The neural correlates of recollection and retrieval monitoring: Relationships with age and recollection performance

Abstract

The relationships between age, retrieval-related neural activity, and episodic memory performance were investigated in samples of young (18–29 yrs), middle-aged (43–55 yrs) and older (63–76 yrs) healthy adults. Participants underwent fMRI scanning during an associative recognition test that followed a study task performed on visually presented word pairs. Test items comprised pairs of intact (studied pairs), rearranged (items studied on different trials) and new words. fMRI recollection effects were operationalized as greater activity for studied pairs correctly endorsed as intact than for pairs incorrectly endorsed as rearranged. The reverse contrast was employed to identify retrieval monitoring effects. Robust recollection effects were identified in the core recollection network, comprising the hippocampus, along with parahippocampal and posterior cingulate cortex, left angular gyrus and medial prefrontal cortex. Retrieval monitoring effects were identified in the anterior cingulate and right dorsolateral prefrontal cortex. Neither recollection effects within the core network, nor the monitoring effects differed significantly across the age groups after controlling for individual differences in associative recognition performance. Whole brain analyses did however identify three clusters outside of these regions where recollection effects were greater in the young than in the other age groups. Across-participant regression analyses indicated that the magnitude of hippocampal and medial prefrontal cortex recollection effects, and both of the prefrontal monitoring effects, correlated significantly with memory performance. None of these correlations were moderated by age. The findings suggest that the relationships between memory performance and functional activity in regions consistently implicated in successful recollection and retrieval monitoring are stable across much of the healthy adult lifespan.

Decoding the content of recollection within the core recollection network and beyond

“…In agreement with other recent work from our laboratory (de Chastelaine, Mattson, Wang, Donley, & Wang, 2016), Wang et al (2016) reported that age did not exert a detectable influence on either of these classes of effects. While not the primary focus of the present analysis, we took advantage of the dataset to examine whether, in contrast to our prior findings for content-selective cortical regions, reinstatement effects in members of the core recollection network are age-sensitive.…”

Individual differences in associative memory among older adults explained by hippocampal subfield structure and function

“…It bears noting, however, that other standard-resolution studies report a positive relationship between hippocampal retrieval activity and associative memory performance across the life span (see, e.g., ref. 54). Given that averaging activity across subfields may produce variable findings, continued high-resolution investigation of hippocampal function may help to resolve such inconsistencies.…”

Independent contributions of fMRI familiarity and novelty effects to recognition memory and their stability across the adult lifespan

“…Notably, studies employing fMRI have identified largely non-overlapping patterns of neural activity associated with recollection- and familiarity-based memory judgments (e.g.,Johnson et al, 2013; Montaldi et al, 2006; for reviews, see Kim, 2010, 2013). When recollection is operationalized by the contrast between correctly recognized memory test items for which recollection succeeded or failed, enhanced activity is evident in a characteristic brain network (the ‘core recollection’ network) that includes the hippocampus and medial prefrontal, posterior cingulate, middle temporal and ventral parietal cortex (Rugg and Vilberg, 2013) (The reverse contrast, identifying where activity is greater for familiar than recollected items, has frequently been employed to study the neural correlates of ‘retrieval monitoring’; see de Chastelaine et al, 2016a, and Wang et al, 2016, for recent examples). Familiarity (operationalized, for example, by the contrast between recognized but unrecollected items and unstudied items) is associated with enhanced activity in a different set of regions, including the intra-parietal sulcus (IPS), precuneus, lateral and anterolateral prefrontal cortex and caudate nucleus (Kim, 2010, 2013).…”

“…Motivated by the vulnerability of recollection to increasing age (see above), several studies have been reported where fMRI was employed to contrast recollection-related neural activity according to age (see de Chastelaine et al, 2016a, and Wang et al, 2016, for two recent examples, and Wang and Cabeza, 2016, for review). There are fewer reports describing age effects on neural correlates of familiarity-based memory judgments (Angel et al, 2013; Daselaar et al, 2006b; Duarte et al, 2010; Wang and Giovanello, 2016), and only a handful of fMRI studies that have examined the influence of age on novelty processing more generally (Bowman and Dennis, 2015; Moriguchi et al, 2011; Wang et al, 2015).…”

“…Here, we further examine the question of whether familiarity or novelty effects are age-sensitive. We took advantage of a previously described large dataset (N = 136; de Chastelaine et al, 2016a) to examine the neural correlates of familiarity and novelty processing with participant samples that spanned the adult lifespan more continuously than was the case in prior studies (all of which employed extreme age group designs), and that provided statistical power sufficient to allow a sensitive assessment of whether these correlates co-vary with memory performance.…”