Topological Origin of the Diversity of Timescales in Recurrent Neural Circuits

TL;DR

This paper develops a theoretical framework linking the heterogeneity in neural connectivity to diverse timescales of neural activity, explaining how network topology influences neural dynamics and computation.

Contribution

It introduces a heterogeneous dynamical mean-field theory for recurrent networks with tunable degree heterogeneity, revealing how topology induces timescale diversity and affects network stability.

Findings

Degree heterogeneity induces a broad distribution of activity timescales.

Hubs in the network act as integrators for slow input components.

The model explains the observed correlation between neuron in-degree and timescale in mouse cortex.

Abstract

Structural and functional heterogeneity are hallmarks of cortical circuits, from broad degree distributions in the mouse connectome to diverse intrinsic neuronal timescales. Yet a mechanistic link between connectivity heterogeneity and functional diversity is lacking. To bridge this gap, we introduce a random recurrent network in which connectivity is generated by a configuration model with tunable degree heterogeneity and synaptic weights exhibiting varying levels of correlation. Using generating-functional methods, we derive a heterogeneous dynamical mean-field theory (hDMFT) with degree-conditioned stochastic dynamics. The theory shows that the interaction of partial symmetry in the weights and degree heterogeneity induces a non-Markovian memory term in the form of an emergent self-coupling whose strength scales with degree and produces a broad distribution of activity timescales. We obtain analytic stability criteria demonstrating that degree heterogeneity lowers the critical gain and localizes unstable modes onto hubs. The resulting rich dynamical landscape includes silent, chaotic, and multistable regimes, which we uncover via spectral, replica, and Lyapunov exponent analyses. We highlight the computational benefits of the observed timescale heterogeneity by revealing that, under an external input drive featuring a broadband spectrum, slow hub neurons act as integrators, demixing slow input components. Finally, instantiating the model with the empirically measured topology from the MICrONS cubic-millimeter mouse connectome explains the broad range of single-neuron timescales and their positive correlation with in-degree observed in resting-state recordings. Our results provide a mechanistic link between connectome topology, neural dynamics, and computation, identifying hubs in partially symmetric networks as a natural substrate for multiplexed processing across timescales.