The temporal organization of corticostriatal communications

ABSTRACT The cortex and striatum are linked by hundreds of thousands of structural connections, and the transmission of temporally aligned communications across many of these connections at once is an electrophysiological prerequisite for striatal activation. Despite the importance of communication timing in corticostriatal circuitry, there is little understanding of its system-level organization and properties. To investigate this, we leveraged emerging methods to “temporally unwrap” fMRI data and measure patterns of cortex-striatum node-pair coactivation at frame-wise (i.e., <1 sec) resolution in low head-motion subjects from the Human Connectome Project. First, we identify communities of cortex-striatum node-pairs with preferentially synchronized coactivation patterns. Surprisingly, we find that the map of striatal areas with temporally aligned cortical coactivation patterns does not simply reflect the map of striatal areas with similar cortical connectivity profiles. As a result of the distinct spatial organization of these gradients, striatal nodes connected to similar areas of cortex may nonetheless interact with these cortical areas at different times, and striatal nodes connected to different areas of cortex may nonetheless interact with these areas at similar times. We provide evidence for a possible mechanism driving this divergence: striatal nodes with similar cortical connectivity profiles may have differently timed interactions with cortex if they have different modulatory input profiles (i.e., from the midbrain and thalamus) that differentially gate their responsivity to cortical input. Overall, this blended organization may serve to both increase the repertoire of striatal responses to frontal input and facilitate coordination across functional domains in the temporal dimension. Findings provide a framework to investigate the role of corticostriatal temporal coordination in behavior and disease. SIGNIFICANCE STATEMENT We provide the first systems-level account of temporal communication patterns between cortex-striatum node-pairs, mapping communities of node-pairs with synchronized communication patterns using an emerging fMRI temporal-unwrapping technique and providing evidence for the mechanism that dictates the organization of these communities. Findings have broad implications for our understanding of the functional architecture of corticostriatal circuits.