Functional correlates of the anterolateral processing hierarchy in human auditory cortex

Abstract

Converging evidence supports the hypothesis that an anterolateral processing pathway mediates sound identification in auditory cortex, analogous to the role of the ventral cortical pathway in visual object recognition. Studies in nonhuman primates have characterized the anterolateral auditory pathway as a processing hierarchy, composed of three anatomically and physiologically distinct initial stages: core, belt, and parabelt. In humans, potential homologs of these regions have been identified anatomically, but reliable and complete functional distinctions between them have yet to be established. Because the anatomical locations of these fields vary across subjects, investigations of potential homologs between monkeys and humans require these fields to be defined in single subjects. Using functional MRI, we presented three classes of sounds (tones, band-passed noise bursts, and conspecific vocalizations), equivalent to those used in previous monkey studies. In each individual subject, three regions showing functional similarities to macaque core, belt, and parabelt were readily identified. Furthermore, the relative sizes and locations of these regions were consistent with those reported in human anatomical studies. Our results demonstrate that the functional organization of the anterolateral processing pathway in humans is largely consistent with that of nonhuman primates. Because our scanning sessions last only 15 min/subject, they can be run in conjunction with other scans. This will enable future studies to characterize functional modules in human auditory cortex at a level of detail previously possible only in visual cortex. Furthermore, the approach of using identical schemes in both humans and monkeys will aid with establishing potential homologies between them.

Figure 1.

Three functionally discrete regions identified in human auditory cortex using BOLD imaging and sounds with different spectral complexity. A, Example stimuli used. Subjects were presented with PT, BPN, and species-specific vocalization (VOW) stimuli, based on the ability to differentiate core, belt, and parabelt using these stimulus classes in previous nonhuman primate studies. B, Random-effects group analysis (n = 13). A hierarchy of three functionally separable regions is clearly visible in each hemisphere. PT activation (blue) was centered on Talairach coordinates [48, −20, 7] and [−45, −24, 8]. Adjacent voxels responded to BPN but not PT (yellow), and further regions of cortex responded to VOW, but not BPN or PT. Minimum t value for all conditions is 9.8.

Figure 2.

A progression from simple to complex selectivity in the anterolateral direction. A BPN > PT contrast (yellow) yielded activation largely restricted to areas adjacent to the medial and lateral extents of Heschl's gyrus in each hemisphere. The VOW > BPN contrast yielded significant activation in anterolateral aspects of the superior temporal gyrus. The two contrasts share little overlap (orange). Thresholds were p < 0.05 for both contrasts, and the sizes and Talairach coordinates of the resulting clusters are reported in Table 1.

Figure 3.

Functional organization in individual subjects. The three functionally differentiable regions identified in the group were also consistently identified in all 13 subjects in each hemisphere. Three representative subjects are shown here. Thresholds varied by subject and are reported in Table 2.

Figure 4.

Quantification of single-subject analysis. A, Activation volume by stimulus condition across subjects. B, Quantification of the spatial overlap between stimulus conditions. Matrix values indicate the percentage of voxels within the region of interest displayed along the horizontal axis that are also activated by the conditions shown along the vertical axis. Dark colors indicate a low percentage of overlap between conditions (i.e., few active voxels in common), while light colors indicate a high percentage of overlap. C, Average location of active voxels for each condition across subjects (medial–lateral coordinates are reported as absolute values because both hemispheres were collapsed). *p < 0.05, **p < 0.01, ***p < 0.001.

Figure 5.

Benefits of functional localization in individual subjects compared to group analysis. A, In three example subjects, the mismatch between PT activation defined by the group analysis and the single-subject is apparent. B, Fraction of voxels in single-subject ROIs that are also present in the group-defined ROI. Minimum t value was 9.8 for the group, and single-subject values are as listed in Table 2.

Figure 6.

Organization based on spectral complexity. In an additional control experiment activation by WN was compared with activation by PT, BPN, and VOW. The results demonstrate that the regional differences do not merely depend on increasing bandwidth, but depend instead on spectral complexity, similar to the monkey. Activation volume across subjects (n = 7) for each stimulus condition is shown. Minimum t values for each subject are those listed in Table 2. *p < 0.05, **p < 0.01, ***p < 0.001.