Memory functions of neuronal oscillations and the hippocampo‐neocortical dialogue

Abstract

Two key structures involved in memory are the hippocampus and neocortex. The communication between these structures is governed by distinctive neuronal oscillations, emerging from rhythmic activity of neuronal populations. Firstly, during active behavioral states, information is actively encoded and retrieved in order to facilitate learning and goal-directed decision making. Accordingly, the hippocampus may serve to index representations stored in the neocortex. Theta oscillations synchronize the hippocampus with neocortical areas and clock respective encoding and retrieval of information. Gamma oscillations provide a neurophysiological mechanism through which information-coding subpopulations of neurons are synchronized and communicate. Together, theta and gamma oscillations are able to group and encode temporally separated events and maintain memory representations in a working memory buffer. Conversely, during inactive behavioral states, memory representations are strengthened and integrated into existing networks of memory representations, as a result of coordinated repeated reactivation, also known as replay. Memory replay is associated with large synchronous population bursts in hippocampus, called sharp wave ripple events. During slow wave sleep, these sharp wave ripple events are coordinated by neocortical UP and DOWN states of the sleep slow oscillation, and concomitant sleep spindles. Together, sharp wave ripples and sleep spindles provide the optimal environment for long-term potentiation of synaptic connections. In addition, synaptic strengths may be proportionally downscaled by the recurring DOWN states of the slow oscillation, ensuring an energetically sustainable state and an improved signal-to-noise ratio of synaptic representations. In conclusion, fine-tuned neuronal oscillatory mechanisms orchestrate the hippocampo-neocortical dialogue and thereby subserve the encoding, consolidation and retrieval of memory representations.