Asynchronous and coherent dynamics in balanced excitatory-inhibitory populations

ABSTRACT Dynamic excitatory-inhibitory (E-I) balance is a paradigmatic mechanism invoked to explain the irregular low firing activity observed in the cortex. However, we will show that the E-I balance can be at the origin of other regimes observable in the brain. The analysis is performed by combining extensive simulations of sparse E-I networks composed of N spiking neurons with analytical investigations of low dimensional neural mass models. The bifurcation diagrams, derived for the neural mass model, allow to classify the possible asynchronous and coherent behaviours emerging in balanced E-I networks with structural heterogeneity for any finite in-degree K . In the limit N >> K >> 1 both supra and sub-threshold balanced asynchronous regimes can be observed in our system. Due to the heterogeneity the asynchronous states are characterized by the splitting of the neurons in three groups: silent, fluctuation and mean driven. These features are consistent with experimental observations reported for heterogeneous neural circuits. The coherent rhythms observed in our system can range from periodic and quasi-periodic collective oscillations (COs) to coherent chaos. These rhythms are characterized by regular or irregular temporal fluctuations joined to spatial coherence somehow similar to coherent fluctuations observed in the cortex over multiple spatial scales. The COs can emerge due to two different mechanisms. A first mechanism similar to the pyramidal-interneuron gamma (PING) one, usually invoked for the emergence of γ -oscillations. The second mechanism is intimately related to the presence of current fluctuations, which sustain COs characterized by an essentially simultaneous bursting of the two populations. We observe period-doubling cascades involving the PING-like COs finally leading to the appearance of coherent chaos. Fluctuation driven COs are usually observable in our system as quasi-periodic collective motions characterized by two incommensurate frequencies. However, for sufficiently strong current fluctuations we report a novel mechanism of frequency locking among collective rhythms promoted by these intrinsic fluctuations. Our analysis suggest that despite PING-like or fluctuation driven COS are observable for any finite in-degree K , in the limit N >> K >> 1 these solutions finally result in two coexisting balanced regimes: an asynchronous and a fully synchronized one.