Relevance of spectral cues for auditory spatial processing in the occipital cortex of the blind

Abstract

We have previously shown that some blind individuals can localize sounds more accurately than their sighted counterparts when one ear is obstructed, and that this ability is strongly associated with occipital cortex activity. Given that spectral cues are important for monaurally localizing sounds when one ear is obstructed, and that blind individuals are more sensitive to small spectral differences, we hypothesized that enhanced use of spectral cues via occipital cortex mechanisms could explain the better performance of blind individuals in monaural localization. Using positron-emission tomography (PET), we scanned blind and sighted persons as they discriminated between sounds originating from a single spatial position, but with different spectral profiles that simulated different spatial positions based on head-related transfer functions. We show here that a sub-group of early blind individuals showing superior monaural sound localization abilities performed significantly better than any other group on this spectral discrimination task. For all groups, performance was best for stimuli simulating peripheral positions, consistent with the notion that spectral cues are more helpful for discriminating peripheral sources. PET results showed that all blind groups showed cerebral blood flow increases in the occipital cortex; but this was also the case in the sighted group. A voxel-wise covariation analysis showed that more occipital recruitment was associated with better performance across all blind subjects but not the sighted. An inter-regional covariation analysis showed that the occipital activity in the blind covaried with that of several frontal and parietal regions known for their role in auditory spatial processing. Overall, these results support the notion that the superior ability of a sub-group of early-blind individuals to localize sounds is mediated by their superior ability to use spectral cues, and that this ability is subserved by cortical processing in the occipital cortex.

Keywords: PET; auditory spatial processing; blindness; crossmodal reorganization; functional neuroimaging; spectral cues; visual cortex plasticity.

Figure 1

Spectrum analysis. Here are illustrated the spectrograms of two sample stimuli used in the discrimination task. Specifically, these two stimuli were often compared to one another when the reference (first) stimulus was simulating +15° azimuth. As can be seen, the differences in spectral content between both sounds are very subtle, consistent with the difficulty level of the task.

Figure 2

Behavioral performance for the spectral discrimination task. Here are plotted the performance of each group across the different azimuthal regions tested. The EBSP group significantly outperformed all other groups while all other comparisons were non-significant. Noteworthy is the finding that performance is best for spectral cues corresponding to peripheral positions, for all groups, consistent with the notion that spectral cues are most beneficial for peripheral auditory space in the horizontal plane.

Figure 3

Task-related contrasts for each group. Illustrated here are the occipital (de)activation foci generated by the task-related contrasts (task-control baseline) for each group (see Table 1 for complete list of significantly activated brain regions).

Figure 4

Intergroup contrasts. Illustrated here are the differences in occipital activation between groups, relative to baseline, obtained via intergroup contrast analyses (see Table 2 for complete list of significant differentially activated brain regions).

Figure 5

Independent voxel-wise covariation analysis in the blind. The percentage of CBF change (relative to baseline) significantly correlated with performance of blind subjects scores in two regions: (A) left lingual gyrus (tal. coord.: −8, −102, −5) and (B) the left precentral gyrus/inferior frontal gyrus (tal. coord.: −50, −2, 24). The left column illustrates the average percent CBF change per group for each region relative to baseline while the middle column shows sagittal and horizontal slices highlighting the two regions. The right column illustrates the correlation between percent CBF change and performance across all blind subjects. Note that the data points for sighted subjects are also included in the scatter plot for comparison purposes, but were not included in the correlation analysis.

Figure 6

Inter-regional correlation analysis. Illustrated here are the regions in which the activity covaried with that of the activity of a user defined seed region: the left lingual gyrus centered at tal. coord.: (−8, −102, −5). The seed point corresponds to the voxel whose activity most correlated with performance across all blind individuals (see Figure 5). Four peaks reached above threshold values for significant covariation: right inferior frontal gyrus (orange arrow), right middle frontal gyrus (yellow arrow, circle), left middle frontal gyrus (white arrow, circle), and right superior parietal lobule (green arrow, circle).