Coincidence detection of place and temporal context in a network model of spiking hippocampal neurons

Recent advances in single-neuron biophysics have enhanced our understanding of information processing on the cellular level, but how the detailed properties of individual neurons give rise to large-scale behavior remains unclear. Here, we present a model of the hippocampal network based on observed biophysical properties of hippocampal and entorhinal cortical neurons. We assembled our model to simulate spatial alternation, a task that requires memory of the previous path through the environment for correct selection of the current path to a reward site. The convergence of inputs from entorhinal cortex and hippocampal region CA3 onto CA1 pyramidal cells make them potentially important for integrating information about place and temporal context on the network level. Our model shows how place and temporal context information might be combined in CA1 pyramidal neurons to give rise to splitter cells, which fire selectively based on a combination of place and temporal context. The model leads to a number of experimentally testable predictions that may lead to a better understanding of the biophysical basis of information processing in the hippocampus. Author Summary. Understanding how behavior is connected to cellular and network processes is one of the most important challenges in neuroscience, and computational modeling allows one to directly formulate hypotheses regarding the interactions between these scales. We present a model of the hippocampal network, an area of the brain important for spatial navigation and episodic memory, memory of "what, when, and where." We show how the model, which consists of neurons and connections based on biophysical properties known from experiments, can guide a virtual rat through the spatial alternation task by storing a memory of the previous path through an environment. Our model shows how neurons that fire selectively based on both the current location and past trajectory of the animal (dubbed "splitter cells") might emerge from a newly discovered biophysical interaction in these cells. Our model is not intended to be comprehensive, but rather to contain just enough detail to achieve performance of the behavioral task. Goals of this approach are to present a scenario by which the gap between biophysics and behavior can be bridged and to provide a framework for the formulation of experimentally testable hypotheses.Northwestern University; National Science Foundation (NSF-IGERT, DGE 9987577, NSF SCL SBE 0354378); National Institutes of Health (NIMH 71702, NIMH-60013, NIDA-16454, NS-46064