The Sync/deSync model: How a synchronized hippocampus and a de-synchronized neocortex code memories

Abstract

Neural oscillations are important for memory formation in the brain. The de-synchronisation of Alpha (10Hz) oscillations in the neo-cortex has been shown to predict successful memory encoding and retrieval. However, when engaging in learning, it has been found that the hippocampus synchronises in Theta (4Hz) oscillations, and that learning is dependent on the phase of Theta. This inconsistency as to whether synchronisation is good for memory formation leads to confusion over which oscillations we should expect to see and where during learning paradigm experiments. This paper seeks to respond to this inconsistency by presenting a neural network model of how a well-functioning learning system could exhibit both of these phenomena, i.e. desynchronization of alpha and synchronisation of theta during successful memory encoding.\n\nWe present a spiking neural network (the Sync/deSync model) of the neo-cortical and hippocampal system. The simulated hippocampus learns through an adapted spike-time dependent plasticity rule, in which weight change is modulated by the phase of an extrinsically generated theta oscillation. Additionally, a global passive weight decay is incorporated, which is also modulated by theta phase. In this way, the Sync/deSync model exhibits theta phase-dependent long-term potentiation and long-term depression. We simulated a learning paradigm experiment and compared the oscillatory dynamics of our model with those observed in single-cell and scalp-EEG studies of the medial temporal lobe. Our Sync/deSync model suggests that both the de-synchronisation of neo-cortical Alpha and the synchronisation of hippocampal Theta are necessary for successful memory encoding and retrieval.\n\nSignificance statementA fundamental question is the role of rhythmic activation of neurons, i.e. how their firing oscillates between high and low rates. A particularly important question is how oscillatory dynamics between the neo-cortex and hippocampus contribute to memory formation. We present a spiking neural-network model of such memory formation, with the central ideas that 1) in neo-cortex, neurons need to break-out of an alpha oscillation in order to represent a stimulus (i.e. alpha desynchronises), while 2) in hippocampus, the firing of neurons at theta facilitates formation of memories (i.e. theta synchronises). Accordingly, successful memory formation is marked by reduced neo-cortical alpha and increased hippocampal theta. This pattern has been observed experimentally and gives our model its name - the Synch/deSynch model.