A reservoir of timescales emerges in recurrent circuits with heterogeneous neural assemblies

Abstract

The temporal activity of many physical and biological systems, from complex networks to neural circuits, exhibits fluctuations simultaneously varying over a large range of timescales. Long-tailed distributions of intrinsic timescales have been observed across neurons simultaneously recorded within the same cortical circuit. The mechanisms leading to this striking temporal heterogeneity are yet unknown. Here, we show that neural circuits, endowed with heterogeneous neural assemblies of different sizes, naturally generate multiple timescales of activity spanning several orders of magnitude. We develop an analytical theory using rate networks, supported by simulations of spiking networks with cell-type specific connectivity, to explain how neural timescales depend on assembly size and show that our model can naturally explain the long-tailed timescale distribution observed in the awake primate cortex. When driving recurrent networks of heterogeneous neural assemblies by a time-dependent broadband input, we found that large and small assemblies preferentially entrain slow and fast spectral components of the input, respectively. Our results suggest that heterogeneous assemblies can provide a biologically plausible mechanism for neural circuits to demix complex temporal input signals by transforming temporal into spatial neural codes via frequency-selective neural assemblies.