Functional and structural changes over learning indicate rapid build-up of neocortical memory

Introduction: Traditional models of learning and memory consolidation postulate two interacting memory systems, with rapid encoding supported by the hippocampus and only gradually developing, stable storage in neocortical circuits (McClelland et al., 1995). There is an ongoing debate about which neocortical regions subserve long-term memory consolidation, including the idea, that the same regions originally involved in processing the input later provide the neural substrate for the memory trace. In a recently published fMRI study we have shown rapidly emerging neocortical memory-related activity in the posterior parietal cortex (PPC) that over learning repetitions becomes independent of hippocampal signaling and fulfills all criteria for a long-term memory representation (Brodt et al., 2016). 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 (Sagi et al., 2012). In the current study, we investigated functional and structural changes in the neocortex over the course of learning. Methods: Two groups of human subjects (n=41) learned object-place associations over 8 learning-recall repetitions in two sessions spaced 13 hours apart. 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. Results: Confirming our previous results, functional activity in the PPC, specifically in the precuneus, increases rapidly over learning repetitions, is stable over an offline period 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, PPC areas as well as other areas along the dorsal and ventral processing streams show a marked decrease in mean diffusivity after the first learning session, which is stable for at least 12 hours and correlates with performance improvement between the task sessions. Conclusions: The simultaneous investigation of functional and structural changes confirms the rapid build-up of long-term memory representations in areas involved in the original processing of later remembered stimuli and emphasize the special role that posterior parietal areas play for memory function