We observed widespread effects of aging on subsequent memory for self-referenced information, relative to other-referenced information. Previous studies examining subsequent memory for nonsocial information report age differences in a variety of regions including prefrontal, medial temporal, and parietal cortices. The age differences in these studies tend to be relatively focal and, although older adults may activate regions of prefrontal cortex more than young (Dennis, Daselaar, et al., 2007
; Gutchess et al., 2005
; Kensinger & Schacter, 2008
), the more common pattern is one of greater activation, or deactivation, for younger than older adults (Daselaar et al., 2003
; Dennis, Daselaar, et al., 2007
; Gutchess et al., 2005
; Miller et al., 2008
). The nature of our results is surprising because older adults show greater differences than young during self-referencing in widespread regions, and the pattern of activity in some regions reverses with age. As seen in , young adults exhibit subsequent forgetting effects for self-referenced information in anterior and posterior cingulate, and superior and inferior frontal regions. Previous research identified only subsequent memory effects. Older adults, in contrast, tend to show subsequent remembering effects in these same regions. Considering the other person condition suggests even more complex findings, with other person judgments tending to show the reverse pattern of the self judgments (i.e., if the region exhibits a subsequent forgetting effect for self, it tends to exhibit a subsequent memory effect for other) and younger and older adults again contrasting each other (i.e., one group exhibits subsequent memory effects, the other group shows subsequent forgetting effects).
As discussed in the literature, subsequent forgetting effects may reflect failures to engage encoding-related processes or to disengage from internal processes that disrupt attention-demanding tasks (Otten & Rugg, 2001
; Wagner & Davachi, 2001
). It seems surprising, then, that young adults exhibit greater subsequent forgetting effects than older adults, who are known to experience greater difficulty inhibiting irrelevant processes (Hasher & Zacks, 1988
). However, subsequent forgetting effects can also reflect the reallocation of resources in ways that support successful task performance (Daselaar, Prince, & Cabeza, 2004
), an explanation that may be more consistent with greater effects in the young adults.
While several studies identify difficulty in deactivating regions with age (e.g., Grady, Springer, Hongwanishkul, McIntosh, & Winocur, 2006
; Miller et al., 2008
; Persson, Lustig, Nelson, & Reuter-Lorenz, 2007
), our finding of reversals in which conditions engage a region across the age groups is less common. This finding may at first seem perplexing; however, our study is one of the first to contrast multiple encoding tasks in a subsequent memory design with age and this design feature could shape our results in a few distinct ways. Our results could suggest fundamental differences in the way that individuals encode information about self and others across age groups. Older adults could engage elaborative processes that benefit memory for the self but young adults may engage the same elaborative encoding processes to encode information about other people. For example, older adults could consider the self in a more normative manner, thinking about the traits they possess that are shared with many people. Young adults could adopt a similar approach when making judgments about Albert Einstein, but when making self-referential judgments, they could focus on the unique aspects of their personalities. Evaluating others who are similar or dissimilar to oneself activates distinct regions of mPFC, with similar others engaging the ventral portion of mPFC typically engaged for judgments of the self and dissimilar others activating a more dorsal mPFC region (Mitchell et al., 2006
). Our dorsal mPFC activation, depicted in , is close to that identified by Mitchell et al. (2006)
, and is present for subsequent memory for other person judgments in the young adults but for subsequent memory of self judgments in the older adults, consistent with our suggestion for age differences in elaborative encoding processes. Evidence for overall age differences in the processes engaged during self-referential judgments did not emerge in our previous study (Gutchess, Kensinger, & Schacter, 2007
) but perhaps the age groups differ only for the trials on which additional elaborative processes are engaged to support encoding.
Another possible explanation is that there may have been some interference across task conditions. Because conditions were intermixed in a pseudorandom design, the task might require considerable monitoring and attention to the task, and it is possible that participants initially referenced the incorrect target on some trials. For example, when prompted to judge whether or not a word described another person, participants could have initially attended to whether the word was self-relevant. These initial errors in orientation could have impacted later memory for the word, leading to forgetting. Younger and older adults could be differentially subject to these types of errors, consistent with findings of inhibitory deficits with age (Hasher & Zacks, 1988
). The involvement of ACC and PCC, implicated in conflict detection (Carter & van Veen, 2007
) and monitoring the internal environment (Gusnard & Raichle, 2001
), respectively, could support a case for interference. The heightened activation of ACC when judging that a word does not describe oneself (Macrae et al., 2004
) suggests that the region may also respond to conflict during self-referencing tasks. While differences in interference across conditions could contribute in part to the pattern of results, it seems unlikely to fully account for the pattern of data. Interference could explain a main effect of age, but would be predicted to affect both the self or other person conditions rather than disproportionately affecting one over the other. An alternative possibility is that potential interference between conditions actually reflects age differences in the concepts of self and other, with older adults making more normative judgments of the self that, implicitly or explicitly, reference other people. It is important to note that we are not suggesting that older adults were unable to perform the task. Accuracy is high in the case condition, the only condition with an objectively accurate answer, with both groups performing with greater than 94% accuracy3
and no significant age differences.
While age differences in interference across task conditions could operate in conjunction with other mechanisms, our suggestion of age differences in the elaborative encoding processes that support self- and other- referencing is the most parsimonious explanation at present. Because previous studies (Macrae et al., 2004
) of subsequent memory for the self included only self-reference trials and did not find subsequent forgetting effects, we suggest that the inclusion of multiple conditions contributes to the pattern of data that emerges in our study for young adults alone. Appropriate designs are needed to further explore the nature of these effects and to tease apart the underlying processes occurring in young adults alone, as well as across age groups.
Aside from exploring age differences in the memory encoding network as a function of the social and self-relevant nature of stimuli, a second aim of the study was to assess the degree to which the specificity of the mPFC response to social information was intact with age. Previous studies have identified a loss of specificity in ventral visual regions with age (Park et al., 2004
) and we questioned whether this same finding would extend to the specialized domain of social processes with age. While our exploratory analyses suggest that the mPFC response is selectively enhanced for self relative to other (as reported in Gutchess, Kensinger, & Schacter, 2007
), and particularly when the self-referenced information is later remembered, the region did not emerge in our random effects analyses. While the pattern of data is generally supportive, it requires further substantiation through a study with greater power.
Low power is a potential limitation of the present study. Participants' relatively high recognition performance in the self condition resulted in small bins of self-forgotten items (M = 14.12 for the young adults and M = 16.27 for the older adults). However, the reported results seem to be robust. In a subsample of thirteen young and fourteen elderly participants who had at least 10 items in each bin, a threshold consistent with previous studies (Harvey et al., 2007
; Kensinger & Schacter, 2007
), the results from the regions of interest are consistent with those displayed in 4
. Future investigations with more trials will be needed to assess whether age differences in the engagement of neural regions occur during successful encoding of self-referenced information, which would complement our findings of age differences primarily in subsequent forgetting effects. An additional concern is whether our study design is more robust for one age group than the other. In a subsequent memory design, trials are assigned to conditions based on each participant's distribution of responses, which could introduce systematic differences in the design across the age groups. If the designs tend to be more robust for one age group than the other, this could explain the tendency for significant subsequent memory effects in the older, but not younger, group. However, analyses of design efficiency (Smith, Jenkinson, Beckmann, Miller, & Woolrich, 2007
) do not reveal significant age differences for either of our random effects analyses5
The limited number of trials also prevented us from examining other questions of interest, such as the potential for age differences in the elaborative encoding processes for adjectives endorsed as describing oneself (or another person) compared to those that did not describe the target individual. Ventral MPFC and ACC differentially respond during “yes” and “no” responses during self-referencing (Macrae et al., 2004
; Moran, Macrae, Heatherton, Wyland, & Kelley, 2006
). Although robust age differences did not emerge in the behavioral frequency of “yes” vs. “no” responses or in the neural activity during self-referencing (Gutchess et al., 2007
), age differences could be selective to engaging neural regions during the successful encoding
of these different types of items. It is possible that our finding of age differences in regions of ACC reflect, to some extent, the contribution of endorsing an item as self-descriptive, but we lack the power to contrast “yes” and “no” responses. Future studies will be needed to fully address this question.
In conclusion, aging alters the neural activity associated with the successful formation of memories for self-referenced information. Despite relative preservation of the regions engaged during self-referential processing (Gutchess, Kensinger, & Schacter, 2007
), there are fundamental age differences in the regions tied to successful encoding of self-referenced information. Thus, though young and older adults both engage a similar network of regions during self-referential processing, the function that the regions play in modulating memory formation appears to be altered with aging. Whereas young exhibit subsequent forgetting effects in prefrontal and parietal regions, older adults tend to show subsequent memory effects in these same regions. Because of this reversal in the pattern of activity across the age groups, these changes do not seem to reflect simple age-related cognitive declines or even compensatory mechanisms. Rather, younger and older adults differ in the elaborative encoding processes engaged for self- and other-referencing. Future studies will be needed to assess the extent to which the inclusion of multiple, intermixed trial types contributes to these results. In contrast to our previous finding that young and elderly similarly engage regions implicated in self-referencing, the present data suggests that widespread age differences emerge when memories are formed while referencing the self or another person. The findings are consistent with previous literature that suggests age-related changes in the activation of regions guiding memory formation. These age differences emerge even for social information, and in spite of the effectiveness of self-referencing as a strategy to support encoding.