Asymmetric Synaptic Plasticity Provides an Attractor-Based Mechanism for θ-γ Coupling and Pathological Synchronization.

Abstract

Short-term synaptic plasticity continuously reshapes the balance between excitation and inhibition, yet most population models assume that excitatory and inhibitory synapses share similar short-term dynamics. Experimental studies, however, have shown that inhibitory synapses typically exhibit stronger short-term depression (STD) than recurrent excitatory connections. Here, we investigate how this cell-type-specific asymmetry influences cortical population dynamics by combining a neural mass model with large-scale spiking network simulations. We show that asymmetric inhibitory STD qualitatively changes the attractor structure of the network, generating a bistable regime that is absent under the conventional symmetric assumption. Within this regime, endogenous finite-size fluctuations drive spontaneous transitions between a stable focus and a stable limit cycle, giving rise to metastable dynamics. The asymmetric paradigm exhibits θ-γ phase-amplitude coupling of strength similar to that of the symmetric one, although it arises from fundamentally different dynamics. We further show that slowing synaptic recovery progressively eliminates this bistable regime, leading to persistent hypersynchronous oscillations and reduced phase-amplitude coupling. These results identify asymmetric inhibitory STD as a mechanism that reshapes cortical attractor dynamics and suggest how altered synaptic recovery may contribute to pathological network activity.