Abstract

The behavioral and neurofunctional consequences of blindness often include performance enhancements and recruitment of occipital regions for nonvisual tasks. How the neuroanatomical changes resulting from this sensory loss relate to these functional changes is, however, less clear. Previous studies using cortical thickness (CT) measures have shown thicker occipital cortex in early-blind (EB) individuals compared with sighted controls. We hypothesized that this finding reflects the crossmodal plasticity often observed in blind individuals and thus could reflect behavioral adaptations. To address this issue, CT measures in blind (early and late) and sighted subjects were obtained along with several auditory behavioral measures in an attempt to relate behavioral and neuroanatomical changes. Group contrasts confirmed previous results in showing thicker occipital cortex in the EB. Regression analyses between CT measures across the whole brain of all blind individuals with the behavioral scores from 2 tasks in which EB subjects were superior (pitch and melody discrimination) showed that CT of occipital areas was directly related to behavioral enhancements. These findings constitute a compelling demonstration that anatomical changes in occipital areas are directly related to heightened behavioral abilities in the blind and hence support the idea that these anatomical features reflect adaptive compensatory plasticity.

Introduction

It is now well established that crossmodal reorganization occurs in the brain of the visually deprived (Pascual-Leone et al. 2005), manifesting itself as activity in typically visual occipital regions during nonvisual tasks. In parallel, many blind individuals compensate behaviorally for their sensory loss by developing heightened abilities in their remaining sensory modalities (Merabet and Pascual-Leone 2010; Voss et al. 2010). Crucial to our understanding of these adaptations was the demonstration that occipital recruitment is directly related to improved behavioral skill, either through correlational analyses (Röder et al. 2002; Amedi et al. 2003; Gougoux et al. 2005; Stevens et al. 2007) or via transient disruptions of occipital function (Cohen et al. 1997; Amedi et al. 2004; Collignon et al. 2007).

The link between these functional changes and any neuroanatomical changes resulting from blindness has remained largely unexplored. Using various morphometry analyses, several groups have observed significant gray (GM) and white matter (WM) reductions throughout the visual system in early-blind (EB) individuals (Noppeney et al. 2005; Pan et al. 2007; Ptito et al. 2008; Lepore et al. 2010). Several groups have also shown significant atrophy in the geniculocortical tracts (Shimony et al. 2006; Park et al. 2007; Shu, Li et al. 2009) using diffusion imaging. What remains unclear from this literature is how the apparent atrophy of these structures can be compatible with the consistent recruitment of occipital regions for nonvisual tasks.

In contrast to these widespread volume decreases, cortical thickness (CT) analyses have shown thicker occipital cortex in the EB compared with sighted individuals (Bridge et al. 2009; Jiang et al. 2009; Park et al. 2009). The significance of these findings and how they fit with the evidence of atrophy remains elusive. While Jiang et al. (2009) argued that this finding was likely due to reduced synaptic pruning following early visual loss, Park et al. (2009) rather suggested that it was the result of crossmodal plastic changes following visual deprivation.

In other domains, regional brain structure has been successfully linked to behavior. For instance, GM/WM concentration and CT in specific cerebral areas correlate with performance on musical tasks (Schneider et al. 2005; Hyde et al. 2006; Foster and Zatorre 2010b), speech tasks (Golestani et al. 2002; Wong et al. 2008), and visual tasks (Schwarzkopf et al. 2011). These studies suggest that anatomical measures can reflect the individual differences in processing of the regions in question. Therefore, our goal in the present study was to investigate this issue in blind individuals and to identify neuroanatomical structures that predict performance. More specifically, we aimed to identify cortical plastic changes that are associated with significant enhancements in auditory perceptual abilities following early blindness. Given the established relationship between visual cortical activation and improved processing of nonvisual stimuli modalities (see Merabet & Pascual-Leone 2010; Voss et al. 2010) and the observation of larger CT in the EB (Bridge et al. 2009; Jiang et al. 2009; Park et al. 2009), we expected that CT measures of these areas should predict performance in auditory tasks in blind individuals if the hypothesis is correct that anatomical changes reflect compensatory mechanisms and hence lead to significant behavioral improvements.

Materials and Methods

Subjects

Forty-nine participants initially took part in the study. Three were excluded from all analyses. Two were discarded due to severe motion artifacts and one because of the presence of congenital hydrocephaly. Blind subjects were divided into 2 groups based on the age of onset of blindness, to ascertain its effect on the different measures obtained. Fourteen EB (38.2 ± 13.8 years of age; 10 males and 4 females), 13 late-blind (LB) (46.6 ± 8.5 years; 5 males and 8 females), and 19 sighted subjects (37.6 ± 12.0 years; 8 males and 11 females) participated in the study. The cutoff point between both groups was based on the age at which synaptic density in the visual cortex normally reaches adult levels, generally by ∼5 years of age (Johnson 1997). Demographic data and causes of blindness are summarized in Table 1. In each case of blindness, the visual deficit resulted from anomalies in peripheral structures with no neurological deficits and led to total blindness except for minimal residual light sensitivity in 5 LB subjects and in 4 EB subjects. The EB had an average age of onset of blindness of 0.5 ± 1.2 years and an average duration of blindness of 37.7 ± 14.3 years, whereas these values for the LB were, respectively, 29.4 ± 15.4 and 17.5 ± 10.6 years. Audiometric thresholds were assessed for all participants and indicated normal and comparable hearing in both ears. Given the potential influence of musical training on the tasks, we compared the number of years of formal training in each group: EB (4.78 ± 4.54 years), LB (1.69 ± 2.05 years), and sighted (3.47 ± 6.11 years). An analysis of variance confirmed the absence of any statistical difference in the number of years of formal musical training between groups (F = 1.406, P = 0.256). All subjects gave written informed consent in accordance with the guidelines approved by the Montreal Neurological Institute (MNI) and the Nazareth and Louis-Braille Institute (NLBI) for the blind. The research protocols were approved by the ethics committees of the Centre de Recherche Interdisciplinaire en Réadaptation (CRIR), which coordinates research with blind subjects sponsored by the NLBI and by the research ethics board of the MNI, where the scanning procedures were carried out. During testing, all subjects wore a blindfold to avoid any impact that vision (sighted) and residual light perception (blind) could have had on the results. During breaks and between tasks subjects were instructed to remove the blindfold to avoid any behavioral (Kauffman et al. 2002; Facchini and Aglioti 2003; Lewald 2007) or neural long-term effects of sensory deprivation in the sighted (Boroojerdi et al. 2000; Pascual-Leone and Hamilton 2001; Kauffman et al. 2002; Weisser et al. 2005; Lewald 2007; Pitskel et al. 2007; Merabet et al. 2008).

Table 1

Subject demographic information

Subjects Age Sex Onset Duration LP Cause of blindness 
EB1 32 28 No Retinoblastoma 
EB2 27 27 No Retinal detachment 
EB3 37 37 No Congenital glaucoma 
EB4 57 57 No Retinopathy of prematurity 
EB5 21 21 No Retinopathy of prematurity 
EB6 26 26 No Congenital cataracts 
EB7 40 40 No Retinopathy of prematurity 
EB8 52 52 No Medical accident (retina damage) 
EB9 20 20 Yes Congenital malformation (no cristallin) 
EB10 59 59 Yes Congenital cataracts 
EB11 24 21 No Retinoblastoma 
EB12 45 45 No Congenital glaucoma 
EB13 39 39 Yes Retinopathy of prematurity 
EB14 56 56 Yes Retinal detachment 
LB1 44 21 23 No Congenital glaucoma 
LB2 48 28 20 No Diabetic retinopathy 
LB3 48 24 24 No Ischemic retinopathy 
LB4 53 30 23 Yes Retinal degeneration 
LB5 53 19 34 No Glaucoma 
LB6 60 48 12 No Failed cornea transplant 
LB7 52 50 Yes Dehydration of the optic nerve 
LB8 59 54 No Retinitis pigmentosa 
LB9 46 43 Yes Glaucoma + retinal detachment 
LB10 48 32 16 Yes Retinal detachment 
LB11 29 17 13 Yes Congenital Glaucoma 
LB12 37 18 No Congenital Glaucoma 
LB13 42 35 No Lenticular fibroplasia 
Subjects Age Sex Onset Duration LP Cause of blindness 
EB1 32 28 No Retinoblastoma 
EB2 27 27 No Retinal detachment 
EB3 37 37 No Congenital glaucoma 
EB4 57 57 No Retinopathy of prematurity 
EB5 21 21 No Retinopathy of prematurity 
EB6 26 26 No Congenital cataracts 
EB7 40 40 No Retinopathy of prematurity 
EB8 52 52 No Medical accident (retina damage) 
EB9 20 20 Yes Congenital malformation (no cristallin) 
EB10 59 59 Yes Congenital cataracts 
EB11 24 21 No Retinoblastoma 
EB12 45 45 No Congenital glaucoma 
EB13 39 39 Yes Retinopathy of prematurity 
EB14 56 56 Yes Retinal detachment 
LB1 44 21 23 No Congenital glaucoma 
LB2 48 28 20 No Diabetic retinopathy 
LB3 48 24 24 No Ischemic retinopathy 
LB4 53 30 23 Yes Retinal degeneration 
LB5 53 19 34 No Glaucoma 
LB6 60 48 12 No Failed cornea transplant 
LB7 52 50 Yes Dehydration of the optic nerve 
LB8 59 54 No Retinitis pigmentosa 
LB9 46 43 Yes Glaucoma + retinal detachment 
LB10 48 32 16 Yes Retinal detachment 
LB11 29 17 13 Yes Congenital Glaucoma 
LB12 37 18 No Congenital Glaucoma 
LB13 42 35 No Lenticular fibroplasia 

Note: The “Onset” column refers to the age at which the subjects lost their sight. The “Duration” column refers to the number of years that the subjects have been blind. The “LP” column indicates whether subjects still had any residual light perception.

Behavioral Tasks

Several different auditory behavioral measures were obtained, taken from Foster and Zatorre (2010a). Two low-level auditory tasks: 1) pitch discrimination and 2) loudness discrimination; and 3 higher level auditory tasks: 3) simple melody discrimination, 4) transposed melody discrimination, and 5) phoneme discrimination. These pitch and melody tasks were selected on the basis that they were likely to be sensitive to blind people's enhanced tonal perception (Gougoux et al. 2004; Wan et al. 2010). The loudness task was selected as a control task for the pitch task, as previous research has shown that blind individuals do not have lower loudness thresholds (Sakurabayashi et al. 1956; Starlinger and Niemeyer 1981), whereas the phoneme task was selected as control task for the melody tasks, as it was designed to be matched to them for duration and number of items and to equate the overall working memory load.

All 5 auditory tasks were administered by a computer running Presentation software (Neurobehavioral systems) in a sound-treated room. The stimuli were presented binaurally using “Sennheiser Koss” headphones, driven by a “RME Fireface 800” interface and amplified by a “Behringer powerplay pro-8” headphone amp, and adjusted to a comfortable sound level. Task order was counterbalanced across subjects and divided into 2 brief sessions. Each session consisted in 1 repetition of each high-level auditory task, 2 repetitions of each low-level auditory task, and lasted approximately 30 min. The individual trials were randomized within each repetition of the task, with the exception of the 2 low-level auditory tasks as they were designed to produce sensitivity thresholds via a staircase paradigm, whereas the higher level auditory tasks produced percentage scores.

Low-Level Auditory Tasks

Both tasks were same/different discrimination tasks for which the subjects responded via button press on a 2-button mouse.

  1. Pitch discrimination task. Subjects had to specify which of 2 tones was higher in pitch. The reference tone was a 500 Hz pure tone, and the task followed a 2-down/1-up staircase procedure (the initial difference between the 2 tones was stepped down after 2 sequential correct responses and stepped up after a single incorrect response). This procedure produces runs of increasing and decreasing the difference between stimuli whose endpoints (reversal points) bracket the 71% threshold (Levitt 1970). The initial difference in frequency was 7%, and the initial step factor was 2 (to converge rapidly onto the subject's approximate threshold). After 2 reversals, the step factor was reduced to 1.25 to determine the threshold with greater precision. One staircase run was completed after 15 reversals, and the geometric mean of the value of the last 8 reversals was taken as the threshold. The threshold is therefore unaffected by the choice of starting difference because the first 7 endpoints are not entered into the calculation. Four separate interleaved runs were conducted for each subject and averaged to produce the final value.

  2. Loudness discrimination task. Subjects had to specify which of 2 tones was the louder. The procedure was identical to that of the pitch discrimination task with the lone exception of the initial difference in loudness being set at 10 dB. For each task, the subjects responded with the aid of a 2-button mouse. The standard reference loudness of the tones was set at 65 dB sound pressure level.

High-Level Auditory Tasks

All 3 higher level auditory tasks and stimuli used are described in more detail elsewhere (Foster and Zatorre 2010a). For each task, subjects had to respond whether 2 sequences were identical or not via a button press on a 2-button mouse. The sequences were composed of 5–13 elements (notes or phonemes), and each element had a 320-ms duration. Briefly, they were:

  1. Simple melody discrimination task. Subjects were instructed to determine whether 2 sequential melodies were identical or different. All stimuli were unfamiliar melodies in the Western major scale. On half of the trials (different trials), the pitch of a single note was changed anywhere in the melody by up to ±5 semitones (median of 2 semitones). The change maintained the key of the melody as well as the melodic contour.

  2. Transposed melody discrimination task. This task was identical to the previous task with 2 exceptions. First, all the notes of the second stimulus pattern were transposed 4 semitones higher in pitch (in both the “same” and the “different” trials). Second, in different trials, 1 note was altered by 1 semitone to a pitch outside the pattern's new key, maintaining the melodic contour. This task therefore requires that the listener compare the pattern of pitch intervals (frequency ratios) between each successive tone, as opposed to the absolute pitches of each tone, since these are always different in the 2 melodies of the pair due to the transposition. As such, this task requires a more abstract relational processing, as opposed to the simple melody task, which can be accomplished by direct comparison of the individual pitch values.

  3. Phoneme discrimination task. Subjects were instructed to determine whether 2 sequences of phonemes were identical or different. The stimuli were monotone real speech consonant–vowel syllables. The full set of phonemes consisted of 12 permutations of 8 consonants [b,k,f,n,p,r,s,j] and 4 vowels [o,a,u,i] and were selected to have minimal semantic association. In half of the trials (different trials), one of the elements of the second pattern was changed to a different phoneme. Importantly, both stimuli presented in a same trial used different source recordings of the same speaker, so that acoustical cues unrelated to phoneme identify could not be used.

Image Acquisition

T1-weighted images (time echo = 2.98 ms, time repetition = 2300 ms, matrix size: 256 × 256, voxel size 1 × 1 × 1 mm) were acquired on a Siemens Magnetom 3-T MRI scanner.

CT Analysis

All MRIs were submitted to the CIVET pipeline (version 1.1.9; Zijdenbos et al. 2002; Ad-Dab'bagh et al. 2005). T1 images were registered to the ICBM152 nonlinear sixth generation template with a 12-parameter linear transformation (Collins et al. 1994; Grabner et al. 2006), RF inhomogeneity corrected (Sled et al. 1998), and tissue classified (Zijdenbos et al. 1998; Tohka et al. 2004). Deformable models were then used to create the WM/GM and GM/cerebrospinal fluid interfaces for each hemisphere separately (MacDonald et al. 2000; Kim et al. 2005), resulting in 4 polygonal mesh surfaces of 40 962 vertices each. From these surfaces, the t-Laplace metric was derived by using the Laplacian method for determining the distance between the white and the gray surfaces (Jones et al. 2000; Lerch and Evans 2005; Haidar and Soul 2006). The thickness data were subsequently blurred using a 20-mm surface-based diffusion blurring kernel in preparation for statistical analyses (Chung and Taylor 2004). Unnormalized native-space thickness values were used in all analyses owing to the poor correlation between CT and brain volume (Ad-Dab'bagh et al. 2005; Sowell et al. 2007). This is because normalizing for global brain size, when it has little pertinence to CT, risks introducing noise and reducing power.

All statistical analyses were performed using in-house software (Surfstat Matlab toolbox; http://www.math.mcgill.ca/keith/surfstat/) developed at the MNI. First, we compared global differences across groups, by contrasting the CT values between the EB, LB, and sighted. Second, we computed the correlation between CT values and age at which sight was lost, as well as number of years of blindness; this was done to determine whether any changes seen in the group contrast could be ascribed to just one or to both of these factors. Finally, we determined the correlation between CT values and task performance, for both the pitch discrimination task and the transposed melody task, across the whole cortical surface using vertexwise generalized linear model analyses in which the behavioral values were entered as regressors. These 2 tasks were selected for correlational analysis because they were the only ones to show statistically significant behavioral enhancements in the EB over sighted individuals. This rationale is in line with our goal to identify cortical plastic changes associated with significant compensatory behavioral changes following early blindness.

Results

Behavioral Results

The dependent variables from each behavioral task were entered into analyses of variance in order to compare overall performance across the 3 groups. No significant differences were observed between groups for the loudness discrimination task (F2,43 = 0.854, P = 0.433) or the phoneme discrimination task (F2,43 = 0.814, P = 0.450). However, significant differences were found for the pitch discrimination task (F2,43 = 4.104, P = 0.024), the simple melody task (F = 6.480, P = 0.003), and the transposed melody discrimination task (F2,43 = 4.088, P = 0.024) (see Figs 1 and 2). Post hoc Tukey's tests confirmed that these effects are driven by the EB group outperforming one or both of the other groups (pitch task: LB [P = 0.14], sighted [P = 0.02]; simple melody: LB [P = 0.002], sighted [P = 0.086]; transposed melody: LB [P = 0.036], sighted [P = 0.049]). As an additional control, we entered the number of years of formal musical training that each subject had as a covariate; the main group effects for the pitch, simple melody, and transposed melody tasks all remained significant (P < 0.05), indicating that any residual differences in musical training across the groups did not account for the advantage shown by the EB.

Figure 1.

Group threshold averages for the pitch (left) and loudness (right) discrimination tasks showing that EB individuals have a significantly better pitch but not loudness discrimination ability. Stars between columns denote significant differences between blind groups, whereas stars above columns denote a significant difference between the EB group and the sighted group (SIG); no differences were observed between the LB group and the sighted group. Error bars represent the standard error of the mean.

Figure 1.

Group threshold averages for the pitch (left) and loudness (right) discrimination tasks showing that EB individuals have a significantly better pitch but not loudness discrimination ability. Stars between columns denote significant differences between blind groups, whereas stars above columns denote a significant difference between the EB group and the sighted group (SIG); no differences were observed between the LB group and the sighted group. Error bars represent the standard error of the mean.

Figure 2.

Group score averages for the simple melody (top), transposed melody (middle), and phoneme (bottom) discrimination tasks, indicating that the EB have superior performance in the 2 melody tasks but not in the phoneme task. Stars between columns denote significant differences between blind groups, whereas stars above columns denote a significant difference between the EB group and the sighted group (SIG); no differences were observed between the LB group and the sighted group. Error bars represent the standard deviation.

Figure 2.

Group score averages for the simple melody (top), transposed melody (middle), and phoneme (bottom) discrimination tasks, indicating that the EB have superior performance in the 2 melody tasks but not in the phoneme task. Stars between columns denote significant differences between blind groups, whereas stars above columns denote a significant difference between the EB group and the sighted group (SIG); no differences were observed between the LB group and the sighted group. Error bars represent the standard deviation.

CT Contrasts

Figure 3 illustrates the different regions where differences were observed between groups (for complete list of differences observed for all contrasts, see Table 2). When contrasted with the sighted, the EB were shown to have thicker cortex in the left lingual gyrus and the right lateral occipital gyrus, whereas the sighted shown to possess thicker cortex in the left entorhinal cortex and the right superior parietal lobule, relative to the EB. The LB, when contrasted with the sighted, rather show cortical thinning in previously visual areas: the lingual gyrus bilaterally, the cuneus bilaterally and the left inferior/middle occipital gyrus. Finally, the LB also showed cortical thinning relative to the EB in the lingual gyrus bilaterally, the left cuneus, the left fusiform gyrus, and in the left lateral occipital gyrus.

Table 2

List of peak areas where cortical differences between groups were above T = 3.53 (P = 0.0005, uncorrected), with the exception of the Sighted–Early and Early–Sighted contrasts, where the threshold was reduced to P = 0.005, to highlight differences in predicted regions in the Early–Sighted contrast

Contrast Region Coordinates T value P value 
  x y z   
Early–Sighted 
    LH Lingual gyrus −10 −77 −4 3.01 <0.005 
    RH Lateral occipital gyrus 20 −87 −9 2.48 <0.005 
Early–Late 
    LH Lingual gyrus −26 −59 −5 5.46 <0.000001* 
    RH Lingual gyrus 5 −74 6 5.08 <0.000005* 
    LH Supramarginal gyrus −57 −48 35 3.82 <0.0005 
    LH Postcentral gyrus −40 −15 49 3.77 <0.0005 
    LH Lateral occipital gyrus −46 −60 13 3.66 <0.0005 
    LH Fusiform gyrus −42 −23 −23 3.64 <0.0005 
    LH Angular gyrus −50 −57 33 3.60 <0.0005 
    LH Cuneus −6 −75 17 3.57 <0.0005 
    LH Superior frontal gyrus −13 68 3.57 <0.0005 
Sighted–Early 
    LH Entorhinal cortex −24 −1 −32 3.12 <0.005 
    RH Superior parietal lobule 14 −42 78 3.09 <0.005 
    LH Posterior orbital gyrus −18 13 −22 3.01 <0.005 
    RH Cingulate gyrus 37 13 2.86 <0.005 
Sighted–Late 
    LH Lingual gyrus −24 −54 −5 5.12 <0.000005* 
    RH Cuneus 7 −82 32 4.38 <0.00005 
    LH Supramarginal gyrus −60 −43 38 4.37 <0.00005 
    LH Cingulate gyrus −8 20 32 4.31 <0.00005 
    LH Inferior frontal gyrus −52 16 4.27 <0.0001 
    LH Middle frontal gyrus −39 25 41 4.23 <0.0001 
    RH Superior frontal gyrus 29 49 4.2 <0.0001 
    LH Cingulate gyrus −8 16 34 4.14 <0.0001 
    RH Superior parietal lobule 12 −48 75 4.09 <0.0001 
    RH Lingual gyrus 24 −56 −5 4.02 <0.0005 
    LH Superior parietal lobule −18 −57 67 3.99 <0.0005 
    RH Insular gyrus 33 15 −13 3.97 <0.0005 
    LH Cuneus −5 −76 17 3.96 <0.0005 
    LH Insular gyrus −38 −3 −3 3.88 <0.0005 
    RH Inferior temporal gyrus 34 −43 3.88 <0.0005 
    LH Postcentral gyrus −41 −13 50 3.75 <0.0005 
    LH Inferior/middle occipital gyrus −17 −82 −11 3.66 <0.0005 
    RH Insular gyrus 40 −6 3.60 <0.0005 
Contrast Region Coordinates T value P value 
  x y z   
Early–Sighted 
    LH Lingual gyrus −10 −77 −4 3.01 <0.005 
    RH Lateral occipital gyrus 20 −87 −9 2.48 <0.005 
Early–Late 
    LH Lingual gyrus −26 −59 −5 5.46 <0.000001* 
    RH Lingual gyrus 5 −74 6 5.08 <0.000005* 
    LH Supramarginal gyrus −57 −48 35 3.82 <0.0005 
    LH Postcentral gyrus −40 −15 49 3.77 <0.0005 
    LH Lateral occipital gyrus −46 −60 13 3.66 <0.0005 
    LH Fusiform gyrus −42 −23 −23 3.64 <0.0005 
    LH Angular gyrus −50 −57 33 3.60 <0.0005 
    LH Cuneus −6 −75 17 3.57 <0.0005 
    LH Superior frontal gyrus −13 68 3.57 <0.0005 
Sighted–Early 
    LH Entorhinal cortex −24 −1 −32 3.12 <0.005 
    RH Superior parietal lobule 14 −42 78 3.09 <0.005 
    LH Posterior orbital gyrus −18 13 −22 3.01 <0.005 
    RH Cingulate gyrus 37 13 2.86 <0.005 
Sighted–Late 
    LH Lingual gyrus −24 −54 −5 5.12 <0.000005* 
    RH Cuneus 7 −82 32 4.38 <0.00005 
    LH Supramarginal gyrus −60 −43 38 4.37 <0.00005 
    LH Cingulate gyrus −8 20 32 4.31 <0.00005 
    LH Inferior frontal gyrus −52 16 4.27 <0.0001 
    LH Middle frontal gyrus −39 25 41 4.23 <0.0001 
    RH Superior frontal gyrus 29 49 4.2 <0.0001 
    LH Cingulate gyrus −8 16 34 4.14 <0.0001 
    RH Superior parietal lobule 12 −48 75 4.09 <0.0001 
    RH Lingual gyrus 24 −56 −5 4.02 <0.0005 
    LH Superior parietal lobule −18 −57 67 3.99 <0.0005 
    RH Insular gyrus 33 15 −13 3.97 <0.0005 
    LH Cuneus −5 −76 17 3.96 <0.0005 
    LH Insular gyrus −38 −3 −3 3.88 <0.0005 
    RH Inferior temporal gyrus 34 −43 3.88 <0.0005 
    LH Postcentral gyrus −41 −13 50 3.75 <0.0005 
    LH Inferior/middle occipital gyrus −17 −82 −11 3.66 <0.0005 
    RH Insular gyrus 40 −6 3.60 <0.0005 

Note: Occipital/visual regions are listed in bold as it was hypothesized that differences would emerge in these regions.

*Significant at P < 0.05 corrected for multiple comparisons across all vertices.

Figure 3.

Illustration of the CT differences between groups. Images were thresholded at the indicated values (uncorrected P values). The EB show increased occipital thickness compared with the sighted in the left lingual gyrus and the right lateral occipital gyrus (extreme left column; orange arrows), whereas the LB rather show a reduction in occipital thickness compared with the sighted in both the left and the right lingual gyrus, as well as in the left and right cuneus (extreme right column; green arrows).

Figure 3.

Illustration of the CT differences between groups. Images were thresholded at the indicated values (uncorrected P values). The EB show increased occipital thickness compared with the sighted in the left lingual gyrus and the right lateral occipital gyrus (extreme left column; orange arrows), whereas the LB rather show a reduction in occipital thickness compared with the sighted in both the left and the right lingual gyrus, as well as in the left and right cuneus (extreme right column; green arrows).

Regression Analyses

Four separate vertexwise regression analyses were carried out across all blind subjects (early and late combined). Two of these regressions were intended to identify regions that varied as a function of the age of the onset of blindness and the total duration of blindness (see Fig. 4). Occipital regions and the fusiform gyrus were found to correlate significantly with both measures (for more complete details, see Table 3). The duration of blindness explained 30% of the variance at the maximal peak of covariation in the right cuneus (coord: 6, −73, 20; r = 0.55), whereas the age of onset of blindness explained 37% of the variance at the maximal peak of covariation in the right cuneus (coord: 18, −64, 14; r = −0.61).

Table 3

List of peak areas where cortical differences between groups were above T = 3.70 (P = 0.0005, uncorrected)

Regression Region Coordinates T value P value 
  x y z   
Onset 
    LH Precentral gyrus −42 −12 48 4,15 <0.0005 
    LH Superior frontal gyrus −22 29 44 4,02 <0.0005 
    LH Angular gyrus −39 −62 45 3,78 <0.0005 
    RH Postcentral gyrus 22 −28 63 3,77 <0.0005 
    LH Fusiform gyrus −28 −55 −13 3,72 <0.0005 
    RH Cuneus 18 −64 14 3,71 <0.0005 
    RH Lingual gyrus 16 −75 −4 3,58 <0.001 
    LH Cuneus −4 −82 −2 3,55 <0.001 
    RH Cuneus 5 −80 1 3,5 <0.001 
Duration 
    RH Cuneus 6 −73 20 4,46 <0.0001 
    LH Fusiform gyrus −39 −44 −19 4,36 <0.0001 
    LH Lingual/fusiform gyrus −30 −58 −13 4,22 <0.0005 
    LH Middle/lateral occipital gyrus −42 −69 −4 4,14 <0.0005 
    RH Cingulate gyrus −11 28 3,93 <0.0005 
Pitch 
    RH Cuneus 11 −73 24 4,96 <0.00005 
    LH Superior frontal gyrus −5 58 4,92 <0.00005 
    RH Middle/lateral occipital gyrus 18 −99 17 4,7 <0.00005 
    LH Supramarginal gyrus −54 −44 46 4,52 <0.0001 
    LH Lingual gyrus −19 −41 −9 4,52 <0.0001 
    RH Fusiform gyrus 31 −64 −11 4,48 <0.0001 
    LH Middle frontal gyrus −28 26 42 4,33 <0.0001 
    LH Cuneus −7 −76 19 4,26 <0.0005 
    LH Middle/lateral occipital gyrus −17 −96 18 4,2 <0.0005 
    LH Inferior frontal gyrus −55 23 16 4,17 <0.0005 
    LH Superior frontal gyrus −24 28 41 4,1 <0.0005 
    LH Superior frontal gyrus −22 62 <0.0005 
    RH Lingual gyrus 19 −67 −3 3,98 <0.0005 
    LH Fusiform gyrus −29 −61 −11 3,86 <0.0005 
    RH Precentral gyrus 43 −13 42 3,77 <0.0005 
Transposed melody 
    RH Cuneus 7 −78 18 6,29 <0.000001* 
    RH Lingual gyrus −5 −82 1 5,78 <0.000001* 
    LH Middle/lateral occipital gyrus −31 −91 −11 5,41 <0.00001* 
    LH Cingulate cortex −9 40 4,97 <0.00005 
    LH Cuneus −5 −77 17 4,83 <0.00005 
    RH Entorhinal cortex 26 −26 4,82 <0.00005 
    RH Postcentral gyrus 21 −28 64 4,79 <0.00005 
    RH Cingulate cortex −13 29 4,63 <0.00005 
    LH Precuneus −7 −46 35 4,62 <0.0001 
    RH Cingulate cortex −41 12 4,38 <0.0001 
    LH Lingual gyrus −10 −71 −1 4,1 <0.0005 
    LH Fusiform gyrus −42 −53 −14 4,01 <0.0005 
    LH Fusiform gyrus −26 −21 −18 4,05 <0.0005 
    RH Fusiform gyrus 36 −26 −26 3,93 <0.0005 
    LH Inferior occipital gyrus −41 −73 −11 3,92 <0.0005 
    RH Superior temporal gyrus 52 −46 14 3,87 <0.0005 
    LH Inferior temporal gyrus −58 −16 −25 3,86 <0.0005 
Regression Region Coordinates T value P value 
  x y z   
Onset 
    LH Precentral gyrus −42 −12 48 4,15 <0.0005 
    LH Superior frontal gyrus −22 29 44 4,02 <0.0005 
    LH Angular gyrus −39 −62 45 3,78 <0.0005 
    RH Postcentral gyrus 22 −28 63 3,77 <0.0005 
    LH Fusiform gyrus −28 −55 −13 3,72 <0.0005 
    RH Cuneus 18 −64 14 3,71 <0.0005 
    RH Lingual gyrus 16 −75 −4 3,58 <0.001 
    LH Cuneus −4 −82 −2 3,55 <0.001 
    RH Cuneus 5 −80 1 3,5 <0.001 
Duration 
    RH Cuneus 6 −73 20 4,46 <0.0001 
    LH Fusiform gyrus −39 −44 −19 4,36 <0.0001 
    LH Lingual/fusiform gyrus −30 −58 −13 4,22 <0.0005 
    LH Middle/lateral occipital gyrus −42 −69 −4 4,14 <0.0005 
    RH Cingulate gyrus −11 28 3,93 <0.0005 
Pitch 
    RH Cuneus 11 −73 24 4,96 <0.00005 
    LH Superior frontal gyrus −5 58 4,92 <0.00005 
    RH Middle/lateral occipital gyrus 18 −99 17 4,7 <0.00005 
    LH Supramarginal gyrus −54 −44 46 4,52 <0.0001 
    LH Lingual gyrus −19 −41 −9 4,52 <0.0001 
    RH Fusiform gyrus 31 −64 −11 4,48 <0.0001 
    LH Middle frontal gyrus −28 26 42 4,33 <0.0001 
    LH Cuneus −7 −76 19 4,26 <0.0005 
    LH Middle/lateral occipital gyrus −17 −96 18 4,2 <0.0005 
    LH Inferior frontal gyrus −55 23 16 4,17 <0.0005 
    LH Superior frontal gyrus −24 28 41 4,1 <0.0005 
    LH Superior frontal gyrus −22 62 <0.0005 
    RH Lingual gyrus 19 −67 −3 3,98 <0.0005 
    LH Fusiform gyrus −29 −61 −11 3,86 <0.0005 
    RH Precentral gyrus 43 −13 42 3,77 <0.0005 
Transposed melody 
    RH Cuneus 7 −78 18 6,29 <0.000001* 
    RH Lingual gyrus −5 −82 1 5,78 <0.000001* 
    LH Middle/lateral occipital gyrus −31 −91 −11 5,41 <0.00001* 
    LH Cingulate cortex −9 40 4,97 <0.00005 
    LH Cuneus −5 −77 17 4,83 <0.00005 
    RH Entorhinal cortex 26 −26 4,82 <0.00005 
    RH Postcentral gyrus 21 −28 64 4,79 <0.00005 
    RH Cingulate cortex −13 29 4,63 <0.00005 
    LH Precuneus −7 −46 35 4,62 <0.0001 
    RH Cingulate cortex −41 12 4,38 <0.0001 
    LH Lingual gyrus −10 −71 −1 4,1 <0.0005 
    LH Fusiform gyrus −42 −53 −14 4,01 <0.0005 
    LH Fusiform gyrus −26 −21 −18 4,05 <0.0005 
    RH Fusiform gyrus 36 −26 −26 3,93 <0.0005 
    LH Inferior occipital gyrus −41 −73 −11 3,92 <0.0005 
    RH Superior temporal gyrus 52 −46 14 3,87 <0.0005 
    LH Inferior temporal gyrus −58 −16 −25 3,86 <0.0005 

Note: Additional occipital/visual regions were listed (with P < 0.001) given our a priori hypotheses regarding these regions (listed in Italic). All occipital/visual regions are listed in bold as it was hypothesized that differences would emerge in these regions.

*Significant at P < 0.05 corrected for multiple comparisons across all vertices.

Figure 4.

Illustration of the covariation between CT and the duration of blindness (left column) and the age of onset of blindness (right column). Images were thresholded at the indicated values (uncorrected P values). The strongest associations were found in the right cuneus, the lingual gyrus bilaterally, and left fusiform gyrus. The bottom panels graphically illustrate the correlations for the peak that showed maximum covariation for each regression analysis. To the right of each graph, the CT values of each sighted subject are plotted for comparison with those of the blind.

Figure 4.

Illustration of the covariation between CT and the duration of blindness (left column) and the age of onset of blindness (right column). Images were thresholded at the indicated values (uncorrected P values). The strongest associations were found in the right cuneus, the lingual gyrus bilaterally, and left fusiform gyrus. The bottom panels graphically illustrate the correlations for the peak that showed maximum covariation for each regression analysis. To the right of each graph, the CT values of each sighted subject are plotted for comparison with those of the blind.

The other 2 regressions were performed to identify regions where CT would covary with the performance of all blind subjects on tasks in which the EB were shown to be superior to the sighted (pitch discrimination task and transposed melody task; see Fig. 5). This allowed us to measure plastic changes that are specifically related to behavioral enhancements in the blind. Even though only the EB showed behavioral enhancements, we chose to include both blind groups in the analyses as the poorer performances of the LB do not necessarily equate a breakdown of potential relationships between thickness measures in specific brain areas and performance.

Figure 5.

Illustration of the covariation between CT and the performance on the pitch (left column) and transposed melody (right column) tasks. Images were thresholded at the indicated values (uncorrected P values). The strongest associations were found in the right cuneus in both cases. The bottom panels graphically illustrate the correlations for the peak that showed maximum covariation for each regression analysis. The EB are represented by black dots, while the LB are represented by gray dots.

Figure 5.

Illustration of the covariation between CT and the performance on the pitch (left column) and transposed melody (right column) tasks. Images were thresholded at the indicated values (uncorrected P values). The strongest associations were found in the right cuneus in both cases. The bottom panels graphically illustrate the correlations for the peak that showed maximum covariation for each regression analysis. The EB are represented by black dots, while the LB are represented by gray dots.

The performance on the pitch task was shown to correlate most strongly with the right cuneus and was also correlated with other normally visual regions, such as the lateral occipital gyrus bilaterally, the lingual gyrus bilaterally, and the fusiform gyrus bilaterally (for complete list of correlations across the cortex, see Table 3 ). Performance on the transposed melody task was shown to correlate with the CT of the right cuneus and the right lingual gyrus, straddling the calarine sulcus. The thickness at the point of maximal covariation with pitch threshold in the right cuneus (coord: 11, −72, 23; r = −0.70) explained 49% of the variance in performance among blind individuals, whereas the thickness at the point of maximal covariation with the ability to discriminate transposed melodies in the right cuneus (coord: 7, −78, 17; r = 0.76) explained nearly 58% of the variance in performance. Finally, to ensure these effects were task specific, we also performed additional regression analyses with the performance of the loudness and phoneme tasks as regressors. Neither of these analyses showed CT correlations in the occipital cortex above a T value of 3.45, corresponding to a P value of 0.001 (uncorrected).

Discussion

The present study provides clear evidence that a neuroanatomical measure of occipital cortex thickness can be related to behavioral outcome. We show that the thickness of the occipital cortex in blind individuals is significantly correlated with performance on 2 pitch-based auditory tasks on which the EB outperform the sighted. Therefore, the present findings support the idea that the thicker occipital cortex observed in EB individuals reflects adaptive compensatory plasticity, in marked contrast with the atrophy of occipital structures described in other studies. Thus, the present findings serve to dissociate anatomical changes likely to be atrophy secondary to deafferentation from changes that reflect crossmodal reorganization.

Behavioral Findings

With regards to pitch discrimination, our results showing smaller thresholds in the EB are consistent with both those of Gougoux et al. (2004) and Wan et al. (2010), in that not only do blind individuals appear to develop heightened pitch processing abilities but that these abilities appear to be exclusive to EB individuals. Indeed, in all 3 studies, LB were equal in performance to the sighted group, suggesting that the improved ability to discriminate these subtle auditory cues only develops following an early onset of blindness. In contrast, we did not find any group differences with regards to loudness discrimination abilities, consistent with previous research (Sakurabayashi et al. 1956; Starlinger and Niemeyer 1981).

Few studies have investigated musical abilities of blind individuals via melody discrimination tasks. The present demonstration of superior performance of EB subjects compared with sighted ones in both tasks is most likely driven, at least in part, by the heightened ability of the EB to process pitch. However, the transposed melody task involves a much more abstract processing in which relationships between pitches must be computed; thus, good pitch discrimination is not sufficient. We did not observe a difference in the phoneme task, despite evidence from other studies indicating that the blind are better at some speech tasks (Röder et al. 2003; Hughdahl et al. 2004).

Increased CT in the Blind

The finding of thicker occipital cortex in EB individuals compared with LB or sighted replicates recent findings (Bridge et al. 2009; Jiang et al. 2009; Park et al. 2009). Our results from the EB-sighted contrast are very similar to those obtained by Park et al. (2009), in that thicker cortex is observed mainly in the left lingual gyrus. Although Bridge et al. (2009) also observed a larger extent of changes in the left hemisphere, changes were also observed in the cuneus, similar to what was observed by Jiang et al. (2009). We observed cortical thinning in the EB in the entorhinal cortex, as did Jiang et al. (2009), and in the right postcentral gyrus, as did Park et al. (2009). The results from the LB-sighted contrast showed cortical thinning in the LB in the cuneus, similar to Park et al. (2009), as well as in the fusiform gyrus, consistent with Jiang et al. (2009). However, the absence of evidence for occipital cortical thinning in the LB by Jiang et al. (2009) is in marked contrast with our findings. This is likely due to the fact that their LB group comprised individuals who had lost their sight as early as 1 year of age, individuals who would have been part of our EB group, thus possibly canceling out opposing effects of thickening in those with an earlier onset and thinning in the others.

In addition to contrasting the EB with the LB, we performed 2 regression analyses to better ascertain the effects the age of onset of blindness and the total duration of blindness would have on CT across the whole cortical surface (see Fig. 4 and Table 3). The results essentially confirmed the findings of the EB-LB contrast, where the thickness of the right cuneus is the most affected by both variables and the thickness of the left lingual and fusiform gyrus also strongly affected. The main difference between both analyses resides in the right lingual gyrus, where CT appeared to only be affected by the age of onset of blindness and not by its duration. These findings highlight 2 important points. The first relates to the impact an early onset of blindness has on occipital CT, suggesting the existence of a critical period after which the microstructure of the occipital cortex is not as plastic as during early childhood. Indeed, the synaptic density of the visual cortex reaches levels greater than that of adults in early infancy through synaptogenetic processes and then gradually decreases to adult levels by approximately 5 years of age through pruning of exuberant connections (Johnson 1997). Importantly, it has been shown that this process of synaptic revision within the visual cortex is dependent on visual input and is interrupted by visual deprivation (Stryker and Harris 1986). Therefore, following the pruning period, the EB may utilize and strengthen these exuberant connections to compensate for the loss of sight through experience-dependent plasticity. This hypothesis is further supported by the second point, the strong positive relationship between the duration of blindness and occipital thickness. Indeed, a longer duration of blindness equates to more time for experience-dependent thickening of the occipital cortex in the blind.

Given the limited spatial resolution of MRI, one can only speculate on which specific layers of visual cortex are particularly affected by or responsible for the observed increased CT. There is reason to believe that the effect is not driven by changes in layer IV, which receives its input from the lateral geniculate nucleus, as several animal studies have shown a reduction of cell numbers and dendrite spines in this layer (Valverde 1968; Windrem and Finlay 1991). This is likely the result of neuronal degeneration processes, which is consistent with the finding of degenerated thalamocortical tracts in humans (Shimony et al. 2006; Ptito et al. 2008). In contrast, the findings of Kingsbury et al. (2002) point to layers II, III, and V as potential sources of the increased occipital thickness. Indeed, the authors showed significant increases in corticocortical connections originating from theses layers in visual thalamus ablated hamsters. Since corticocortical connections are often believed to underlie the crossmodal takeover of the occipital cortex, there is reason to believe that increased connectivity in these layers could be the cause of increased occipital CT in humans.

The above-mentioned process is unlikely to occur in the LB as the occipital cortex is most likely hardwired through visual experience. In addition, the finding of occipital cortical thinning probably reflects neuronal degeneration resulting from disuse of the visual system. This finding is consistent with the functional neuroimaging literature, showing that the LB do not tend to recruit the formerly visual system for nonvisual processing to the same extent as the EB do (see Voss et al. 2010). Correspondingly, the LB have rarely been shown to benefit from heightened sensory abilities, again potentially testifying to the reduced neural resources available to them to carry out nonvisual tasks when compared with EB individuals.

Occipital CT as a Predictor of Auditory Performance

The established link between occipital neural activity in blind individuals and the ability to perform auditory tasks (Röder et al. 2002; Gougoux et al. 2005; Collignon et al. 2007; Stevens et al. 2007) begs the question of whether or not the thickening of the occipital cortex in blind individuals is related to the crossmodal neuroplastic changes that follow visual deprivation. Until now, there has been no direct evidence demonstrating that the occipital thickening is an adaptive and functional consequence of crossmodal plasticity. To address this issue, we carried out regression analyses between measures of CT across the whole brain of blind individuals and their individual performance scores on auditory behavioral tasks. We found that occipital CT strongly predicts behavioral scores on a pitch discrimination task and a melody discrimination task. These results, particularly those relating to the transposed melody task, differ from the finding that CT of the intraparietal sulcus and the superior temporal gyrus are the best predictors of performance on the same task in sighted individuals (Foster and Zatorre 2010b). This is indicative of how crossmodal plasticity not only alters the functioning and the neural computations carried out in the occipital cortex of blind individuals but also affects the neuroanatomical development of the occipital cortex. These structural changes are likely to play a determining role in how the occipital cortex becomes responsive to nonvisual input, which in turn enable the development of heightened abilities in nonvisual modalities.

Finally, it is of interest that the regions where CT best predicted performance on the auditory tasks (cuneus and surrounding regions) overlap only in part with the regions that distinguished the groups in terms of CT (particularly the left lingual gyrus). This is likely because group contrasts are unspecific and hence reveal any differences that exist, whereas the use of performance as a regressor ensures task specificity, revealing only the regions showing a specific relationship with the computations elicited by the task. Similarly, functional neuroimaging studies of blind individuals have often presented the same pattern of results, where the regions whose activity best predicted performance did not always overlap with regions where a difference in activity was observed via group contrasts (Gougoux et al. 2005; Voss et al. 2008).

In conclusion, the present findings confirm previous results showing thicker occipital cortex in the EB compared with sighted controls. The novel finding here is the demonstration that the CT of occipital areas in blind subjects is directly related to auditory behavioral enhancements. This is one of the first demonstrations that anatomical changes associated with sensory deprivation are directly related to behavioral performance and hence support the idea that these anatomical features reflect adaptive compensatory plasticity.

Funding

Canadian Institutes of Health Research (CIHR) (grant #14995 and #11541 to R.J.Z.). CIHR postdoctoral fellowship to P.V.

We thank all the individuals that volunteered to participate in this study. We also thank the Nazareth and Louis-Braille Institute (NLBI) for its assistance in recruiting blind participants. We thank Dr Alan Evans for making the CIVET pipeline available to us. We thank Marc Bouffard and Patrick Bermudez for their assistance in running many of the image preprocessing steps and Nick Foster for making the auditory tasks available to us. We also would like to thank the staff at the McConnell Brain Imaging Center for their assistance during the scanning procedures. Conflict of Interest: None declared.

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