Beta Oscillations and Hippocampal Place Cell Learning during Exploration of Novel Environments

Abstract

Berke et al. (2008) reported that beta oscillations occur during the learning of hippocampal place cell receptive fields in novel environments. Place cell selectivity can develop within seconds to minutes, and can remain stable for months. Paradoxically, beta power was very low during the first lap of exploration, grew to full strength as a mouse traversed a lap for the second and third times, and became and remained low again after the first two minutes of exploration. Beta oscillation power also correlated with the rate at which place cells became spatially selective, and not with theta oscillations. We explain such beta oscillations as a consequence of how place cell receptive fields may be learned as spatially selective categories due to feedback interactions between entorhinal cortex and hippocampus. Top-down attentive feedback helps to ensure rapid learning and stable memory of place cells. Beta oscillations are generated when top-down feedback mismatches bottom-up data as place cell receptive fields are refined. Beta oscillations do not occur on the first trial because adaptive weights in feedback pathways are all sufficiently large then to match any input pattern. On subsequent trials, adaptive weights become pruned as they learn to match the sharpening receptive fields of the place cell categories, thereby causing mismatches until place cell receptive fields stabilize.