Nonlinear transient amplification in recurrent neural networks with short-term plasticity

Abstract To rapidly process information, neural circuits have to amplify specific activity patterns transiently. How the brain performs this nonlinear operation remains elusive. Hebbian assemblies are one possibility whereby symmetric excitatory connections boost neuronal activity. However, such Hebbian amplification is often associated with dynamical slowing of network dynamics, non-transient attractor states, and pathological run-away activity. Feedback inhibition can alleviate these effects but typically linearizes responses and reduces amplification gain. At the same time, other alternative mechanisms rely on asymmetric connectivity, in conflict with the Hebbian doctrine. Here we propose nonlinear transient amplification (NTA), a plausible circuit mechanism that reconciles symmetric connectivity with rapid amplification while avoiding the above issues. NTA has two distinct temporal phases. Initially, positive feedback excitation selectively amplifies inputs that exceed a critical threshold. Subsequently, short-term plasticity quenches the run-away dynamics into an inhibition-stabilized network state. By characterizing NTA in supralinear network models, we establish that the resulting onset transients are stimulus selective and well-suited for speedy information processing. Further, we find that excitatory-inhibitory co-tuning widens the parameter regime in which NTA is possible. In summary, NTA provides a parsimonious explanation for how excitatory-inhibitory co-tuning and short-term plasticity collaborate in recurrent networks to achieve transient amplification.