Facilitating the propagation of spiking activity in feedforward networks by including feedback

Transient oscillations in the network activity upon sensory stimulation have been reported in different sensory areas. These evoked oscillations are the generic response of networks of excitatory and inhibitory neurons (EI-networks) to a transient external input. Recently, it has been shown that this resonance property of EI-networks can be exploited for communication in modular neuronal networks by enabling the transmission of sequences of synchronous spike volleys (‘pulse packets’), despite the sparse and weak connectivity between the modules. The condition for successful transmission is that the pulse packet (PP) intervals match the period of the modules’ resonance frequency. Hence, the mechanism was termed communication through resonance (CTR). This mechanism has three sever constraints, though. First, it needs periodic trains of PPs, whereas single PPs fail to propagate. Second, the inter-PP interval needs to match the network resonance. Third, transmission is very slow, because in each module, the network resonance needs to build-up over multiple oscillation cycles. Here, we show that, by adding appropriate feedback connections to the network, the CTR mechanism can be improved and the aforementioned constraints relaxed. Specifically, we show that adding feedback connections between two upstream modules, called the resonance pair, in an otherwise feedforward modular network can support successful propagation of a single PP throughout the entire network. The key condition for successful transmission is that the sum of the forward and backward delays in the resonance pair matches the resonance frequency of the network modules. The transmission is much faster, by more than a factor of two, than in the original CTR mechanism. Moreover, it distinctly lowers the threshold for successful communication by synchronous spiking in modular networks of weakly coupled networks. Thus, our results suggest a new functional role of bidirectional connectivity for the communication in cortical area networks. Author summary The cortex is organized as a modular system, with the modules (cortical areas) communicating via weak long-range connections. It has been suggested that the intrinsic resonance properties of population activities in these areas might contribute to enabling successful communication. A module’s intrinsic resonance appears in the damped oscillatory response to an incoming spike volley, enabling successful communication during the peaks of the oscillation. Such communication can be exploited in feedforward networks, provided the participating networks have similar resonance frequencies. This, however, is not necessarily true for cortical networks. Moreover, the communication is slow, as it takes several oscillation cycles to build up the response in the downstream network. Also, only periodic trains of spikes volleys (and not single volleys) with matching intervals can propagate. Here, we present a novel mechanism that alleviates these shortcomings and enables propagation of synchronous spiking across weakly connected networks with not necessarily identical resonance frequencies. In this framework, an individual spike volley can propagate by local amplification through reverberation in a loop between two successive networks, connected by feedforward and feedback connections: the resonance pair. This overcomes the need for activity build-up in downstream networks, causing the volley to propagate distinctly faster and more reliably.