Embedding multiple trajectories in simulated recurrent neural networks in a self-organizing manner.

Complex neural dynamics produced by the recurrent architecture of neocortical circuits is critical to the cortex's computational power. However, the synaptic learning rules underlying the creation of stable propagation and reproducible neural trajectories within recurrent networks are not understood. Here, we examined synaptic learning rules with the goal of creating recurrent networks in which evoked activity would: (1) propagate throughout the entire network in response to a brief stimulus while avoiding runaway excitation; (2) exhibit spatially and temporally sparse dynamics; and (3) incorporate multiple neural trajectories, i.e., different input patterns should elicit distinct trajectories. We established that an unsupervised learning rule, termed presynaptic-dependent scaling (PSD), can achieve the proposed network dynamics. To quantify the structure of the trained networks, we developed a recurrence index, which revealed that presynaptic-dependent scaling generated a functionally feedforward network when training with a single stimulus. However, training the network with multiple input patterns established that: (1) multiple non-overlapping stable trajectories can be embedded in the network; and (2) the structure of the network became progressively more complex (recurrent) as the number of training patterns increased. In addition, we determined that PSD and spike-timing-dependent plasticity operating in parallel improved the ability of the network to incorporate multiple and less variable trajectories, but also shortened the duration of the neural trajectory. Together, these results establish one of the first learning rules that can embed multiple trajectories, each of which recruits all neurons, within recurrent neural networks in a self-organizing manner.