Intrinsic dynamics of randomly clustered networks generate place fields and preplay of novel environments

Abstract

During both sleep and awake immobility, hippocampal place cells reactivate time-compressed versions of sequences representing recently experienced trajectories in a phenomenon known as replay. Intriguingly, spontaneous sequences can also correspond to forthcoming trajectories in novel environments experienced later, in a phenomenon known as preplay. Here, we present a model showing that sequences of spikes correlated with the place fields underlying spatial trajectories in both previously experienced and future novel environments can arise spontaneously in neural circuits with random, clustered connectivity rather than pre-configured spatial maps. Moreover, the realistic place fields themselves arise in the circuit from minimal, landmark-based inputs. We find that preplay quality depends on the network’s balance of cluster isolation and overlap, with optimal preplay occurring in small-world regimes of high clustering yet short path lengths. We validate the results of our model by applying the same place field and preplay analyses to previously published rat hippocampal place cell data. Our results show that clustered recurrent connectivity can generate spontaneous preplay and immediate replay of novel environments. These findings support a framework whereby novel sensory experiences become associated with preexisting “pluripotent” internal neural activity patterns. Neural circuits with small-world connectivity spontaneously emit sequences of spikes that are correlated with any of the distinct sequences of realistic place fields produced by location-modulated, monotonically varying input. Jordan Breffle: Conceptualization, Formal Analysis, Investigation, Methodology, Software, Visualization, Writing – original draft, Writing – review & editing Hannah Germaine: Conceptualization, Methodology, Software, Writing – review & editing Justin D. Shin: Data curation, Investigation, Writing – review & editing Shantanu P. Jadhav: Conceptualization, Funding acquisition, Resources, Supervision, Writing – review & editing Paul Miller: Conceptualization, Funding acquisition, Methodology, Project administration, Resources, Supervision, Writing – review & editing NIH/NINDS R01NS104818, NIH/NIMH R01MH112661, NIH/NIMH R01MH120228, and Brandeis University Neuroscience Graduate Program