Human brain activity and functional connectivity as memories age from one hour to one month

Abstract

Theories of memory consolidation suggest the role of brain regions and connectivity between brain regions change as memories age. Human lesion studies indicate memories become hippocampus-independent over years, whereas animal studies suggest this process occurs across relatively short intervals, from days to weeks. Human neuroimaging studies suggest that changes in hippocampal and cortical activity and connectivity can be detected over these short intervals, but many of these studies examined only two time periods. We examined memory and fMRI activity for photos of indoor and outdoor scenes across four time periods to examine these neural changes more carefully. Participants (N = 21) studied scenes 1 hour, 1 day, 1 week, or 1 month before scanning. During scanning, participants viewed scenes, made old/new recognition memory judgments, and gave confidence ratings. Memory accuracy, confidence ratings, and response times changed with memory age. Brain activity in a widespread cortical network either increased or decreased with memory age, whereas hippocampal activity was not related to memory age. These findings were almost identical when effects of behavioral changes across time periods were minimized. Functional connectivity of the ventromedial prefrontal cortex with the posterior parietal cortex increased with memory age. By contrast, functional connectivity of the hippocampus with the parahippocampal cortex and fusiform gyrus decreased with memory age. In sum, we detected changes in cortical activity and changes in hippocampal and cortical connectivity with memory age across short intervals. These findings provide support for the predictions of systems consolidation and suggest that these changes begin soon after memories are formed.

Keywords: Consolidation; Functional Connectivity; functional magnetic resonance imaging; neuroimaging; retrograde memory.

Figure 1.

Note. Study design. Participants studied a different set of 80 color photographs of indoor and outdoor scenes one hour, one day, one week, or one month before scanning. In the scanner, participants made old/new recognition memory judgments with confidence ratings (1 = definitely new to 6 = definitely old) in response to scenes (240 studied scenes intermixed with 240 novel scenes) and made odd/even judgments in response to digits (baseline trials).

Figure 2.

Note. In-scanner behavioral measures of memory. Average in-scanner recognition memory performance for all trials as a function of memory age. A. Measure of discrimination (d’ [D Prime]) between old and new scenes B. Confidence ratings from 1 (definitely new) to 6 (definitely old) for targets. C. Response time in milliseconds for targets. Error bars show SEM.

Figure 3.

Note. Brain regions in which activity followed memory age. A. Coronal sections displaying brain regions in which brain activity for targets decreased (cold colors) or increased (warm colors) as a function of memory age (one hour to one month; voxel-wise p < 0.001, cluster-wise p < 0.05). Sections from anterior (upper left) to posterior (lower right). Higher F values indicate activity that more closely followed a power function. Red arrows and numbers highlight regions included in panel B. B. Patterns of brain activity (beta coefficients) in selected regions from the frontal and parietal lobes shown in A. Ang., Angular; ACC., Anterior Cingulate Cortex.; B., Bilateral; PCC., Posterior Cingulate Cortex; G., Gyrus.; IPL., Inferior Parietal Lobule; Med., Medial. MFG.; Middle Frontal Gyrus; R., Right. SPL.; Superior Parietal Lobule. Error bars show SEM.

Figure 4.

Note. Pattern of brain activity (beta coefficients) in the bilateral anatomical hippocampal region of interest. No significant difference was detected across the timepoints (ANOVA: Memory Age)

Figure 5.

Note. Minimal overlap of retrieval activity related to memory age and encoding-related activity. Brain regions where activity was related to memory retrieval of targets (blue) or incidental encoding (red) of foils. Retrieval regions are as shown in Figure 3. Activity in encoding regions significantly distinguished subsequently remembered foils versus subsequently forgotten foils based on the surprise post-scan recognition memory test (see Supplemental Table 3). Yellow voxels indicate areas of overlap between the two networks where green circles highlight the four small areas of overlap. A., Anterior; L, Left.

Figure 6.

Note. Ventromedial prefrontal cortex (vmPFC) and hippocampal functional connectivity. A. Sagittal section showing bilateral vmPFC seed region of interest (red). B. Coronal section showing bilateral hippocampal seed region of interest (red). C. Sagittal section showing a cluster in the posterior parietal cortex (PPC = posterior cingulate/precuneus) where functional connectivity with the vmPFC changed with memory age according to a power function (voxel-wise p < 0.001, cluster-wise p < 0.05). D. Coronal sections showing two clusters (see green circles: left parahippocampal cortex [PHC] and right fusiform gyrus; see Table 2) where functional connectivity significantly decreased with memory age (voxel-wise p < 0.001, cluster-wise p < 0.05). Exploratory analysis at a lower probability value (voxel-wise p < 0.01, cluster-wise p < 0.05) revealed that these regions were part of a larger network that included clusters in the PFC, insula, medial temporal lobe, lateral temporal lobe, posterior cingulate, parietal cortex, and occipital cortex (see Table 2). Higher F values indicate connectivity that more closely followed a power function. E. Pattern of functional connectivity (beta coefficients) between the vmPFC and the PPC for targets (black circles) or foils (white circle). F. Patterns of hippocampal functional connectivity for the regions circled in panel D for targets (black circles) and foils (white circles). L., Left; R., Right. Error bars show SEM.