Frequency Selectivity of Voxel-by-Voxel Functional Connectivity in Human Auditory Cortex

Abstract

While functional connectivity in the human cortex has been increasingly studied, its relationship to cortical representation of sensory features has not been documented as much. We used functional magnetic resonance imaging to demonstrate that voxel-by-voxel intrinsic functional connectivity (FC) is selective to frequency preference of voxels in the human auditory cortex. Thus, FC was significantly higher for voxels with similar frequency tuning than for voxels with dissimilar tuning functions. Frequency-selective FC, measured via the correlation of residual hemodynamic activity, was not explained by generic FC that is dependent on spatial distance over the cortex. This pattern remained even when FC was computed using residual activity taken from resting epochs. Further analysis showed that voxels in the core fields in the right hemisphere have a higher frequency selectivity in within-area FC than their counterpart in the left hemisphere, or than in the noncore-fields in the same hemisphere. Frequency-selective FC is consistent with previous findings of topographically organized FC in the human visual and motor cortices. The high degree of frequency selectivity in the right core area is in line with findings and theoretical proposals regarding the asymmetry of human auditory cortex for spectral processing.

Keywords: frequency selectivity; functional connectivity; functional magnetic resonance imaging; functional organization; human auditory cortex.

Figure 1.

Stimulus presentation and fMRI sparse sampling. Functional images were acquired every 9 s. Within a block of 4 acquisitions, each of the first 2 acquisitions was preceded by a 4-s stimulus sequence (pure tones 187 ms in duration presented every 250 ms). Frequency conditions of the pure tones were randomly changed across blocks as indicated herein as f4, f2, and f7 which correspond to 573.8, 338.8, and 4723.1 Hz.

Figure 2.

Preferred frequency map, FC map, and voxel-by-voxel FC as a function of preferred frequency. (A) Preferred frequency maps of 3 slices (in-plane; z = 7, 8, and 9) in a representative participant (top) and corresponding FC maps of 3 seed voxels (bottom). Top: Closed curves indicate the core-fields regions and black crosshairs locate the 3 seed voxel locations in each slice. Bottom: FC in each panel is computed by correlating the residual activity of the seed voxel and the remaining (target) voxels. (B) Voxel-by-voxel FC as a function of preferred frequency from each slice in the 3 columns. Gray dots mark FC of every pair of voxels in each slice and black curves are the average of preferred frequency binned with 1-octave width. Red vertical lines indicate the preferred frequency of the seed voxels. (C) Voxel-by-voxel FC as a function of difference in preferred frequency (Δ preferred frequency) for each slice in the 3 columns. The consequence of taking Δ preferred frequency is that the preferred frequency of all seed voxels is aligned to 0 (red vertical lines). Black curves indicate the average of each bin of Δ preferred frequency). (D) Pooled data from the 3 slices. The FC of individual pairs was pooled and binned. Note that this figure shows only the scheme of the method with 3 exemplary seed voxels.

Figure 3.

Frequency-selective FC within and between hemispheres. (A) FC matrix as a function of preferred frequency of the seed and target voxels. Preferred frequencies were binned in 1 octave steps. Left (L–L): FC of the voxels within the left hemisphere; center (R–R): FC within the right hemisphere; right (L-R): FC between the hemispheres. (B) FC as a function of preferred frequency of target voxels. Each of the 8 curves corresponds to averaged data across seed voxels that prefer similar frequencies of 1 octave range. Error bars are shown only at the data points of preferred frequency of seed voxels for clarity. Note that each curve in B corresponds to each row of the matrix that is aligned along the column. Error bars represent ±1 STE of the mean across subjects. (C) FC as a function of difference in preferred frequency (Δ preferred frequency). In B and C, each column corresponds to the ones in (A) These graphs indicate that intervoxel FC is higher for voxels with more similar frequency tuning.

Figure 4.

FC as a function of difference in preferred frequency within and between hemispheres in individual participants. Data from the 7 individual participants are plotted in the same format as Figure 3C. All 7 individuals clearly show decreasing FC as a function of increasing distance of voxel frequency preference.

Figure 5.

Intervoxel distance effect. (A) Temporal correlation of residual activity as a function of intervoxel distance in the pure-tone sensitive ROIs (ROIs; black), the gray matter outside the auditory ROIs (GM; dark gray) and the white matter (WM; light gray). Error bars represent ±1 STE across subjects. (B) FC in the ROIs predicted by intervoxel distance in the GM. The inset shows the FC matrix as in Figure 3A.

Figure 6.

Distance-corrected functional connectivity. Distance-corrected frequency-selective FC within the left hemisphere (L–L), within the right hemisphere (R–R) and between the hemispheres (L–R) is plotted in the same format as in Figure 3. The distance effect is corrected by subtracting the FC predicted by the distance in the gray matter from the original FC. The pattern of corrected results is similar to the principal effects shown in Figure 3.

Figure 7.

Frequency-selective FC in resting epochs. (A) FC in resting epochs as a function of difference in preferred frequency (Δ preferred frequency). (B) (A) FC in resting epochs as a function of Δ preferred frequency after regressing out stimulus conditions. Note that only the fourth TRs of the blocks were used to compute FC. The pattern obtained in the resting epochs replicates that observed in the other conditions.

Figure 8.

Frequency-selective FC in within and between core and noncore fields. FC is plotted as a function of difference in preferred frequency of voxels (Δ frequency) within and between the core and noncore fields within the hemispheres (A) and between the hemispheres (B). Note the steeper slope of the function corresponding to voxels within the right core region, compared with all the rest.

Figure 9.

Comparison of within-area FC between areas. (A) Frequency selectivity of residual FC within 4 ROIs (LC: left core; RC: right core; LN: left noncore; and RN: right noncore). (B) Frequency selectivity of resting-epoch FC within 4 ROIs (LC: left core; RC: right core; LN: left noncore; and RN: right noncore). The frequency selectivity is highest for the right core compared with the other regions.