How does the hippocampus rapidly consolidates novel information for spatial navigation?

Brad E. Pfeiffer. Spatial learning drives rapid goal representation in hippocampal ripples without place field accumulation or goal-oriented theta sequences. Journal of Neuroscience 8 April 2022, JN-RM-2479-21; DOI: 10.1523/JNEUROSCI.2479-21.2022

Abstract
The hippocampus is critical for rapid acquisition of many forms of memory, although the circuit-level mechanisms through which the hippocampus rapidly consolidates novel information are unknown. Here, activity of large ensembles of hippocampal neurons in adult male Long-Evans rats were monitored across a period of rapid spatial learning to assess how the network changes during the initial phases of memory formation and retrieval. In contrast to several reports, the hippocampal network did not display enhanced representation of the goal location via accumulation of place fields or elevated firing rates at the goal. Rather, population activity rates increased globally as a function of experience. These alterations in activity were mirrored in the power of the theta oscillation and in the quality of theta sequences, without preferential encoding of paths to the learned goal location. In contrast, during brief ‘offline’ pauses in movement representation of a novel goal location emerged rapidly in ripples, preceding other changes in network activity. These data demonstrate that the hippocampal network can facilitate active navigation without enhanced goal representation during periods of active movement and further indicate that goal representation in hippocampal ripples prior to movement onset supports subsequent navigation, possibly through activation of downstream cortical networks.”

SIGNIFICANCE STATEMENT:

Understanding the mechanisms through which the networks of the brain rapidly assimilate information and use previously learned knowledge are fundamental areas of focus in neuroscience. In particular, the hippocampal circuit is a critical region for rapid formation and use of spatial memory. In this study, several circuit-level features of hippocampal function were quantified while rats performed a spatial navigation task requiring rapid memory formation and use. During periods of active navigation, a general increase in overall network activity is observed during memory acquisition, which plateaus during memory retrieval periods, without specific enhanced representation of the goal location. During pauses in navigation, rapid representation of the distant goal well emerges before either behavioral improvement or changes in online activity.”

Brad E. Pfeiffer. Spatial learning drives rapid goal representation in hippocampal ripples without place field accumulation or goal-oriented theta sequences. Journal of Neuroscience 8 April 2022, JN-RM-2479-21; DOI: 10.1523/JNEUROSCI.2479-21.2022