Parallel Engagement of Regions Associated with Encoding and Later Retrieval Forms Durable Memories

Abstract

The fate of a memory is partly determined at initial encoding. However, the behavioral consequences of memory formation are often tested only once and shortly after learning, which leaves the neuronal predictors for the formation of durable memories largely unknown. Here, we hypothesized that durable memory formation (as opposed to weak or no memory formation) is reflected through increased activation in the medial temporal lobes and prefrontal cortex, and more consistent processing (i.e., stronger pattern similarity) across encoding material. Thirty-four human subjects studied unique picture-location associations while undergoing fMRI and performed a cued recall test immediately after study as well as 48 h later. Associative memories were defined as "weak" if they were retrieved during the immediate test only. Conversely, "durable" memories persisted also after 48 h. The posterior cingulate cortex showed increased pattern similarity during successful memory formation, independent of the eventual durability. For durable memory encoding, we found increased activation in medial and inferior temporal, prefrontal, and parietal regions. This was accompanied by stronger pattern similarity in lateral prefrontal and parietal regions, as well as in anterior and posterior midline structures that were also engaged during later memory retrieval. Thus, we show that pattern similarity, or consistent processing, in the posterior cingulate cortex predicts associative memory formation at encoding. If this is paralleled by additional activation increases in regions typically related to encoding, and by consistent processing in regions involved in later retrieval, formed memories appear durable for at least 48 h.

Neural pattern similarity differentially affects memory performance of younger and older adults: Age differences in neural similarity and memory

“…Surprisingly, the hypothesis of the cognitive aging literature suggesting that reduced neural specificity underlies cognitive decline is in stark contrast to the prevalent evidence in general memory research that increased similarity is actually advantageous for performance: In young adult samples, various studies have shown that the representational similarity between different items is positively related to memory performance for these items (Davis et al, 2014; Lu et al, 2015; Wagner et al, 2016), which is in line with cognitive and computational models (Clark and Gronlund, 1996; Gillund and Shiffrin, 1984). Between-item pattern similarity may support memory by capturing regularities across experiences (LaRocque et al, 2013) and by giving rise to a sense of familiarity (Davis et al, 2014).…”

“…Hence, while the age group differences replicated previous reports of increased neural similarity in older compared to younger adults, the within-person direction of the similaritymemory association among older adults corroborates cognitive models of memory (Clark and Gronlund, 1996; Gillund and Shiffrin, 1984; Hintzman, 1988) as well as previous memory studies with younger adults. These studies showed that higher similarity between different item representations (often called ‘global similarity’) is beneficial for subsequent recognition memory (LaRocque et al, 2013; Lu et al, 2015; Ye et al, 2016), memory confidence and categorization (Davis et al, 2014), fear memory (Visser et al, 2013), and associative memory formation (Wagner et al, 2016).…”

“…While high pattern distinctiveness may be beneficial for memory performance to prevent false memories, high pattern similarity may support mnemonic decisions by capturing regularities across experiences (LaRocque et al, 2013) and by giving rise to a feeling of familiarity (Davis et al, 2014). Higher pattern similarity may also reflect more consistent processing that facilitates associative memory formation (Wagner et al, 2016). Strikingly, a tendency for more generalized memories (Koutstaal and Schacter, 1997; Koutstaal et al, 2001; Tun et al, 1998) and a stronger reliance on familiarity (Light et al, 2000; Prull et al, 2006; Yonelinas, 2002) is indeed often reported for older adults.…”

Pattern similarity and connectivity of hippocampal-neocortical regions support empathy for pain

“…We moved a spherical searchlight (Kriegeskorte et al, 2006; see also Wagner et al, 2016) with a radius of 8 mm (251 voxels) throughout the brain volume while only considering searchlights that contained at least 30 gray matter voxels. Single-trial beta estimates from voxels within a given searchlight were extracted and reshaped into a trial × voxel matrix, whereby trials were sorted according to the four experimental conditions (i.e., self pain, self no pain, other pain, other no pain).…”

Integrating memories: Congruency and reactivation aid memory integration through reinstatement of prior knowledge

“…The second recall test that was administered a week after scanning was not used for final analyses, because very little trials were useful. We were planning to do a memory durability analysis on these data (see Wagner et al, 2016). However, since this test was exactly the same as the first recall test, including the associative recognition phase where the right scene was shown on the screen, participants could learn associations during this test as well.…”