In humans the hippocampus is not only important for memory; it also has a role in imagining the future. Johnson and Redish now show that the hippocampus might be similarly forward-looking in rats, and provide evidence that the neurophysiological basis for this might lie in place-cell firing.

Place cells are hippocampal neurons with firing frequencies that increase dramatically when an animal is in a specific location (known as the neuron’s place field) in an environment. However, in rats they sometimes also fire when the rat is outside of the neuron’s place field, a phenomenon called extra-field spik-ing. In this study, the authors recorded from hippocampal ensembles in rats

that ran two types of maze containing a food reward in one of the arms. Both mazes contained a ‘choice point’ at which the rats had to decide whether to turn left or right in order to obtain the reward.

Using a novel decoding algorithm to examine extra-field spikes at a millisecond timescale, the authors found that particular place cells in the hippocampal CA3 region dis-played extra-field spiking especially when the rat was at the choice point in the maze. The place fields of these cells mostly represented positions in the two paths that the rat could fol-low after the choice point, rather than positions in the path that the rat had already covered. Importantly, place cells with fields that lay on one side of the choice point would fire first, followed by cells with place fields on the other side.

Extra-field spiking also occurred when a rat made a ‘wrong’ choice of direction, both in place cells representing positions forward on the path and in cells representing positions back towards the choice point. Once a rat had learned upon which arm of the maze the food was located, the pauses at the choice points became shorter and the extra-field spiking changed accordingly:

neurons with place fields on the ‘wrong’ side of the maze no longer fired. This adaptation did not occur if the arm upon which the reward was placed was unpredictable.

The authors then analysed the local field potentials (LFPs) at the choice points, and found that they displayed theta and gamma waves, but no sharp waves. Extra-field spiking also occurred while the rats were retrieving the food reward, but the LFPs measured here did dis-play sharp-wave ripple activity. Thus, the signature of extra-field firing at the choice points differed from the reactivation and replay firing that is known to occur at food-reward points.

These findings show that the firing of hippocampal place cells not only corresponds to a rat’s current position in an environment, but that it can also represent the path ahead, signifying possibilities for the route the rat can take. Is this the animal equivalent of imagining the future?

Leonie Welberg

Original research PaPer Johnson, A. & Redish, A. D. Neural ensembles in CA3 transiently encode paths forward of the animal at decision point. J. Neurosci. 27, 12176–12189 (2007)

P l ac e c e l l s

A few moves ahead

Nature Reviews Neuroscience | AOP, published online 12 December 2007; doi:10.1038/nrn2305

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