Neuropsychologia 48 (2010) 631–635

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Congenital blindness leads to enhanced vibrotactile 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 17 February 2009 Received in revised form 25 September 2009 Accepted 1 October 2009 Available online 9 October 2009 Keywords: Blind Plasticity Tactile perception Onset age

a b s t r a c t Previous studies have shown that in comparison with the sighted, blind individuals display superior nonvisual perceptual abilities and differ in brain organisation. In this study, we investigated the performance of blind and sighted participants on a vibrotactile discrimination task. Thirty-three blind participants were classified into one of three groups (congenital, early, late), depending on the age at which they became blind. Consistent with previous neuroimaging data, individuals blinded after late childhood (14 years) showed no advantage over sighted participants. Both the congenitally- and early-blind participants were better than the sighted. The congenitally blind participants were even more accurate than the early-blind participants; a distinction that has not been drawn previously. Duration of blindness did not predict task performance and the effect of onset age persisted after duration of daily Braille reading was accounted for. We conclude that complete visual deprivation early in life leads to heightened tactile acuity. © 2009 Elsevier Ltd. All rights reserved.

1. Introduction Deprived of any visual input, blind individuals are forced to rely on other sensory modalities, such as audition and touch. This increased reliance has been linked to superior perceptual abilities in these modalities in blind relative to sighted individuals (Goldreich & Kanics, 2003; Gougoux et al., 2004). Different patterns of brain activation have also been observed in blind individuals during audition and tactile tasks, likely underlying the superior performance of the blind (Sadato et al., 1996; Weeks et al., 2000). Similarly, blindfolding sighted individuals for a period of five-days has been shown to lead to changes in the occipital cortex (e.g., Merabet et al., 2008). The assessment of tactile perception skills in blind individuals has posed several challenges. Most studies have used Braille or Braille-like dots (Sadato et al., 1996), which require participants to actively scan the stimuli with their fingers. One limitation of these tasks is that blind and sighted individuals may employ different motor strategies to make sense of the material. It is also challenging to match blind and sighted participants on Braille reading experience as sighted Braille instructors typically learn to read Braille visually, rather than by touch (Pascual-Leone, Theoret, Merabet, Kauffman, & Schlaug, 2006).

∗ Corresponding author. E-mail address: [email protected] (S.J. Wilson). 0028-3932/$ – see front matter © 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2009.10.001

To address confounds associated with Braille reading experience, recent studies have used a grating orientation task to assess tactile abilities. For example, Van Boven, Hamilton, Kauffman, Keenan, and Pascual-Leone (2000) reported that grating orientation thresholds were lower in blind compared to sighted participants. Similarly, Goldreich and Kanics (2006) found that blind participants were able to perceive thinner grooves compared to their sighted participants. The perception of grating or dot patterns, however, requires judgements about the spatial properties of the stimuli, which may be superior in the blind due to Braille reading experience. As an alternative, vibrotactile discrimination tasks may allow blind and sighted participants to have similar levels of experience as they do not require spatial discrimination judgments. Despite their advantage, vibrotactile tasks have not been commonly used and performance differences associated with varying levels of task difficulty remain unexplored. Burton, Sinclair, and McLaren (2004) tested blind and sighted participants on a task that was intended to yield near-perfect discrimination (25 Hz vs 100 Hz). Most of the participants performed at ceiling levels demonstrating that the task could be adequately performed by both blind and sighted individuals. Further investigation of vibrotactile discrimination is warranted in blind and sighted individuals using a greater range of task difficulty levels. The timing of blindness onset during development may determine the degree of sensory enhancement in the non-visual modalities (Neville & Bavelier, 2002). Neuroimaging studies of Braille reading show that individuals blinded after 14–16 years

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show no evidence of cross-modal (occipital) activation compared to those blinded earlier (Cohen et al., 1999; Sadato, Okada, Honda, & Yonekura, 2002). Contrasting with this, however, there is evidence implicating the role of the occipital cortex in non-visual processing even among sighted individuals. After being blindfolded for five consecutive days, TMS over the occipital cortex of sighted participants disrupted Braille character recognition (Merabet et al., 2008). Very few behavioural studies have directly examined the timing of blindness onset, and the results have been mixed. For example, Grant, Thiagarajah, and Sathian (2000) failed to find any effects of blindness onset age on the discrimination of dot patterns and gratings. Similar stimuli were used in a study by Stilla et al. (2008), who also reported no performance differences between early- and late-blind individuals. However, this study may have been underpowered due to the relatively small sample size (n = 5) of the groups. In contrast, Heller (1989) reported that late-blind individuals were better than congenitally blind or sighted individuals at tactile picture identification, whereas congenitally blind individuals were superior at making tactile temporal order judgments (Röder, Rösler, & Spence, 2004). Unlike previous studies, the task used by Röder et al. did not require spatial discrimination judgements and thus, was less likely to be affected by differences in practice associated with Braille reading. The aim of the present study was to assess tactile acuity in blind and sighted individuals on an unfamiliar vibrotactile task. We also compared performance in individuals blinded at three phases of development (congenital, early-onset, late-onset) to assess whether vision during childhood influences vibrotactile perception in blind adults.

2. Method 2.1. Participants A total of 33 blind participants participated in the study. Depending on the onset age of complete vision loss, participants were classified into one of three blindness groups: congenital-, early-, and late-onset, with 11 participants in each group. The congenitally blind participants (aged 19–63 years) were born blind or became blind soon after birth (see Table 1 for onset details). The early-blind participants (aged 25–53 years) became completely blind between the ages of 1.4–13 years. Based on the neuroimaging study by Cohen et al. (1999), we defined late-blind individuals as those who became completely blind after 14 years of age. Thus, our late-blind participants (aged 38–59 years) became completely blind between 14.5 and 54 years. Table 1 also presents the demographic characteristics and Braille reading history of the blind participants. At the time of testing, all blind participants had no pattern vision, minimal (or no) sensitivity to light, and no history of neurological disorders other than blindness. Although all of the blind participants were Braille literate, some of them relied mostly on aurally presented material through audio books and the internet (i.e., some did not read Braille daily). For each blind participant, there was an age and gender matched sighted control. 2.2. Vibrotactile device and procedures Stimuli were suprathreshold sinusoidal vibration frequencies between 20 and 100 Hz. Peak-to-peak vibration amplitudes ranged from 0.41 mm for 100 Hz to 0.9 mm for 20 Hz and exceeded standard detection thresholds (Summers et al., 1997). Vibrotactile stimuli were produced by a vibration device that consisted of a control unit connected to two plastic response boxes (one for each hand) with three tactors mounted on each top. There was also a side mounted response button fitted to each box. Each tactor was made of a 1.5 cm diameter distensible latex rubber diaphragm. For each hand, the thumb was placed on the response button, while the index, third, and fourth fingers were placed on each rubber diaphragm. The control unit interfaced with a computer and powered six solenoids which determined the rate of vibration of the tactors. These solenoid coils activated six lightweight neodymium iron boron magnets situated under the rubber diaphragms.

Table 1 Demographic, medical, and Braille reading characteristics of the blind participants. Participant

Cause of blindness

Con 1 Con 2 Con 3 Con 4 Con 5 Con 6 Con 7 Con 8 Con 9 Con 10 Con 11

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

Early 1 Early 2 Early 3 Early 4 Early 5 Early 6 Early 7 Early 8 Early 9 Early 10 Early 11 Late 1 Late 2 Late 3 Late 4 Late 5 Late 6 Late 7 Late 8 Late 9 Late 10 Late 11

Age of blindness onset (years)a

Age at testing (years)

Gender

Years reading Braille

Daily Braille reading (hours)

0 0.3 0.3 0 0.2 0 0 0.2 0.2 0 0.2

31 22 63 36 26 26 33 21 55 19 35

M M M F F F M F F M F

25 16 57 30 20 20 27 15 49 13 29

4+ 2–3 2–3 1–2 3–4 0–1 1–2 1–2 1–2 0–1 1–2

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

11 5 1.4 1.5 13 12 8 9 13 12 1.5

52 40 48 36 53 38 25 48 48 43 35

M F F F M M M M M F M

46 34 42 30 47 25 17 39 34 30 29

2–3 2–3 1–2 1–2 3–4 0–1 0–1 2–3 2–3 0–1 1–2

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

14.5 24 20 54 27 33 33 25 18.5 31 17.5

44 39 48 59 54 46 50 50 38 40 42

M F F M M F F F F F M

29 32 34 33 10 13 40 33 22 20 28

0–1 4+ 0–1 0–1 0–1 0–1 1–2 1–2 0–1 0–1 0–1

Con = congenitally blind; Early = early-blind; Late = late-blind. a The exact time of complete blindness for some of the ROP participants was not known, as their parents were only informed of the extent of vision loss when the participants were discharged from hospital. Thus, the blindness onset age reported for individuals with ROP reflects the age at discharge, rather than the exact time of blindness.

C.Y. Wan et al. / Neuropsychologia 48 (2010) 631–635 A desktop PC ran an in-house DOS program, controlling the delivery of vibratory stimuli. The vibration device produced identical, repeatable, and precise vibration frequencies across the six diaphragm tactors, and the precision of the stimuli was confirmed using an oscilloscope. To mask potential auditory cues generated by the vibration device, pink noise of approximately 60 dB was delivered through speakers during the session. Participants also wore earplugs and sound-attenuating earmuffs to minimise auditory interference. None of the participants had experience with vibrotactile discrimination prior to the study. All participants (blind or sighted) were blindfolded. This was to ensure the blind participants (especially those with minimal light perception) were subjected to the same experimental conditions as the sighted participants. A practice session was given to familiarize the participants with the equipment and the task. Participants were required to discriminate between two consecutively presented vibrotactile frequencies (two-interval forced choice), each lasting 750 ms and separated by an interval of 300 ms. The same frequency was delivered simultaneously to each response box to control for variability in hand preference. We used four standard frequencies (20, 40, 63, 100 Hz) and for each frequency level, there was an easy (20 Hz vs 40 Hz, 40 Hz vs 63 Hz, 63 Hz vs 83 Hz, 100 Hz vs 83 Hz) and a difficult (20 Hz vs 25 Hz, 40 Hz vs 45 Hz, 63 Hz vs 67 Hz, 100 Hz vs 90 Hz) comparison condition. There were 20 trials of each comparison, resulting in a total of 160 trials that were presented in two separate blocks of 80 trials each. For both conditions, participants were required to indicate via a button response whether the second frequency was faster or slower than the first one. Response accuracy was emphasized over response speed.

3. Results The primary dependent variable was percentage correct. A logit transformation, log(p/(1 − p)), was applied to these percentages to put them on a suitable scale for statistical analyses (Fox, 1997). A mixed 3 group × (2 vision × 2 difficulty) analysis of variance 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 of blind and sighted participants, vision was treated as a within-blocks factor (Howell, 2002). There were significant main effects of blindness (F1,60 = 26.235, p < 0.001) and group (F2,60 = 6.246, p = 0.003). There was also a significant main effect of difficulty (F1,60 = 76.255, p < 0.001), with more accurate performance on the easy compared to the difficult condition. The interaction between vision and group was significant (F1,30 = 5.521, p = 0.009). To explore the nature of this interaction, we examined whether vision had an impact on performance accuracy within each group. For both the congenital and early-onset groups, blind participants outperformed their sighted controls (F1,10 = 14.613, p = 0.003; F1,10 = 14.452, p = 0.003 respectively). In contrast, the difference between blind and sighted participants in the late-onset group was not significant (F1,10 = 2.176, p > 0.1). As expected, within the sighted cohort there were no differences in performance between participants assigned to the three groups (F2,30 = 0.065, p > 0.9). For the blind participants, significant group differences were observed (F2,30 = 7.26, p = 0.003). Post

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hoc comparisons revealed that the congenitally blind participants (estimated marginal mean M = 84.55, std = 2.96) were significantly better (p = 0.025) than early-blind participants (M = 75, std = 2.081) at vibrotactile discrimination, whereas there was no difference (p = 0.437) between early- and late-blind participants (M = 71.82, std = 3.08). As illustrated in Fig. 1, our results indicate that both the congenitally and early-blind participants significantly outperformed their sighted controls, and within the blind cohort the performance of the congenitally blind was better than the earlyblind participants. This suggests that having minimal (or no) visual experience at birth confers an even greater advantage on vibrotactile discrimination. Within the blind cohort, Pearson correlational analyses were used to examine the relationships between task performance and years of blindness, years of Braille reading, and hours spent reading Braille each day. There was a significant positive relationship between daily Braille reading and performance (r = 0.432, p = 0.012), indicating that active engagement with Braille was associated with enhanced vibrotactile discrimination ability. No significant correlations were found between years of blindness (r = 0.127) or years of Braille reading (r = −0.081) and task performance. To determine whether performance differences across the blindness groups remained after accounting for the effects of daily Braille reading, we performed a between groups analysis of covariance for the blind cohort. The independent variable was group (congenital, early-, and late-onset), and the dependent variable was mean performance accuracy. The number of hours of Braille reading per day was used as the covariate in the analysis (F1,29 = 4.641, p = 0.04). This showed a significant effect of group on performance accuracy (F2,29 = 5.805, p = 0.008), with estimated marginal means indicating that the performance of the congenitally blind (M = 83.712, std = 2.695) was superior (p = 0.008) to the earlyblind (M = 74.479, std = 2.681), but the early-blind did not differ (p = 0.976) from the late-blind participants (M = 73.172, std = 2.735). A chi-squared analysis showed no significant relationship between group membership and daily Braille reading hours when individuals were classified according to more or less than two hours of daily Braille reading (2 = 3.73; p = 0.155, phi = 0.336). 4. Discussion This study compared the performance of congenital, early-, and late-blind individuals on a vibrotactile task. Both the congenital and early blind participants were better at vibrotactile discrimination than the sighted participants. We also found that congenitally blind participants performed even better than early-blind participants. In contrast, late-blind participants performed no better than sighted controls. Together, these findings suggest that complete

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

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visual deprivation very early in development leads to heightened tactile acuity. In the present study, we did not calibrate stimulus amplitudes on frequency-dependent detection thresholds for each participant. This means that individual differences in absolute detection thresholds may have accounted for the group differences that we found in sensitivity. Previous research has shown that tactile discrimination thresholds may depend on absolute thresholds, although the dependence is weak (see Verrillo & Bolanowski, 2008). Thus, even if the groups differed in absolute thresholds, it is unlikely that such differences could account for the significant differences in frequency discrimination that we observed. Another argument is that because the stimulus amplitudes varied slightly across stimulus frequencies, it is possible that the discriminations were made on the basis of amplitudes rather than frequencies. This possibility is unlikely, however, given that the differences in amplitude were very close if not below the JNDs for amplitude discrimination (Verrillo, 1963; Verrillo & Bolanowski, 2008). Furthermore, the possibility of this confound does not alter our conclusion that early-blind, but not late-blind, individuals exhibit superior tactile discrimination abilities. We observed a positive relationship between task performance and daily Braille reading hours. This relationship suggests that there may be some components of Braille reading that overlap with vibrotactile abilities. At a basic level, Braille may be considered a vibrotactile stimulus, as the fingers scan over raised dots. More generally, it is possible that blind individuals have greater experience with using vibrotactile information in the environment. However, years of Braille reading did not correlate with task performance suggesting that it is current Braille reading practice rather than long-term experiences that enhance vibrotactile discrimination. Furthermore, our data indicate that it is the timing (i.e., onset), rather than the duration of blindness that is responsible for heightened sensitivity in the blind. Importantly, the advantage of the congenitally blind persisted even when daily Braille reading was accounted for. Thus, our data are consistent with those of Röder et al. (2004) who reported that congenital, but not lateblind individuals, were better than sighted individuals on temporal order judgments for tactile stimuli. They also indicate that the precise relationship between tactile acuity and practice (in terms of Braille reading experience) warrants further investigation (Sathian, 2000). Differences in tactile acuity between blind and sighted individuals may be attributed to their brain organization. For example, as a result of intensive task practice, enlarged finger representations (i.e., intramodal plasticity) have been observed in blind Braille readers (Pascual-Leone & Torres, 1993). Blind individuals also show activation in the occipital cortex (i.e., cross-modal plasticity) when they read Braille (Sadato et al., 1996) or perform a tactile microspatial discrimination task (Stilla et al., 2008). Consistent with this, bilateral occipital damage has been associated with an inability to read Braille in a congenitally blind woman (Hamilton, Keenan, Catala, & Pascual-Leone, 2000) Thus, there appears to be at least two possible neural mechanisms responsible for the heightened tactile acuity. One is the involvement of the occipital cortex during tactile processing. In addition, the association with daily Braille reading suggests a role for intramodal plasticity. The idea of a sensitive period has long been accepted in the language acquisition literature (e.g., Hurford, 1991). Similarly, it has been argued that the timing of blindness onset during development may determine the degree of sensory enhancement in the non-visual modalities (Neville & Bavelier, 2002). However, few behavioral studies have directly compared early-blind and lateblind individuals. From the neuroimaging literature, there appears to be a critical period for cross-modal activation of the occipital cortex to develop (Cohen et al., 1999; Sadato et al., 2002): individuals

blinded after 14–16 years show no occipital activation compared to those blinded earlier. These neuroimaging data are consistent with those of the present study as tactile acuity was enhanced, on average, only in those individuals who became blind before the age of 14 years. We have provided evidence that congenital blindness leads to enhanced vibrotactile discrimination ability. It is the timing, rather than the duration, of blindness that appears responsible for this heightened sensitivity. Importantly, the effects of blindness onset persisted even when daily Braille reading hours were accounted for, suggesting that sensory deprivation early in life is a critical determinant of heightened tactile discrimination in the blind. Acknowledgements This research was supported by The Melbourne Research Grant Scheme 2006. A.G.W. was supported by a National Health and Medical Research Council Clinical Research Training Fellowship (251755). We sincerely thank all the blind volunteers, without whom this study could not be conducted. We would also like to thank Max Rademacher and Young Ho Kim for their technical assistance and Jason Forte and Charles Liu for their comments. References Burton, H., Sinclair, R. J., & McLaren, D. G. (2004). Cortical activity to vibrotactile stimulation: An fMRI study in blind and sighted individuals. Human Brain Mapping, 23, 210–228. Cohen, L. G., Weeks, R. A., Sadato, N., Celnik, P., Ishii, K., & Hallett, M. (1999). Period of susceptibility for cross-modal plasticity in the blind. Annals of Neurology, 45, 451–460. Fox, J. (1997). Applied regression analysis, linear models, and related methods. Thousand Oaks, CA: Sage. Goldreich, D., & Kanics, I. M. (2003). Tactile acuity is enhanced in blindness. Journal of Neuroscience, 23, 3439–3445. Goldreich, D., & Kanics, I. M. (2006). Performance of blind and sighted humans on a tactile grating detection task. Perception & Psychophysics, 68, 1363–1371. Gougoux, F., Lepore, F., Lassonde, M., Voss, P., Zatorre, R., & Belin, P. (2004). Pitch discrimination in the early blind. Nature, 430, 309–1309. Grant, A. C., Thiagarajah, M. C., & Sathian, K. (2000). Tactile perception in blind Braille readers: A psychophysical study of acuity and hyperacuity using gratings and dot patterns. Perception & Psychophysics, 62, 301–312. Hamilton, R., Keenan, J. P., Catala, M., & Pascual-Leone, A. (2000). Alexia for Braille following bilateral occipital stroke in an early blind woman. Neuroreport, 11, 237–240. Heller, M. A. (1989). Picture and pattern perception in the sighted and blind: The advantage of the late blind. Perception, 18, 379–389. Howell, D. C. (2002). Statistical Methods for Psychology (5th ed.). Australia: Duxbury. Hurford, J. R. (1991). The evolution of the critical period for language-acquisition. Cognition, 40, 159–201. Merabet, L. B., Hamilton, R., Schlaug, G., Swisher, J. D., Kiriakopoulos, E. T., Pitskel, N. B., et al. (2008). Rapid and reversible recruitment of early visual cortex for touch. PLoS ONE, 3(8), e3046. Neville, H., & Bavelier, D. (2002). Human brain plasticity: Evidence from sensory deprivation and altered language experience. Progress in Brain Research, 138, 177–188. Pascual-Leone, A., Theoret, H., Merabet, L. B., Kauffman, T., & Schlaug, G. (2006). The role of visual cortex in tactile processing: A metamodal brain. In M. A. Heller, & S. Ballesteros (Eds.), Touch and blindness: Psychology and neuroscience (pp. 171–195). New Jersey: Lawrence Erlbaum Associates. Pascual-Leone, A., & Torres, F. (1993). Plasticity of the sensorimotor cortex representation of the reading finger in Braille readers. Brain, 116, 39–52. Röder, B., Rösler, F., & Spence, C. (2004). Early vision impairs tactile perception in the blind. Current Biology, 14, 121–124. Sadato, N., Okada, T., Honda, M., & Yonekura, Y. (2002). Critical period for crossmodal plasticity in blind humans: A functional MRI study. Neuroimage, 16, 389–400. Sadato, N., Pascual-Leone, A., Grafman, J., Ibanez, V., Deiber, M. P., Dold, G., et al. (1996). Activation of the primary visual cortex by Braille reading in blind subjects. Nature, 380, 526–528. Sathian, K. (2000). Practice makes perfect: Sharper tactile perception in the blind. Neurology, 54, 2203–2204. Stilla, R., Hanna, R., Hu, X. P., Mariola, E., Deshpande, G., & Sathian, K. (2008). Neural processing underlying tactile microspatial discrimination in the blind: A functional magnetic resonance imaging study. Journal of Vision, 8(10).

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