Independent theta phase coding accounts for CA1 population sequences and enables flexible remapping

Abstract

Hippocampal place cells encode an animal's past, current, and future location through sequences of action potentials generated within each cycle of the network theta rhythm. These sequential representations have been suggested to result from temporally coordinated synaptic interactions within and between cell assemblies. Instead, we find through simulations and analysis of experimental data that rate and phase coding in independent neurons is sufficient to explain the organization of CA1 population activity during theta states. We show that CA1 population activity can be described as an evolving traveling wave that exhibits phase coding, rate coding, spike sequences and that generates an emergent population theta rhythm. We identify measures of global remapping and intracellular theta dynamics as critical for distinguishing mechanisms for pacemaking and coordination of sequential population activity. Our analysis suggests that, unlike synaptically coupled assemblies, independent neurons flexibly generate sequential population activity within the duration of a single theta cycle.

DOI: http://dx.doi.org/10.7554/eLife.03542.001

eLife digest

When we explore a new place, we naturally create a mental map of the location as we go. This mental map is stored in a region of the brain called the hippocampus, which contains cells called place cells. These cells can carry information about our past, present, and future location in the form of electrical signals. They connect to each other to form networks and it has been proposed that these connections can store the information needed for the mental maps.

Real-time maps are represented in the information carried by the electrical signals themselves. A physical location is specified by the individual place cell that is activated, and by the timing of the electrical signal it produces relative to a ‘brain wave’ called the theta rhythm. Brain waves are patterns of electrical signals activated in sets of brain cells and the theta rhythm is produced in the hippocampus of an animal as it explores its surroundings.

Previous experiments suggested that when a rat explores an area, several sets of brain cells in the hippocampus are activated in sequence within each cycle of the theta rhythm. As the rat moves forward, the sequence shifts to different sets of cells to reflect the upcoming locations ahead of the rat. It has been thought that these sequences are triggered by the individual connections between the place cells.

Here, Chadwick et al. developed mathematical models of the electrical activity in the brains of rats as they explored. They used these models to analyze data from previous experiments and found that the sequences of electrical activity arise from the timing of each cell's activity relative to the theta rhythm, rather than from the connections between the cells.

Chadwick et al.'s findings suggest that the mental map may be highly flexible, allowing vast numbers of distinct memories to be stored within the same network of place cells without interference. Future studies will involve investigating the role of brain waves in the forming new mental maps and creating new memories.

DOI: http://dx.doi.org/10.7554/eLife.03542.002