Hippocampal-cortical encoding activity predicts the precision of episodic memory

Abstract

Our recollections of past experiences can vary both in the number of specific event details accessible from memory and the precision with which such details are reconstructed. Prior neuroimaging evidence suggests the success and precision of episodic recollection to rely on distinct neural substrates during memory retrieval. In contrast, the specific encoding mechanisms supporting later memory precision, and whether they differ from those underlying successful memory formation in general, are currently unknown. Here, we combined continuous measures of memory retrieval with model-based analyses of behavioural and neuroimaging data to tease apart the encoding correlates of successful memory formation and mnemonic precision. In the MRI scanner, participants encoded object-scene displays, and later reconstructed features of studied objects using a continuous scale. We observed overlapping encoding activity in inferior prefrontal and posterior perceptual regions to predict both which object features were later remembered versus forgotten, and the precision with which they were reconstructed from memory. In contrast, hippocampal encoding activity significantly predicted the precision, but not overall success, of subsequent memory retrieval. The current results identify a hippocampal-cortical encoding basis for episodic memory precision, and suggest a contribution of shared cortical encoding mechanisms to the formation of both accessible and precise memory representations.

Memory precision of object-location binding is unimpaired inAPOEε4-carriers with spatial navigation deficits

“…28,84,[102][103][104][105] Functional MRI data suggest that the precision task further engages posterior parietal cortex regions upon retrieval to allow for the faithful reinstatement and visuospatial reconstruction of object features 24,84 and that hippocampal activity at encoding scales with precision. 20 Importantly, MTL-parietal connectivity tracks memory precision, which is of note given that these connections may already be altered in the early stages of AD, and even among relatively young ε4-carriers. 83,84,[106][107][108] Despite the absence of a precision memory deficit in the present sample, Coughlan and colleagues recently described suboptimal navigation patterns in these same ε3ε4 carriers (a subset of whom were enrolled in this study).…”

“…[17][18][19] Memory for high fidelity representations crucially relies on hippocampus, ERC, perirhinal cortex and posterior parietal regions. The ERC supports high fidelity representations of objects, spatial features of objects and the environment, [20][21][22][23][24][25][26] which are bound by the hippocampus into holistic episodes [27][28][29][30][31] that can be faithfully reinstated upon retrieval with the concerted action of the recollection network. 32,33 Importantly, tau spreads from transentorhinal to parietal regions of the recollection network that are crucial for memory fidelity, 21 and the communication of these brain regions is already altered in preclinical AD and genetic-risk carriers.…”

Reduced memory precision in older age is associated with functional and structural differences in the angular gyrus

“…The continuous report task has been described in detail in Korkki et al 41 . A total of 9 study-test blocks were completed (see Figure 1).…”

“…All participants completed a memory task that involved studying a series of object-scene displays (see Figure 1, see also refs 22,41,42 ). Importantly, the colour and location of each object presented were randomly drawn from circular parameter spaces, allowing us to assess participants' memory for these object attributes using a continuous, analogue scale.…”

“…To gain trial-specific estimates of the success and precision of memory retrieval for the fMRI analyses, the two-component mixture model (von Mises + uniform distribution) was fitted to all retrieval errors across all participants (7020 trials in total) to calculate a cut-off point at which the probability of participants' responses stemming from the target von Mises distribution was less than .05 and responses thus likely reflected guessing 22,41,42 . This cut-off point of ± 59 degrees was then used to classify each retrieval trial as successful (absolute retrieval error ≤ 59 degrees) or unsuccessful (absolute retrieval error > 59 degrees).…”