Abstract
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). In a recent fMRI study we have shown rapidly emerging memory-related activity in the posterior parietal cortex (PPC) that becomes independent of hippocampal activity over learning repetitions 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. Such changes can be assessed by diffusion MRI (dMRI) already several hours after learning (Sagi et al., 2012). In the current study, we investigated functional and structural changes in the hippocampus and neocortex over the course of learning. Additionally, we were interested in the impact of sleep, as it has been shown to support memory systems consolidation (Frankland and Bontempi, 2005).
Methods:
Two groups of human subjects (n=41) learned object-place associations over 7 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 first 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.
Results:
Confirming our previous results, functional activity in the PPC, specifically in the precuneus, increased rapidly over learning repetitions (pFWE < .05) and mirrored the development of recall performance rates (r37 = .519, t37 = 6.38, p < .001). The same holds true for functional brain activity during recall. Importantly, learning also led to structural changes in the PPC. When controlling for circadian effects in gray matter, we observed a decrease in mean diffusivity following the first learning session (pFDR < .05).
Conversely, hippocampal functional activity declined over the first learning session (pFWE < 0.05). Analysis of beta estimates over all 7 learning repetitions shows a steep and persistent decline in functional activity from the first to the second learning repetition.
Sleep had a beneficial effect on memory retention, as performance remained stable over the retention interval in the sleep group, whereas performance declined in the wake group (F1,36= 6.97, p = .01). Functional activity in posterior parietal areas mirrored this effect on behavior (puncorr < .001).
Conclusions:
The simultaneous investigation of functional and structural changes confirms the rapid formation of long-term memory representations in posterior parietal areas, which is further stabilized by sleep. The contribution of the hippocampus to encoding, however, seems to be confined to the very first encounters with new information.
