Abstract
Memories are thought to be encoded as a distributed representation in the neocortex. The medial prefrontal cortex (mPFC) has been shown to support the expression of memories that initially depend on the hippocampus (HPC), yet the mechanisms by which the HPC and mPFC access the distributed representations in the neocortex are unknown. By measuring phase synchronization of local field potential (LFP) oscillations, we found that learning initiated changes in neuronal communication of the HPC and mPFC with the lateral entorhinal cortex (LEC), an area that is connected with many other neocortical regions. LFPs were recorded simultaneously from the three brain regions while rats formed an association between an auditory stimulus (CS) and eyelid stimulation (US) in a trace eyeblink conditioning paradigm, as well as during retention 1 month following learning. Over the course of learning, theta oscillations in the LEC and mPFC became strongly synchronized following presentation of the CS on trials in which rats exhibited a conditioned response (CR), and this strengthened synchronization was also observed during remote retention. In contrast, CS-evoked theta synchronization between the LEC and HPC decreased with learning. Our results suggest that communication between the LEC and mPFC are strengthened with learning whereas the communication between the LEC and HPC are concomitantly weakened, suggesting that enhanced LEC–mPFC communication may be a neuronal correlate for theoretically proposed neocortical reorganization accompanying encoding and consolidation of a memory.
Highlights
The hippocampus (HPC) is necessary to rapidly form associations between elements in an event; its importance for the retrieval of an acquired association is time-limited (Scoville and Milner, 1957; Squire, 1992)
By measuring phase synchronization of local field potential (LFP) oscillations, we found that learning initiated changes in neuronal communication of the HPC and medial prefrontal cortex (mPFC) with the lateral entorhinal cortex (LEC), an area that is connected with many other neocortical regions
Our results demonstrated that this reorganization may be directly reflected in dissociated patterns of interaction between the lateral entorhinal cortex (LEC), dorsal hippocampus (HPC), and medial prefrontal cortex during learning and later retention of associative memory
Summary
The hippocampus (HPC) is necessary to rapidly form associations between elements in an event; its importance for the retrieval of an acquired association is time-limited (Scoville and Milner, 1957; Squire, 1992). One paradigm that demonstrates the time-limited involvement of the HPC in memory is trace eyeblink conditioning, in which an animal learns to associate a neutral conditioned stimulus with an unconditioned stimulus (US) separated by a time, or“trace”interval. The expression of the learned memory association initially requires the HPC (Kim et al, 1995; Takehara et al, 2002, 2003), memory expression later comes to depend on the mPFC (Takehara et al, 2003; Simon et al, 2005; Oswald et al, 2010).
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