Combined Auditory, Tactile, and Visual fMRI Reveals Sensory-Biased and Supramodal Working Memory Regions in Human Frontal Cortex

Abstract

Selectivity for sensory modality characterizes distinct subregions of the human brain, well beyond the primary sensory cortices. We previously identified frontal and posterior cortical regions that are preferentially recruited for visual vs. auditory attention and working memory (WM). Here, we extend our approach to include tactile cognition and to characterize cortical regions recruited by WM in each of three sensory modalities. The joint organization of visual-selective, auditory-selective, tactile-selective, and supramodal WM recruitment within individual subjects has not been fully investigated previously. Male and female human subjects participated in a blocked fMRI task requiring them to perform N-back WM judgements in auditory, visual, or tactile (haptic) modalities. We confirmed our prior reports of multiple visual-biased and auditory-biased frontal lobe regions. We also observed several bilateral tactile-selective regions abutting previously described visual- and auditory-selective regions, including dorsal and ventral precentral sulcus, the postcentral sulcus, and the anterior intraparietal sulcus. Several cortical regions were recruited by WM in all three sensory modalities in individual subjects, including precentral sulcus, inferior frontal sulcus, intraparietal sulcus, anterior insula and pre-supplementary motor area. Supramodal regions exhibited substantial overlap with visual-biased regions in frontal and parietal cortex and comparatively little overlap with tactile- or auditory-biased regions. Lastly, resting-state analyses revealed that auditory-, visual- and tactile-selective WM regions segregate into modality-specific networks that span frontal and posterior cortex. Together, these results shed light on the functional organization of sensory-selective and supramodal regions supporting higher-order cognition. SIGNIFICANCE STATEMENTUsing within-subject fMRI analyses of three different sensory modalities, we identify the fine-scale architecture of sensory-biased and supramodal working memory structures within human frontal cortex. Sixteen bilateral frontal lobe regions are identified: five auditory-biased, four visual-biased, two tactile-biased, and five multiple-demand / supramodal regions. These parcels are largely distinct with the notable exception that the visual-biased regions each partially overlap with supramodal regions, suggesting a tight link between visual and supramodal working memory representations. Sensory-biased frontal lobe regions form modality-specific networks with traditionally-identified posterior sensory cortical regions. The findings demonstrate a pervasive role for sensory modality in the functional organization of frontal cortex and offer a fine-scale parcellation of the human frontal lobe regions supporting working memory.