Self-organization of grid fields under supervision of place cells in a neuron model with associative plasticity

The grid cells (GCs) of the medial entorhinal cortex (MEC) and place cells (PCs) of the hippocampus are assumed to be the key elements of the brain network for the metric representation of space. Existing theoretical models of GC network rely on specific hypotheses about the network connectivity patterns. How these patterns could be formed during the network development is not fully understood. It was previously suggested, within the feedforward network models, that activity of PCs could provide the basis for development of GC-like activity patterns. Supporting this hypothesis is the finding that PC activity remains spatially stable after disruption of the GC firing patterns and that the grid fields almost disappear when hippocampal cells are deactivated. Here a new theoretical model of this type is proposed, allowing for grid fields formation due to synaptic plasticity in synapses connecting PCs in hippocampus with neurons in MEC. Learning of the hexagonally symmetric fields in this model occurs due to complex action of several simple biologically motivated synaptic plasticity rules. These rules include associative synaptic plasticity rules similar to BCM rule, and homeostatic plasticity rules that constrain synaptic weights. In contrast to previously described models, a short-term navigational experience in a novel environment is sufficient for the network to learn GC activity patterns. We suggest that learning on the basis of simple and biologically plausible associative synaptic plasticity rules could contribute to the formation of grid fields in early development and to maintenance of normal GCs activity patterns in the familiar environments. (C) 2015 Elsevier B.V. All rights reserved.