Characteristics of sequential activity in networks with temporally asymmetric Hebbian learning

Significance Sequential activity is a prominent feature of many neural systems, in multiple behavioral contexts. Here, we investigate how Hebbian rules lead to storage and recall of random sequences of inputs in both rate and spiking recurrent networks. In the case of the simplest (bilinear) rule, we characterize extensively the regions in parameter space that allow sequence retrieval and compute analytically the storage capacity of the network. We show that nonlinearities in the learning rule can lead to sparse sequences and find that sequences maintain robust decoding but display highly labile dynamics to continuous changes in the connectivity matrix, similar to recent observations in hippocampus and parietal cortex. Sequential activity has been observed in multiple neuronal circuits across species, neural structures, and behaviors. It has been hypothesized that sequences could arise from learning processes. However, it is still unclear whether biologically plausible synaptic plasticity rules can organize neuronal activity to form sequences whose statistics match experimental observations. Here, we investigate temporally asymmetric Hebbian rules in sparsely connected recurrent rate networks and develop a theory of the transient sequential activity observed after learning. These rules transform a sequence of random input patterns into synaptic weight updates. After learning, recalled sequential activity is reflected in the transient correlation of network activity with each of the stored input patterns. Using mean-field theory, we derive a low-dimensional description of the network dynamics and compute the storage capacity of these networks. Multiple temporal characteristics of the recalled sequential activity are consistent with experimental observations. We find that the degree of sparseness of the recalled sequences can be controlled by nonlinearities in the learning rule. Furthermore, sequences maintain robust decoding, but display highly labile dynamics, when synaptic connectivity is continuously modified due to noise or storage of other patterns, similar to recent observations in hippocampus and parietal cortex. Finally, we demonstrate that our results also hold in recurrent networks of spiking neurons with separate excitatory and inhibitory populations.