A computational model for preplay in the hippocampus

Amir H. Azizi, Laurenz Wiskott, Sen Cheng

The hippocampal network produces sequences of neural activity even when there is no time-varying external drive. In offline states, the temporal sequence in which place cells fire spikes correlates with the sequence of their place fields. Recent experiments found this correlation even between offline sequential activity (OSA) recorded before the animal ran in a novel environment and the place fields in that environment. This preplay phenomenon suggests that OSA is generated intrinsically in the hippocampal network, and not established by external sensory inputs. Previous studies showed that continuous attractor networks with asymmetric patterns of connectivity, or with slow, local negative feedback, can generate sequential activity. This mechanism could account for preplay if the network only represented a single spatial map, or chart. However, global remapping in the hippocampus implies that multiple charts are represented simultaneously in the hippocampal network and it remains unknown whether the network with multiple charts can account for preplay. Here we show that it can. Driven with random inputs, the model generates sequences in every chart. Place fields in a given chart and OSA generated by the network are highly correlated. We also find significant correlations, albeit less frequently, even when the OSA is correlated with a new chart in which place fields are randomly scattered. These correlations arise from random correlations between the orderings of place fields in the new chart and those in a pre-existing chart. Our results suggest two different accounts for preplay. Either an existing chart is re-used to represent a novel environment or a new chart is formed.