Spindle Oscillation Emerges at the Critical State of the Electrically Coupled Network in Thalamic Reticular Nucleus

Abstract

Spindle oscillation is a waxing-and-waning neural oscillation observed in the brain, initiated at the thalamic reticular nucleus (TRN) and typically occurring at 7 – 15 Hz. Recent experiments revealed that in the adult brain, electrical synapses, rather than chemical synapses, are dominating between TRN neurons, indicating that the traditional view of spindle generation via chemical synapses in the TRN needs to be revised. Here, based on the known experimental data, we develop a computational model of the TRN network, in which heterogeneous neurons are connected by electrical synapses. The model consists of two driving forces competing to shape the network dynamics: electrical synapses tend to synchronize neurons, while heterogeneity tends to desynchronize neurons. We demonstrate that the interplay between two forces leads to a network state where multiple synchronized clusters with slightly different oscillation frequencies coexist. In this state, the superposition of neuronal activities gives rise to spindle oscillation, as observed in local field potentials in experiments. Notably, we discover that when TRN neurons generate spindle oscillation, the network operates at the critical state, known for facilitating efficient information processing in complex systems. Our study sheds light on the underlying mechanism of spindle oscillation and its functional significance in neural information processing.