Hippocampal place cells can develop distinct representations of two visually identical environments

The pattern separation ability of hippocampal place cells was tested in an environment in which two visually identical rectangular compartments (Box A and Box B) were connected by a hidden door. Small ensembles of neurons were recorded with tetrodes while the rat searched for randomly distributed loci for reinforcing brain stimulation. The first recording session in Box A was conducted after the rat had explored the environment for the first time for 30 min. Immediately thereafter, a hidden door between Box A and Box B was opened to let the rat into the unexplored compartment, and a 5-min recording session was run with the door concealed. A rearrangement of place fields in Box B was observed in 18/20 neurons and in 5/6 ensembles. Most place fields did not change between two successive sessions in Box B. When the rat returned to Box A, the ensembles of neurons were as likely to adopt the original Box A firing field pattern as the more recent Box B pattern. In order to control for the influence of extra-arena cues, the rat was gradually lifted in a closed bucket from Box A into Box B while the whole arena was rotated by 90 degrees. All but one neuron and all the ensembles followed the intra-arena cues. Both rotated Box B and Box A firing field patterns were represented but Box B pattern was stronger among the neuronal ensembles. These findings indicate that hippocampal place cells not only can develop distinct representations of two visually identical environments but also can selectively reactivate either one of these representations depending on the rat's recent experience.