Goal Location Beta Oscillations and Sharp Wave–Ripples Are Complementary Markers of Learning-Related Changes in Hippocampal–Neocortical Networks

Abstract

The hippocampus and neocortex are thought to undergo reorganization to incorporate new information during learning. How can we identify network states that indicate learning is occurring? In the hippocampus, one network signature with these properties is the sharp wave–ripple (SWR), which occurs more frequently during initial learning. However, it remains unclear which neural signatures track changes in neocortical networks during learning. We therefore recorded local field potentials simultaneously from the dorsal hippocampus (CA1) and prefrontal cortex (PFC) as male rats learned spatial navigation tasks. After animals reached goal locations, we found beta frequency (∼20 Hz) oscillations in PFC that increased in power with improvements in performance across days of training. In contrast, the rate and size of hippocampal SWRs decreased over the same period. Furthermore, goal-entry beta in PFC but not in CA1 was correlated with reward likelihood. Our results suggest that neocortical beta oscillations develop gradually as learning occurs, which stands in contrast to the reduction in hippocampal SWRs as the task becomes familiar. We hypothesize that PFC beta oscillations and hippocampal SWRs are complementary markers of experience-dependent change in hippocampal–neocortical networks during learning.