Fine-grained descriptions of brain connectivity are fundamental for understanding how neural information is processed and relayed across spatial scales. Prior investigations of the mouse brain connectome have employed discrete anatomical parcellations, limiting spatial resolution and potentially concealing network attributes critical to the organization of the mammalian connectome. Here we provide a voxel-level description of the network and hierarchical structure of the directed mouse connectome, unconstrained by regional partitioning. We show that integrative hub regions can be directionally segregated into neural sinks and sources, defining a hierarchical axis. We describe a set of structural communities that spatially reconstitute previously described fMRI networks of the mouse brain, and document that neuromodulatory nuclei are strategically wired as critical orchestrators of inter-modular and network communicability. Notably, like in primates, the directed mouse connectome is organized along two superimposed cortical gradients reflecting unimodal-transmodal functional processing and a modality-specific sensorimotor axis. These structural features can be related to patterns of intralaminar connectivity and to the spatial topography of dynamic fMRI brain states, respectively. Together, our results reveal a high-resolution structural scaffold linking mesoscale connectome topography to its macroscale functional organization, and create opportunities for identifying targets of interventions to modulate brain function in a physiologically-accessible species.
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