Effects of Age on Negative Subsequent Memory Effects Associated with the Encoding of Item and Item-Context Information

Abstract

It has consistently been reported that "negative" subsequent memory effects--lower study activity for later remembered than later forgotten items--are attenuated in older individuals. The present functional magnetic resonance imaging study investigated whether these findings extend to subsequent memory effects associated with successful encoding of item-context information. Older (n = 25) and young (n = 17) subjects were scanned while making 1 of 2 encoding judgments on a series of pictures. Memory was assessed for the study item and, for items judged old, the item's encoding task. Both memory judgments were made using confidence ratings, permitting item and source memory strength to be unconfounded and source confidence to be equated across age groups. Replicating prior findings, negative item effects in regions of the default mode network in young subjects were reversed in older subjects. Negative source effects, however, were invariant with respect to age and, in both age groups, the magnitude of the effects correlated with source memory performance. It is concluded that negative item effects do not reflect processes necessary for the successful encoding of item-context associations in older subjects. Negative source effects, in contrast, appear to reflect the engagement of processes that are equally important for successful episodic encoding in older and younger individuals.

Sensitivity of negative subsequent memory and task-negative effects to age and associative memory performance

“…2008; Park and Rugg, 2008; see also Mattson et al, in press). The effects were restricted mainly to regions that also demonstrated task-negative effects, consistent with the proposal that negative subsequent memory effects primarily reflect modulation of task-negative activity (Daselaar et al, 2004; de Chastelaine and Rugg, 2014).…”

“…In light of prior reports that the magnitude of negative subsequent memory effects covaries with memory performance (de Chastelaine and Rugg, 2014; Duverne et al, 2009; Mattson et al, in press; Miller et al, 2008; Mormino et al, 2012), we computed the across-participant partial correlation (controlling for age) between pR (associative recognition performance) and the magnitude of the negative subsequent memory effects (collapsed across the 9 regions described previously). The correlation was far from significant (r = .04), and the correlations remained non-significant when computed for each age group separately (all rs < 0.19).…”

“…Moreover, negative subsequent memory effects can also be identified in ‘task-positive’ regions that are not part of the default mode network. For example, Daselaar et al (2004) and Mattson et al (in press) both described robust negative subsequent memory effects in the anterior insula, despite the fact that the region exhibited a marked task-positive response with respect to baseline (see also Reynolds et al, 2004, Wagner and Davachi, 2001). Furthermore, it was recently reported that task-negative and negative subsequent memory effects can be dissociated by manipulation of the difficulty of the study task (de Chastelaine & Rugg, 2014): Whereas the former effects were enhanced in the more difficult condition, difficulty had no effect on the magnitude of the negative subsequent memory effects elicited in the same brain regions.…”

“…fMRI studies investigating the cognitive and neural bases of age-related episodic memory decline have focused on the neural correlates of both encoding and retrieval operations. Studies that have investigated age-related differences in the neural correlates of encoding (the focus of the present study) have typically utilized the subsequent memory procedure (e.g., de Chastelaine et al, 2011; Duverne et al, 2009; Gutchess et al, 2005; Mattson et al, in press; Miller et al, 2008; Morcom et al, 2003; Mormino et al, 2012; Park et al, 2013). In this procedure (Paller and Wagner, 2002), blood oxygenation level dependent (BOLD) activity elicited by study items is contrasted according to performance on a later memory test.…”

“…Recently, however, there has been increased interest in the effects of age on ‘negative’ subsequent memory effects, that is, effects taking the form of relative decrements in study activity for items that go on to receive accurate as opposed to inaccurate judgments. Across studies employing a variety of different study tasks and memory tests, negative subsequent memory effects have consistently been reported to be attenuated (and sometimes reversed) in healthy older individuals (e.g., de Chastelaine et al 2011; Duverne et al, 2009; Gutchess et al, 2005; Mattson et al, in press; Miller et al 2008; Mormino et al 2012; Park et al, 2013). Furthermore, the magnitude of negative subsequent memory effects in older adults has been reported to correlate positively with their memory performance (de Chastelaine et al, 2011; Mattson et al, in press; Miller et al, 2008; Mormino et al, 2012; see de Chastelaine and Rugg, 2014, for similar findings in young individuals), suggesting that the effects reflect the engagement of processes that are of functional significance for memory encoding.…”