Feedback stabilizes propagation of synchronous spiking in cortical neural networks

Precisely timed action potentials related to stimuli and behavior have been observed in the cerebral cortex. However, information carried by the precise spike timing has to propagate through many cortical areas, and noise could disrupt millisecond precision during the transmission. Previous studies have demonstrated that only strong stimuli that evoke a large number of spikes with small dispersion of spike times can propagate through multilayer networks without degrading the temporal precision. Here we show that feedback projections can increase the number of spikes in spike volleys without degrading their temporal precision. Feedback also increased the range of spike volleys that can propagate through multilayer networks. Our work suggests that feedback projections could be responsible for the reliable propagation of information encoded in spike times through cortex, and thus could serve as an attentional mechanism to regulate the flow of information in the cortex. Feedback projections may also participate in generating spike synchronization that is engaged in cognitive behaviors by the same mechanisms described here for spike propagation.The firing rates of cortical neurons carry information about sensory inputs and motor actions (1). Precisely timed action potentials related to stimuli and behavior have also been observed in the cerebral cortex (2–4), and the mechanisms underlying precisely timed spike initiation have been studied in cortical neurons in vitro (5). However, the information carried by the precise timing of spikes would have to propagate through a hierarchy of cortical areas (6) and noise could disrupt millisecond precision during the transmission.Previous modeling studies have demonstrated that synchronized volleys of spikes are essential for reliably driving the cortex by sparse thalamic inputs (7) and can indeed propagate through the layers of a feedforward network without compromising the temporal precision (8, 9). Furthermore, the temporal precision of a spike volley sharpens as it propagates through the network (10, 11). However, the results of these modeling studies suggest that only sufficiently strong stimuli that evoke spike volleys with a large number of spikes and a small dispersion of spike times would successfully propagate through the feedforward networks without degrading the temporal precision, whereas neural activities that are too weak or too dispersed will die out. This is a critical limitation on the propagation of synchronous spiking compared with the propagation of firing rates; stimuli evoking even low firing rate activity can successfully propagate through multilayer neural networks (12–14).Here we show that when feedback connections are added to a multilayer feedforward model the propagation of synchronous spiking through the network layers is significantly enhanced without compromising temporal precision.In our model with feedback projections, the state space of the model was divided into two areas: propagation and nonpropagation. In the propagation area all trajectories converged into an attractor state representing successful spike volley propagation; any spike volley starting anywhere inside this area successfully propagated through the network and reached the propagation attractor state with millisecond precision. Spike volleys starting outside the propagation area decayed after a few steps of transmission. The feedback changed the initial state of the spike volleys by moving them into the basin of the attractor for successful spike propagation. In addition, the feedback changed the position of the boundary separating propagation and nonpropagation areas, increasing the size of the basin of the propagation attractor.Feedback projections are ubiquitous in the brain (15, 16), but little is known about what they contribute to information processing (17). The results presented here provide testable hypotheses for the functional role of the feedback projections in the brain.Our model suggests that feedback projections could be responsible for allowing information encoded as spike times to propagate through cortical hierarchies, and therefore feedback projections could serve as an attentional mechanism to regulate the flow of information in the cortex. Feedback connections may also participate in generating spike-time synchronization among populations of neurons that are engaged in cognitive behaviors (18–20) by the same mechanisms described here for propagation of synchronized spikes through cortical areas.