second tone was higher or lower in pitch than the first tone.

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2.2.2. Pitch-timbre categorization This task was adapted from an experiment by Pitt (1994). Instead of using recordings of musical instruments, we digitally synthesized timbre to minimize the effects of familiarity among the musically trained participants. Stimuli consisted of four tones, with two levels of pitch and two levels of timbre. The two levels of pitch were a low tone (D4, 294 Hz) and a high tone (G#4, 417 Hz). Tones lasted 250 ms and were separated by an interval of 1500 ms. Timbre was varied by manipulating the harmonic components of the tones (Starr & Pitt, 1997). Each timbre comprised three consecutive harmonics of equal amplitude, and the fundamental frequency (f1), or the lowest perceived frequency component in the tone that designates the pitch of the tone. The two timbres differed in the distance between the fundamental frequency and frequency location of the three contiguous harmonics (timbre 1 = f1 + f3 + f4 + f5; timbre 2 = f1 + f4 + f5 + f6). Timbre 2 was perceived to sound sharper or brighter than timbre 1. Each trial consisted of two tones, and participants were instructed to make judgments on both pitch and timbre, by classifying the tones into one of four conditions: no change, pitch change, instrument change, and both change. There were 32 trials in each condition, resulting in a total of 128 trials. 2.2.3. Pitch memory The pitch working memory task was similar to that used by Gaab, Gaser, Zaehle, Jancke, and Schlaug (2003). Stimuli were sequences of either 6 or 12 pure tones. The sequence comprised the first (target) and the last (probe) tones, separated by distractor tones. Each tone lasted 300 ms, with an attack and decay rate of 50 ms. The interval between tones was 300 ms. All tones were within the frequency range of 300 Hz (E4) to 622 Hz (D#5). The frequency difference between the first (target) and the last (probe) tone was between 41 and 64 Hz. The frequency range from the lowest to the highest tone in all tone sequences was not more than 110 Hz. The differences between the distractor tones and the target/probe tones ranged from 2.8 to 76.3 Hz. Participants were required to listen to the tones and determine whether the last and first tones were the same. Responses were by button press. There were 36 trials in each condition, resulting in a total of 72 trials.

3. Results For all tasks, the primary dependent variable was proportion correct. We applied the standard logit transformation, log(p/(1 − p)), to these proportions to put them on a suitable scale for statistical analysis (Fox, 1997). For each of the three tasks (pitch discrimination, pitch-timbre categorization, and pitch memory) we asked; is there an advantage of the blind over the sighted and if so, does it vary for the three onset groups (congenital, early, and late) and across difficulty levels?

Fig. 1. (a) Mean performance accuracy (% correct) in the pitch discrimination task for blind and sighted participants in three groups (congenital, early-onset, and lateonset). Error bars indicate standard errors of the means. (b) Mean performance accuracy (% correct) in the pitch-timbre task for blind and sighted participants in three groups (congenital, early-onset, and late-onset). Error bars indicate standard errors of the means.

3.1. Blind and sighted differences across onset age groups 3.1.1. Pitch discrimination A mixed 3 group × (2 vision × 4 difficulty) analysis was performed, with repeated measures on vision and difficulty. The between-subjects factor of group refers to the congenital, early-, and late-onset classifications. Vision refers to the absence (blind) or presence (sighted) of vision. Due to the matching between blind and sighted participants, vision was treated as a within-blocks factor (Howell, 2002). Finally, the factor of difficulty covers the four levels of frequency difference between the two tones (2%, 1%, 0.5%, and 0.25%). We first examined performance averaged across difficulty levels (see Fig. 1a). Within each group, we investigated whether the blind were better than the sighted. For both the congenital and early-onset groups, blind participants outperformed their sighted controls (F1,10 = 19.932, p = 0.001; 2p = 0.666; F1,10 = 6.287, p = 0.031, 2p = 0.386, respectively). The difference between blind and sighted participants in the late-onset group was not significant (F1,10 = 1.298, p = 0.281). Accuracy across all difficulty levels is shown in the top half of Fig. 2. There was a significant three-way interaction involving group, vision, and difficulty (F6,56 = 4.282, p = 0.001, 2p = 0.315), indicating that the difference in performance between blind and sighted participants across difficulty levels depends on blindness onset age. Within the congenital and early-onset groups, we examined whether vision had an impact on performance accuracy at

Fig. 2. Mean and standard errors of percentage correct in the (a) pitch discrimination task, and (b) pitch-timbre categorization task. Error bars indicate standard errors of the means.

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specific levels of difficulty. In the congenital group, the blind participants significantly outperformed their sighted controls at the 2%, 1%, and 0.5% difficulty levels (F1,10 = 12.658, p = 0.005, 2p = 0.559; F1,10 = 23.949, p = 0.001, 2p = 0.705; F1,10 = 20.137, p = 0.001, 2p = 0.668, respectively). There was no difference at the 0.25% difficulty level (F1,10 = 1.375, p = 0.268). In the early-onset group, the difference between blind and sighted individuals was significant only at the 2% difficulty level (F1,10 = 8.879, p = 0.014, 2p = 0.47). 3.1.2. Pitch-timbre categorization A mixed 3 group × (2 vision × 4 condition) analysis was performed. We first examined performance averaged across the four conditions (no change, pitch change, timbre change, both change). As illustrated in Fig. 1b, there was a significant interaction between vision and group (F2,30 = 8.489, p = 0.001, 2p = 0.361). To explore this interaction, simple effects tests were carried out to examine the impact of vision on performance accuracy within each group. For both the congenital and early-onset groups, blind participants outperformed their sighted controls (F1,10 = 19.138, p = 0.001, 2p = 0.657; F1,10 = 9.355, p = 0.012, 2p = 0.483, respectively). However, no significant difference in performance between blind and sighted participants was found for the late-onset group (F1,10 = 1.976, p = 0.19). There was a significant three-way interaction between vision, group, and condition (F6,56 = 3.078, p = 0.011). Accuracy in all conditions is shown in the bottom half of Fig. 2. To examine whether vision (absence or presence) had an impact on performance accuracy for each of the four conditions, simple effects tests were carried out for the congenital and early-onset groups. There was a significant difference between the blind and sighted participants in both the congenital and early-onset groups, for the following stimulus conditions: ‘pitch change’ (F1,10 = 15.926, p = 0.003, 2p = 0.614; F1,10 = 5.483, p = 0.041, 2p = 0.354, respectively), ‘timbre change’ (F1,10 = 5.213, p < 0.046, 2p = 0.343; F1,10 = 6.525, p = 0.029, 2p = 0.395, respectively), and ‘both change’ (F1,10 = 22.309, p = 0.001, 2p = 0.69; F1,10 = 9.410, p = 0.012, 2p = 0.485). These findings indicate that both the congenital and early-onset participants were better at perceiving changes in pitch and timbre compared to their sighted counterparts. 3.1.3. Pitch working memory A 3 group × (2 vision × 2 difficulty) ANOVA revealed only a significant main effect of group (F2,30 = 3.989, p = 0.001, 2p = 0.391). The participants (blind and sighted) in the congenital group were more accurate overall than those in the early-onset and late-onset groups. This difference may reflect the greater number of musically trained participants in the congenital group. Neither the main effect of vision nor the interaction between vision and group was significant (F1,30 = 2.673, p = 0.113; F2,30 = 2.385, p = 0.109, respectively). 3.2. Effects of years of blindness on performance The relationship between years of blindness and performance was investigated for the blind participants using correlational analyses. No significant correlations were found for any of the three tasks: pitch discrimination (r = 0.195, n = 33, p > 0.2), pitch memory (r = 0.007, n = 33, p > 0.9), and pitch-timbre categorization (r = 0.12, n = 33, p > 0.5). 4. Discussion Our data support the notion that becoming blind early in life enhances auditory acuity. Blind participants who had functional vision until late childhood (≥14 years) performed no better than their sighted counterparts. This pattern was replicated across tasks

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and conditions. Our findings are consistent with those of neuroimaging studies which show different patterns of brain activation in early-blind compared to late-blind individuals (Cohen et al., 1999; Sadato et al., 2002). This is the first study to test the performance of congenitally blind and early-blind individuals as separate groups. In the pitch discrimination task, individuals with congenital blindness were more sensitive relative to their matched controls in discriminating frequency differences, than those with early-onset blindness compared to their matched controls. The congenitally blind group outperformed their sighted controls when the frequency difference between two tones was as small as 1% or 0.5%. This superior performance suggests that having minimal (or no) visual experience at birth confers an even greater advantage for detection of pitch differences. Our results suggest that visual deprivation early in life does not necessarily lead to superior performance for all auditory tasks. In contrast to the pitch discrimination and pitch-timbre categorization tasks, the pitch working memory task did not reveal any significant differences between the blind and sighted participants. One interpretation is that enhancement of auditory acuity relating to pitch stimuli in the blind may be restricted to basic perceptual skills rather than higher level processes, such as working memory. At first glance, this appears to be inconsistent with the findings of previous studies, such as those showing that blind individuals have superior sound localization (Lessard et al., 1998), bimodal divided attention (Collignon, Renier, Bruyer, Tranduy, & Veraart, 2006; Kujala, Lehtokoski, Alho, Kekoni, & Naeaetaenen, 1997), auditory attention (Liotti, Ryder, & Woldorff, 1998), environmental sound detection (Roder & Rosler, 2003), voice recognition (Bull, Rathborn, & Clifford, 1983), or verbal memory (Roder, Rosler, & Neville, 2001; Amedi et al., 2003). However, it is possible that the advantage in those tasks previously observed in blind individuals may be due to their greater dependence on auditory spatial cues in everyday life (Loomis, Golledge, & Klatzky, 1998), in order to successfully navigate in the environment (i.e., practice effects). Similarly, their advantage in verbal linguistic tasks may be attributed to their greater reliance on speech stimuli, such as aurally presented reading material (through audio books and the internet) (Kaye, 2000; Petrucci, Harh, Roth, Assimacopoulos, & Pun, 2000). One of the strengths of the present study was the matching of blind and sighted participants on variables such as age, gender, musical experience, and pitch naming ability (absolute pitch). Previous studies have not controlled for musical experience and pitch naming ability, leaving open the possibility that the superior localization, detection, and discrimination abilities reflect general musical skills. Careful matching for factors related to musical experience allowed us to conclude that the enhanced perceptual abilities found in the congenital and early-blind groups are likely to be due to vision loss. The observed behavioral differences reported here could be due to underlying changes in the brain as a result of long-term visual deprivation. In neuroimaging studies, blind individuals show activation of the occipital regions when they perform sound localization (Weeks et al., 2000) and verbal memory tasks (Amedi et al., 2003). There is also evidence for intramodal plastic changes in the brain. For example, Elbert et al. (2002) found a larger tonotopic map in the auditory cortex of blind compared to sighted individuals. Stevens and Weaver (2009) also reported functional plasticity in auditory cortical areas in the early-blind. Equally plausible is that intramodal plasticity may underlie the superior auditory abilities of the blind individuals observed in the present study. Finally, the present research demonstrated an effect of blindness onset on auditory performance. The development of rehabilitation strategies such as sensory substitution devices (e.g., Meijer, 1992) should take this effect into account. Individuals with late-onset blindness may

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