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Abstract

Traditional models of learning and memory consolidation postulate two interacting memory systems, with rapid encoding supported by the hippocampus (HC) and only gradually developing, stable storage in neocortical circuits. In a recent fMRI study we have shown rapidly emerging memory-related activity in the posterior parietal cortex (PPC) that over learning repetitions becomes independent of HC signaling and fulfills all criteria for a long-term memory representation. Besides changes in functional activity, the site where a memory representation is stored for the long-term should also undergo structural changes. These changes can be assessed by diffusion MRI already several hours after learning. In the current study, we investigated functional and structural changes in the HC and neocortex over the course of learning. Additionally, we were interested in the impact of sleep on memory systems consolidation. Two groups of human subjects (n=41) learned object-place associations over 8 learning-recall repetitions in two sessions spaced 13 hours apart. The wake group had the first session in the morning, spent the day awake and returned in the evening for the second session. The sleep group learned in the evening, slept during the night and returned in the morning. Neural activity during learning and recall was tracked with fMRI. To assess structural changes, dMRI was acquired at three time points: immediately before the first learning session, 90 minutes after the first learning session and again before the second learning session. Confirming our previous results, functional activity in the PPC increases rapidly over learning repetitions and mirrors the progression of recall performance rates. The same holds true for functional activity during recall. Concerning structural changes, when controlling for circadian effects in gray matter, PPC areas also show a decrease in mean diffusivity after the first learning session. Conversely, HC functional activity declines only over the first learning session. Analysis of beta estimates over all 8 learning repetitions shows a steep decline in functional activity only from the first to the second learning repetition. Sleep affected behavior, as the performance of the wake, but not the sleep group worsens over the retention interval between sessions and functional activity in posterior parietal areas. The simultaneous investigation of functional and structural changes confirms the rapid build-up of a long-term memory representation in posterior parietal areas, which is further stabilized by sleep. The contribution of the HC to encoding, however, seems to be confined to the very first encounter with new information.