Gradients of function between sensory drive and working memory in human frontal cortex
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The coordination of sensory processing and working memory (WM) is fundamental to cognition. Spatial organization of sensory processing and WM is known to be broadly distributed across the cortex, but finer-scale organization at the interfaces between these functions remains understudied. Although the notion of sharp parcellations of cortex into distinct functional modules dominates the field, a growing body of works support graded changes in function and anatomy in some cortical zones. Based on this and potential advantages of gradient organizational structure in frontal cortex, we hypothesized that sensory-WM interfaces in the frontal cortex are gradient-like, not boundary-like. We examined twenty bilateral cortical regions that participate in visual/auditory WM tasks. In five frontal cortical regions, group-level WM activation overlapped with sensory drive, but was spatially shifted. We compared subject-level (N=20) boundary and gradient models of change in function. Strong individual-level evidence for sensory-WM gradients was observed in pre-supplementary motor area, ventral premotor cortex, and anterior insula in both modalities and in dorsal premotor cortex for visual WM. Conversely, dorsolateral pre-frontal cortex yielded mixed results, favored distinct WM and sensory regions in the left hemisphere, and gave some evidence for gradients in the right hemisphere. These results provide evidence that sensory and WM regions in frontal cortex are largely not distinct with sharp boundaries at their interfaces but instead bleed into each other to form local rostral-caudal sensory-WM gradients. We speculate these gradients may allow efficient interfacing between sensory and WM representations, and/or fine-grained, task-dependent shifting between bottom-up sensory and top-down influences.
Significance Statement
Cognitive neuroscience strongly adheres to the notion that the cerebral cortex is functionally parcellated into distinct regions with sharp anatomical boundaries. In contrast, modern neuroanatomical analysis indicates that, across cortex, boundaries vary from abrupt to gradual. Here, we examine the interface between sensory drive and working memory representations and observe meso-scale gradients (∼ 1 cm) in multiple regions of human frontal cortex. The observed functional gradients span regions previously defined as having sharp boundaries. Gradients offer potential benefits for working memory to balance faithful encoding of stimulus information with cognitive priorities necessary to support behavioral goals. The findings have important implications for understanding the neural architecture of working memory and more broadly for the functional parcellation of the cerebral cortex.