Modeling the influences of non-local connectomic projections on geometrically constrained cortical dynamics

Abstract: The function and dynamics of the cortex are fundamentally shaped by the specific wiring configurations of its constituent axonal fibers, also known as the connectome. However, many dynamical properties of macroscale cortical activity are well captured by instead describing the activity as propagating waves across the cortical surface, constrained only by the surface's two-dimensional geometry. It thus remains an open question why the local geometry of the cortex can successfully capture macroscale cortical dynamics, despite neglecting the specificity of Fast-conducting, Non-local Projections (FNPs) which are known to mediate the rapid and non-local propagation of activity between remote neural populations. Here we address this question by developing a novel mathematical model of macroscale cortical activity in which cortical populations interact both by a continuous sheet and by an additional set of FNPs wired independently of the sheet's geometry. By simulating the model across a range of connectome topologies, external inputs, and timescales, we demonstrate that the addition of FNPs strongly shape the model dynamics of rapid, stimulus-evoked responses on fine millisecond timescales ($\lessapprox 30~\text{ms}$), but contribute relatively little to slower, spontaneous fluctuations over longer timescales ($> 30~\text{ms}$), which increasingly resemble geometrically constrained dynamics without FNPs. Our results suggest that the discrepant views regarding the relative contributions of local (geometric) and non-local (connectomic) cortico-cortical interactions are context-dependent: While FNPs specified by the connectome are needed to capture rapid communication between specific distant populations (as per the rapid processing of sensory inputs), they play a relatively minor role in shaping slower spontaneous fluctuations (as per resting-state functional magnetic resonance imaging).