ReviewAge differences in self-referencing: Evidence for common and distinct encoding strategies
Introduction
Because older adults often experience deficits in memory, it is important to study techniques that can potentially improve memory function with age. One such technique is self referencing. Previous research has shown that relating information to oneself is a successful encoding strategy (Symons and Johnson, 1997). Adjectives encoded in a self referential manner are retrieved more effectively than those encoded in a semantic, structural, or phonemic manner (Rogers et al., 1977). The literature suggests that the self is a unique cognitive structure that possesses special mnemonic capabilities (Macrae et al., 2004). Consistent with this idea, self-referencing has reliably been associated with corresponding activity in the medial prefrontal cortex (mPFC) (Kelley et al., 2002, Macrae et al., 2004, Northoff et al., 2006). Activity in mPFC is elicited in tasks that range from judging whether adjectives describe oneself (e.g., Kelley et al., 2002, Moran et al., 2009), to self-reflection on physical, mental, or personality attributes (Jenkins and Mitchell, 2011), to self-evaluation of performance (Beer et al., 2010), to self-ownership of objects (Turk et al., 2011).
>A number of studies show that a self-referencing strategy benefits memory for older adults as much as young adults’ memory, for a commonly-used adjective task (Glisky and Marquine, 2009, Gutchess et al., 2007, Mueller et al., 1986), as well as for visual details (Hamami et al., 2011) and the source of actions (Rosa and Gutchess, 2011). Results also suggest that the strategy operates spontaneously and effortlessly, without depending on attention (Yang et al., 2012). Correspondingly, functional imaging has shown that the mPFC is similarly activated in younger and older adults during self-referencing (Gutchess et al., 2007). As a result, the activity of the mPFC may remain robust in older adults despite other age related changes to the brain.
The contribution of the mPFC in older adults is less clear when memory is considered. The mPFC has been implicated for younger adults, with activity in the mPFC predicting subsequent memory performance (Macrae et al., 2004). Our previous study attempted to characterize the neural correlates of self-referencing in older adults compared to younger adults during encoding of adjectives. Using a subsequent memory paradigm (Paller and Wagner, 2002), activity was compared at the initial time of encoding for words later remembered compared to words later forgotten (Gutchess et al., 2010). Results were surprising in that no regions converged across age groups to support the encoding of information into memory. Regions, including superior mPFC, anterior and posterior cingulate, and left inferior prefrontal cortex, exhibiting subsequent memory effects for other person judgments in older adults were associated with forgetting in the self-referential condition for young adults. These findings were unexpected, as previous work implicated mPFC across age groups when making judgments of self vs. others across the age groups (Gutchess et al., 2007) and for subsequent memory in young adults (Macrae et al., 2004). Other neural evidence also suggests that older adults should converge with younger adults with some similar components implicated in self-referencing. Dorsal medial prefrontal cortex was implicated across the age groups for accurate subsequent source memory (Leshikar and Duarte, 2013). With ERP, an earlier emerging old-new component supports self-referential encoding across both age groups (Dulas et al., 2011).
Our previous study that did not find convergence across the age groups employed a typical self-referencing paradigm in which older and younger participants were presented with adjectives at encoding and were asked to make a yes/no response regarding the orienting condition indicated for the trial. The three orienting conditions were the self condition, the other condition, and the case condition. Encoding was followed by a surprise recognition task outside of the scanner. It was predicted that in both younger and older adults, the mPFC would be preferentially activated at encoding during self-referential trials compared to other-referential trials, resulting in a subsequent remembering effect (i.e. greater activity in the mPFC during encoding reflects later memory for the item). However, the results indicated reversals in patterns of activity across age groups rather than failure of one group to differentially engage regions for successful versus unsuccessful encoding. The younger adults exhibited subsequent forgetting effects in all regions of interest (left inferior frontal, left superior mPFC, anterior cingulate, right posterior cingulate) for self-referenced items, and subsequent remembering effects in all regions for other referenced items. The older adults demonstrated a reverse pattern of activity in which they showed remembering effects in all regions of interest for self-referenced items, and forgetting effects in all regions of interest for other-referenced items.
These findings could be the result of fundamental differences between younger and older adults in strategies and attention to incoming information. It is possible that older adults engage elaborative processes that benefit memory for the self while young adults use the same processes to encode information for others (Gutchess et al., 2010). However, this contradicts previous research which has shown that both younger adults and older adults exhibit subsequent memory effects for self referenced information (Glisky and Marquine, 2009, Gutchess et al., 2007) and engage the same region for subsequent source memory (Leshikar and Duarte, 2013).
It is also possible that the task design contributed to the pattern of findings in the Gutchess et al. (2010) paper. Because the task paradigm incorporated three conditions in an intermixed pseudorandom design, it is possible that interference across conditions, or task switching demands, impacted the engagement of mPFC. Participants may have made the wrong judgment, or making judgments about other people could differentially impact how older adults make judgments about the self. The identification of dorsal mPFC and anterior cingulate (ACC) in the prior study is consistent with research revealing that these regions can be engaged when thinking about dissimilar vs. similar others (Mitchell et al., 2006), which could suggest that participants thought about themselves in a relative manner. Another concern with the prior data is that there were relatively few forgotten trials in the young adults; this could have contributed to our failure to find robust subsequent memory effects.
In the current study, we utilized the same subsequent memory paradigm as our prior study, except that we sought to reduce the potential for interference by eliminating the other and the case conditions. By maximizing the number of trials associated with self-referencing we hoped to parse out the brain regions that are active in younger and older adults exclusively during the encoding of self-referenced information. We also wanted to acquire a large number of remembered and forgotten self-referencing trials to better power the comparisons. To achieve this, we employed subsequent recall and recognition tasks (rather than only a subsequent recognition task) in order to increase the number of forgotten items, as should be the case for free recall.
Section snippets
Results
Two analyses were conducted on the fMRI data to compare younger and older adults, based on items later free recalled and items later recognized.
Discussion
Across analyses based on recall and recognition data, the results largely converged with prior work implicating mPFC with thinking about the self in younger and older adults (Gutchess et al., 2007) and with subsequent memory for information related to the self in young adults (Macrae et al., 2004). While the precise locus of the activations differed across the analyses, successful encoding as assessed with recall and recognition measures robustly engaged mPFC across both age groups. These
Participants
Seventeen young (ages 18–35; 10 females) and sixteen older (ages 66–83; 10 females) participants volunteered in this study in exchange for monetary compensation1. See Table 3 for participant characteristics. Due to insufficient numbers of trials, one young adult was removed from analyses of recall data (but included in recognition analyses) and two young adults and one older adult were removed
Introduction to Experiment 2
To directly investigate the impact of thinking about others on the ways in which one remembers self-relevant information, we directly compared conditions in which younger and older participants only made judgments about the self (comparable to the present fMRI study) to a condition in which younger and older alternated between judgments about the self and other. We included additional conditions that enhanced the relativity with which one made judgments of the self, including making judgments
Results
Recognition accuracy was compared in response to the Self prompts (both general and relative), as these were the conditions completed by all participants. We employed hit rates, as there was only one pool of lure items so that condition-specific false alarm rates did not exist. Hit rates were compared based on the level of self-descriptiveness judged at encoding, by dividing participants’ ratings of how often the word described them into thirds (low, middle, and high).
We conducted a 2×2×2×2
Discussion
Experiment 2 provides evidence that older adults are more affected than young adults by the social context in which they make judgments, and that this impacts the effectiveness of their memory processes. Young adults’ memory performance is relatively unaffected by the different conditions under which they make judgments about the self. In contrast, older adults performance varies based on the social context of the task in which they make judgments of the self. When the social context of the
Participants
A final sample of 33 young (M age=20.58, SD=1.26) and 30 older (M age=77.06, SD=5.73) adults participated in the study. An additional 9 participants were excluded from data analysis because they did not have ratings in all levels for all conditions. Younger adults (M=79.06, SD=10.73) had higher digit comparison scores than older adults (M age=57.70, SD=13.41), t(62)=7.01, p<.001. Older adults (M=35.72, SD=3.38) had higher Shipley vocabulary scores than younger adults (M=31.22, SD=2.66), t
General discussion
Using measures of recall and recognition, we present evidence that medial prefrontal cortex can support successful self-referential encoding for both younger and older adults. In contrast to prior work that employed both self and other person judgments, minimal age differences emerged when participants made only judgments of the self. We suggest that thinking about others induces differences across the age groups in terms of how one reflects upon the self. As we suggested for our prior fMRI
Acknowledgments
We gratefully acknowledge experimental assistance from Allie Indeck, Maya Siegel, Christine Hosey, Deborah Chamama, and Brian Dahlben. This research was funded by National Institute on Aging (Grant R21AG032382), and portions of the research were conducted while A.H.G. was a fellow of the American Federation for Aging Research. The Athinoula A. Martinos Center for Biomedical Imaging is supported by the National Center for Research Resources (Grant P41 RR14075) and by the MIND Institute.
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2019, NeuropsychologiaCitation Excerpt :Despite structural and functional neuroanatomical changes in healthy aging (Cabeza, 2002; Cabeza and Dennis, 2012; Eyler et al., 2011; Park and Gutchess, 2005; Raz, 2000; Reuter-Lorenz and Lustig, 2005; Turner and Spreng, 2012), the medial prefrontal cortex has been shown to remain relatively preserved (Gutchess et al., 2007a; Hedden and Gabrieli, 2004; Mather, 2003). Neuroimaging studies of the SRE in healthy older adults have likewise found activation of cortical midline structures (Genon et al., 2014; Gutchess et al., 2007a, 2010; 2015; Kalenzaga et al., 2015). Neuroimaging research investigating the SRE in aMCI is limited but provides additional insight into the brain-behaviour relationships governing the phenomenon in this population.
Shared Mechanisms May Support Mnemonic Benefits from Self-Referencing and Emotion
2018, Trends in Cognitive SciencesCitation Excerpt :Thus far, fMRI findings indicate that similar neural regions contribute to the benefits from self and emotion in younger and older adults. For example, younger and older adults engage MPFC when making judgments and encoding self-referential material into memory [71,72], or when viewing and encoding valenced information [68–70]. In terms of ERP measures, a handful of ERP studies have investigated the response of the LPP to emotional information with age, finding that the LPP is modulated during viewing and encoding of emotional information by younger and older adults [89–91], although there can be age differences in the emotional valence of the information that is prioritized (Box 1).
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2017, CortexCitation Excerpt :As such, self-referential encoding promotes episodic memory retrieval by enhancing not only item memory, but also source memory. The robustness of the SRE has been demonstrated across the lifespan in healthy individuals (Glisky & Marquine, 2009; Gutchess, Kensinger, Yoon, & Schacter, 2007; Gutchess et al., 2015; Leshikar, Dulas, & Duarte, 2015). Importantly, while older individuals typically show age-related decline in source memory accuracy (Johnson, Hashtroudi, & Lindsay, 1993; Yonelinas, 2002), recent work has found that these deficits are ameliorated for source information that has been encoded with reference to the self (Leshikar & Duarte, 2013; Leshikar et al., 2015).