Abstract

During the exploration of novel environments, place fields are rapidly formed in hippocampal CA1 neurons. Place cell firing rate increases in early stages of exploration of novel environments but returns to baseline levels in familiar environments. Although similar in amplitude and width, place fields in familiar environments are more stable than in novel environments. We propose a computational model of the hippocampal CA1 network, which describes the formation, dynamics and stabilization of place fields. We show that although somatic disinhibition is sufficient to form place fields, dendritic inhibition along with synaptic plasticity is necessary for place field stabilization. Our model suggests that place cell stability can be attributed to strong excitatory synaptic weights and strong dendritic inhibition. We show that the interplay between somatic and dendritic inhibition balances the increased excitatory weights, such that place cells return to their baseline firing rate after exploration. Our model suggests that different types of interneurons are essential to unravel the mechanisms underlying place field plasticity. Finally, we predict that artificially induced dendritic events can shift place fields even after place field stabilization.

Highlights

  • The hippocampus encodes spatial information through a subset of pyramidal cells—the place cells—that fires action potentials when the animal is in a specific location within the environment—the place fields [1, 2, 3, 4]

  • Here we focus on the role of hippocampal cells in spatial memory development, the hippocampus is associated with other types of memories [17, 18], and the principles governing place field dynamics are likely to be common across several types of hippocampal memory formation

  • We show that the combined action of somatic and dendritic inhibition balances an increase in excitatory weights due to synaptic plasticity, so that place cells after exploration return to their baseline firing rate

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Summary

Introduction

The hippocampus encodes spatial information through a subset of pyramidal cells—the place cells—that fires action potentials when the animal is in a specific location within the environment—the place fields [1, 2, 3, 4] These neurons are thought to encode and store new memories by taking part in activity-dependent synaptic plasticity [5, 6, 7, 8, 9]. Once the external, spatially uniform current is removed, the cell returns to its silent, untuned state [12] These results suggest that silent cells receive place-tuned inputs even though there is no signature of those inputs at the soma. It is not clear which elements of the network are responsible for modulating this dendrite-tosoma propagation

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