Modulation of ventral prefrontal cortex functional connections reflects the interplay of cognitive processes and stimulus characteristics

Abstract

Emerging ideas of brain function emphasize the context-dependency of regional contributions to cognitive operations, where the function of a particular region is constrained by its pattern of functional connectivity. We used functional magnetic resonance imaging to examine how modality of input (auditory or visual) affects prefrontal cortex (PFC) functional connectivity for simple working memory tasks. The hypothesis was that PFC would show contextually dependent changes in functional connectivity in relation to the modality of input despite similar cognitive demands. Participants were presented with auditory or visual bandpass-filtered noise stimuli, and performed 2 simple short-term memory tasks. Brain activation patterns independently mapped onto modality and task demands. Analysis of right ventral PFC functional connectivity, however, suggested these activity patterns interact. One functional connectivity pattern showed task differences independent of stimulus modality and involved ventromedial and dorsolateral prefrontal and occipitoparietal cortices. A second pattern showed task differences that varied with modality, engaging superior temporal and occipital association regions. Importantly, these association regions showed nonzero functional connectivity in all conditions, rather than showing a zero connectivity in one modality and nonzero in the other. These results underscore the interactive nature of brain processing, where modality-specific and process-specific networks interact for normal cognitive operations.

Figure 1.

Behavior measures for the 4 experimental tasks. (A) Mean proportion correct. (B) Mean threshold. (C) Mean reaction time. Error bars show standard error.

Figure 2.

(A) Singular image for the nonrotated task PLS modality LV. On the singular image, time from stimulus onset, expressed in seconds, is indicated on the y-axis of the singular image. The approximate location of the axial slice in MNI atlas space is indicated on the x-axis. Voxels in the image are highlighted according to the magnitude of the ratio of their parameter estimate to the bootstrap-estimated standard error (bootstrap ratio). The singular image is superimposed on a T₁-weighted MRI template. On the singular image, brain regions in blue are more active during visual tasks, and brain regions in yellow are more active during auditory tasks. (B) HRF from BA 22, identified in the modality LV as more active during the visual tasks (MNI template coordinates: x = 68, y = −40, z = 12). Auditory tasks are shown in blue and visual in red to emphasize that change in response was greater for auditory than visual tasks. Responses are expressed as percent change from stimulus onset (T = 0) and are averaged across subjects (±SE).

Figure 3.

(A) Singular image for the nonrotated task PLS task demands LV. Brain regions in blue are more active during control tasks, and brain regions in yellow are more active during experimental tasks. White circle indicates the approximate location of the BA 47 seed voxel used in the seed PLS analysis. (B) Hemodynamic response function from the seed voxel circled in (A) (MNI template coordinates: x = 44, y = 32, z = −24). The averaged response for experimental tasks is shown in blue, and averaged response for control tasks are shown in red. Responses are expressed as percent change from stimulus onset (T = 0) and are averaged across subjects (±SE).

Figure 4.

Singular image (top) and correlation between brain scores and the BA 47 seed voxel for the interaction LV from seed PLS. The singular image identifies peak voxels showing a different pattern of correlations with the BA 47 voxel across tasks. The correlation bar graph captures the task-dependent changes in the correlation with the seed voxel of the areas identified in the singular image. The error bars indicate the 95% confidence interval derived from bootstrap estimation.

Figure 5.

Correlation profiles for selected voxels identified in the interaction LV as shown in Figure 4. Correlations are plotted across the time window from stimulus onset (T = 0). (A) The correlation for left superior temporal cortex (BA 21, MNI template coordinates: x = −60, y = −48, z = 0) and panel B shows medial PFC (BA 10, MNI template coordinates: x = 16, y = 64, z = 4).

Figure 6.

Singular image (top) and correlation between brain scores and the BA 47 seed voxel for the task demands LV from seed PLS. The singular image identifies peak voxels showing a different pattern of correlations with the BA 47 voxel across tasks. The correlation bar graph captures the task-dependent changes in the correlation with the seed voxel of the areas identified in the singular image. The error bars indicate the 95% confidence interval derived from bootstrap estimation.

Figure 7.

Correlation profiles for selected voxels identified in from the task demands LV as shown in Figure 6. Correlations are plotted across the time window from stimulus onset (T = 0). (A) The correlation for ventromedial PFC (BA 10, MNI template coordinates: x = 0, y = 60, z = −4); and (B) occipitoparietal cortex (BA 19, MNI template coordinates: x = 16, y = −94, z = 24).