Co-representation of functional brain networks is shaped by cortical myeloarchitecture and reveals individual behavioral ability.

Large-scale functional networks are spatially distributed in the human brain. Despite recent progress in differentiating the functional roles of specific brain networks, how the brain navigates the spatial coordination among them and the biological relevance of this coordination is still not fully understood. Capitalizing on canonical individualized networks derived from functional MRI data, we proposed a new concept, i.e., co-representation of functional brain networks, to delineate the spatial coordination among them. To further quantify the co-representation pattern, we defined two indexes, i.e., the co-representation specificity (CoRS) and intensity (CoRI), for separately measuring the extent of specific and average expression of functional networks at each brain location by using the data from both sexes. We found that the identified pattern of co-representation was anchored by cortical regions with three types of cytoarchitectural classes along a sensory-fugal axis, including, at the first end, primary (idiotypic) regions showing high CoRS, at the second end, heteromodal regions showing low CoRS and high CoRI, at the third end, paralimbic regions showing low CoRI. Importantly, we demonstrated the critical role of myeloarchitecture in sculpting the spatial distribution of co-representation by assessing the association with the myelin-related neuroanatomical and transcriptomic profiles. Furthermore, the significance of manifesting the co-representation was revealed in its prediction of individual behavioral ability. Our findings indicated that the spatial coordination among functional networks was built upon an anatomically configured blueprint to facilitate neural information processing, while advancing our understanding of the topographical organization of the brain by emphasizing the assembly of functional networks. Significance Statement The human brain is functionally organized into large-scale functional networks that are highly structured in space and time. How these networks are coordinated by the physical embedding of the brain in space is still unclear. We propose the co-representation of functional networks, as a new concept accompanied by two quantitative indexes, to characterize the spatial coordination between networks. We find that the co-representation pattern was anchored along a sensory-fugal axis of cytoarchitectural classes. This pattern is shaped by the cortical myeloarchitecture, demonstrated by both neuroanatomical and transcriptomic data. The manifestation of co-representation is a reliable predictor of individual behavioral performance. Our findings indicate that the co-representation of functional networks is built upon an anatomically configured blueprint to support neurocognitive computations.