We found that novel arm cells were initially much more likely to be reactivated (i.e., to fire at least one spike) during any given ripple than were familiar arm cells on days 1 and 2. These differences were no longer significant on day 3. For example, on day 1 novel arm cells were about two and a half times more likely to be reactivated than their familiar arm counterparts. Since individual novel arm cells were initially more active during ripples, pairs of novel arm cell should have been more co-active than their familiar arm counterparts. Indeed, on day 1 novel arm pairs were about six times more likely to be co-active than familiar arm cell pairs. This significant co-activity remained across all three days of exposure to the novel arm. Furthermore, reactivation of novel arm cell pairs was initially more coordinated: pairs were more co-active than would be expected if the two cells were firing independently during ripples.
We also measured the width (root-mean-square (RMS) time lag) of the CCG between neuron pairs including only spikes that occurred within ripples. Novel arm cell pairs were significantly more precisely coordinated than familiar arm cell pairs on days 1 and 2, but not on day 3. Novel arm cell pairs were therefore more frequently co-active in a window compatible with synaptic plasticity. This highly precise reactivation of novel arm cells was present throughout the environment, and could not be explained by proximity to the novel arm.
If, as has been proposed, reactivation is a simple replay of
experience, then the level of coordinated reactivation during ripples
should reflect the level of coordinated spatial activity during
experience. We therefore examined the evolution of spatio-temporal
structure in single cells and cell pairs. Surprisingly, reactivation
was strongest and most coordinated when spatial activity was least
coordinated, and reactivation became weaker as place cells came to
express reliable spatio-temporal organization during exploration.
These results demonstrate that coordinated reactivation of cell
assemblies is strongest in novel environments where the hippocampus
must form new representations and weaker in familiar environments
where a stable representation is already present. Ripples originate
in hippocampal area CA3, and we propose that one important role for
reactivation is to replay recently learned correlations into CA1,
allowing for off-line learning within the hippocampus following
experience.