A time-resolved theory of information encoding in recurrent neural networks

Information encoding in neural circuits depends on how well time-varying stimuli are encoded by neural populations. Slow neuronal timescales, noise and network chaos can compromise reliable and rapid population response to external stimuli. A dynamic balance of externally incoming currents by strong recurrent inhibition was previously proposed as a mechanism to accurately and robustly encode a time-varying stimulus in balanced networks of binary neurons, but a theory for recurrent rate networks was missing. Here, we develop a non-stationary dynamic mean-field theory that transparently explains how a tight balance of excitatory currents by recurrent inhibition improves information encoding. We demonstrate that the mutual information rate of a time-varying input increases linearly with the tightness of balance, both in the presence of additive noise and with recurrently generated chaotic network fluctuations. We corroborated our findings in numerical experiments and demonstrated that recurrent networks with positive firing rates trained to transmit a time-varying stimulus generically use recurrent inhibition to increase the information rate. We also found that networks trained to transmit multiple independent time-varying signals spontaneously form multiple local inhibitory clusters, one for each input channel. Our findings suggest that feedforward excitatory input and local recurrent inhibition-as observed in many biological circuits-is a generic circuit motif for encoding and transmitting time-varying information in recurrent neural circuits.