Elsevier

NeuroImage

Volume 132, 15 May 2016, Pages 116-128
NeuroImage

Age-related changes in overcoming proactive interference in associative memory: The role of PFC-mediated executive control processes at retrieval

https://doi.org/10.1016/j.neuroimage.2016.02.017Get rights and content

Highlights

  • We studied the effects of age and proactive interference (PI) in associative memory.

  • We disambiguated age-related effects on distinct prefrontal cortex (PFC) processes.

  • Left ventrolateral PFC (VLPFC) was sensitive to PI level, but not resolution accuracy.

  • Anterior and dorsolateral PFC (DLPFC) supported PI resolution and memory accuracy.

  • Age-related memory deficits were related to anterior/DLPFC but not VLPFC dysfunction.

Abstract

Behavioral evidence has shown age-related impairments in overcoming proactive interference in memory, but it is unclear what underlies this deficit. Imaging studies in the young suggest overcoming interference may require several executive control processes supported by the ventrolateral prefrontal cortex (VLPFC) and dorsolateral PFC (DLPFC). The present functional magnetic resonance imaging (fMRI) study investigated whether age-related changes in dissociable executive control processes underlie deficits in overcoming proactive interference in associative memory during retrieval. Participants were tasked with remembering which associate (face or scene) objects were paired with most recently during study, under conditions of high or low proactive interference. Behavioral results demonstrated that, as interference increased, memory performance decreased similarly across groups, with slight associative memory deficits in older adults. Imaging results demonstrated that, across groups, left mid-VLPFC showed increasing activity with increasing interference, though activity did not distinguish correct from incorrect associative memory responses, suggesting this region may not directly serve in successful resolution of proactive interference, per se. Under conditions of high interference, older adults showed reduced associative memory accuracy effects in the DLPFC and anterior PFC. These results suggest that age-related PFC dysfunction may not be ubiquitous. Executive processes supported by ventral regions that detect mnemonic interference may be less affected than processes supported by dorsal and anterior regions that directly resolve interference.

Introduction

Behavioral evidence has suggested that older adults may be particularly impaired on memory tasks that require higher levels of recruitment of executive functions (Hasher and Zacks, 1979, Johnson et al., 1993). Such tasks may include associative memory tasks in which participants must overcome proactive interference. Proactive interference is induced when previous, but no longer valid, information conflicts with current task goals. For example, difficulty remembering a friend's new email address may stem from a strong memory for their previous, but no longer valid, email address. Several studies have shown that older adults demonstrate larger susceptibility to proactive interference compared to young adults in both working memory and episodic memory tasks (Bowles and Salthouse, 2003, Jacoby et al., 2005, Jonides et al., 2000; see Lustig and Jantz, 2015 for review; Lustig et al., 2001, May et al., 1999). The neurocognitive mechanisms underlying this increased susceptibility to proactive interference in older adults are largely unknown. We will investigate these processes in the current study.

Recent neuroimaging evidence suggests that the ventrolateral prefrontal cortex (VLPFC) (BAs 44, 45, and 47) (Jonides and Nee, 2006, Nee et al., 2007, Oztekin et al., 2009), and more specifically, the left mid-VLPFC (BA 44/45) (Badre et al., 2005, Badre and Wagner, 2007), is particularly involved in overcoming proactive interference. Further, both lesion (Thompson-Schill et al., 2002) and transcranial magnetic stimulation studies (TMS) (Feredoes et al., 2011) have demonstrated that disruption of the left VLPFC results in both increased errors and increased response times in response to proactive interference in working memory tasks. It has been suggested that left mid-VLPFC supports a process referred to as post-retrieval selection, which is thought to resolve competition between multiple active representations (Badre et al., 2005, Badre and Wagner, 2007) and is suggested to be critical to the successful resolution of proactive interference (see Badre and Wagner, 2007 for review). That is, after information is retrieved, irrelevant/conflicting information must be suppressed and relevant information likely enhanced. As with the email example, when someone attempts to retrieve their friend's new email, he/she may retrieve both the old and new email addresses. To make a correct memory decision, the person must inhibit the no longer valid, but perhaps strongly encoded previous email address, and select the new, currently relevant email address. Behavioral evidence suggests that post-retrieval selection requires additional processing time, as correct responses to high interference trials are significantly slower than for low interference trials (Jonides and Nee, 2006). One cause of older adults' associative memory impairments may be that they are less likely to engage this process, and thus may incorrectly select the more salient, but no longer valid, associate. It should be noted that left mid-VLPFC is recruited with increasing selection demands across a variety of tasks (see Badre, 2008, Nelson et al., 2009 for reviews), including lexical decision-making (Gold et al., 2006) and semantic interference tasks involving competition via schematically related items (e.g. rejecting the word SLEEP when presented with BED, PILLOW, TIRED, NIGHT) (Atkins and Reuter-Lorenz, 2011). This suggests that it is engaged whenever resolution of conceptual (as opposed to motor) interference is necessary (Badre and Wagner, 2007).

Although the left VLPFC is repeatedly implicated in tasks involving proactive and semantic interference, recent research has called into question whether the left VLPFC is directly involved in this selection process, in which competition in memory is successfully resolved (Atkins and Reuter-Lorenz, 2011, Han et al., 2012, Oztekin et al., 2009). That is, while this region has been repeatedly implicated in detecting mnemonic interference, many of these studies have only analyzed correct response trials, and thus have not investigated whether this region directly supports correct resolution of interference. Alternatively, the left VLPFC may be sensitive to mnemonic interference but may not support accuracy, per se. To our knowledge, only two previous working memory functional magnetic resonance imaging (fMRI) studies have looked at this issue (Atkins and Reuter-Lorenz, 2011, Oztekin et al., 2009). In both studies, the left VLPFC showed greater activity for high interference compared to low interference trials, but did not dissociate successful from unsuccessful responses. Thus, while the left VLPFC may play a role in detection of and attempts to resolve interference between competing mnemonic representations, it may not directly contribute to successful interference resolution.

While the left VLPFC did not distinguish successful vs. unsuccessful resolution of interference, both studies showed evidence of other regions that did, including the dorsolateral prefrontal cortex (DLPFC) (Atkins and Reuter-Lorenz, 2011). In many episodic memory studies, the DLPFC has been implicated in a process referred to as post-retrieval monitoring (Achim and Lepage, 2005, Donaldson et al., 2010, Dulas and Duarte, 2012, Henson et al., 1999b, Ranganath et al., 2007, Turner et al., 2008). Post-retrieval monitoring refers to the evaluation and manipulation of the products of retrieval (Henson et al., 1999b). Previous evidence has shown that post-retrieval monitoring effects are greater when one is near his/her decision criterion (Henson et al., 2000). If demands on post-retrieval monitoring are greater when one is near his/her decision criterion, it is conceivable that the DLPFC may be sensitive to memory accuracy under conditions of high interference. Another related view of the DLPFC is that it contributes to post-retrieval decision-making, in that activity increases with the number of decisions that need to be made after a retrieval attempt (Dobbins and Han, 2006, Han et al., 2009). Under this view, correct high interference responses also may require more internal decisions (e.g. “Did I see both of these items previously? Which item was most recent?” etc.) than an incorrect response, wherein the more salient but no longer valid associate is selected.

The frontal aging hypothesis suggests that aging leads to disproportionate alterations in PFC-mediated executive control processes (West, 1996). There has been little research, however, investigating the effects of age on separable components of executive control. As stated previously, behavioral evidence has consistently demonstrated that older adults show deficits on episodic memory tasks involving proactive interference (Jacoby et al., 2005), as well as semantic interference (Koutstaal and Schacter, 1997, Norman and Schacter, 1997). Some fMRI evidence suggests that older adults show reduced left VLPFC recruitment during relational memory encoding (Addis et al., 2014) and reduced sensitivity to proactive interference in working memory (Jonides et al., 2000). Furthermore, several imaging studies investigating the effects of age on post-retrieval monitoring suggest that older adults under-recruit this process and show reduced DLPFC activity during episodic retrieval (Dulas and Duarte, 2012, Fandakova et al., 2013, Friedman, 2000). To our knowledge however, no previous studies have attempted to disambiguate the effects of age on separable executive control processes in associative memory under conditions of proactive interference. Thus, the extent to which age-related dysfunction in VLPFC and DLPFC operations contributes to older adults' susceptibility to proactive interference is unknown.

The present study investigated the effects of age on PFC-mediated executive control processes during associative memory retrieval under variable levels of proactive interference. During study, participants were shown objects paired with either a face or a scene. Each object was seen multiple times and the paired associate changed across viewings. There were two encoding conditions: High Interference and Low Interference. Interference level depended on how often an object was seen with the critical (most recent) associate vs. the lure. At test, participants were then shown each object again, as well as novel objects not seen previously. For each object, they were asked if it was old (seen previously) or new (not seen previously). They were then presented with a face and scene, and asked to determine which was most recently paired with the object.

We predicted the following:

  • 1.

    Behaviorally, associative memory accuracy would be poorer for high interference compared to low interference across age groups, while item memory accuracy would not be affected by interference. Age-related associative memory accuracy deficits may be disproportionately evident for the high interference condition, in which demands on strategic retrieval processes are high.

  • 2.

    We predicted that we would observe greater activity in the left mid-VLPFC for high interference than for low interference. However, we predicted this region would not distinguish between correct and incorrect associative memory judgments for high interference trials. This would be consistent with the suggestion that this region does not directly resolve proactive interference in service of associative memory performance.

  • 3.

    We predicted that activity in the DLPFC would be greater for correct than incorrect associative memory trials under conditions of high interference. This would be consistent with the idea that this region supports post-retrieval monitoring processes or the number of post-retrieval decisions made.

  • 4.

    While fMRI studies have demonstrated age-related alterations in VLPFC and DLPFC processes during associative memory tasks, no study has examined the differential effects of age on these processes. The present study was designed to disentangle the roles of age-related changes in these regions/processes in the detection and resolution of proactive interference in service of successful associative memory accuracy.

Section snippets

Participants

22 young adults, ages 19–35, as well as 22 older adults, ages 60–80, were recruited from local universities, science and health fairs, and community solicitation. Groups did not significantly differ in gender [χ2(1, N = 44) = 0.86, p = 0.35] or education [t(42) = 0.29, p = 0.77]. Group characteristics may be seen in Table 1. An additional young adult was excluded due to terminating the experiment early. An additional four older adults were excluded as well: one due to terminating the experiment early,

Neuropsychological assessment results

Group characteristics and results for neuropsychological tests are shown in Table 1. All participants scored within one standard deviation of age-adjusted normative averages for all neuropsychological tests. Older adults exhibited significantly poorer performance than young adults on several tests including Trails A & B, Visual Recognition, Delayed Visual Recognition, and Visual Reproduction [t(42)s > 2.38, ps < 0.03]. There were no other significant group differences [t(42)s < 1.00, ps > 0.32].

Behavioral results

Mean

Discussion

The present study investigated the effects of aging on overcoming proactive interference in associative memory. We were particularly interested in assessing the effects of aging on different PFC operations thought to be involved in detecting and overcoming proactive interference. As predicted, associative memory accuracy was poorer for high compared to low interference trials across groups. However, age-related memory deficits were relatively small (only marginally significant), and there was

Conclusions

The present study provides the first evidence that age-related associative memory impairments under conditions of high proactive interference are likely related to reduced engagement of DLPFC and anterior PFC-mediated post-retrieval monitoring and relational processes, respectively, but not reduced engagement of “lower-order” processes supported by the VLPFC. Collectively, these results suggest that the frontal lobe hypothesis likely oversimplifies the relationship between aging and the PFC (

Acknowledgments

We would like to acknowledge our participants for their time and contribution to this study. This material is based upon work supported by the National Science Foundation under Grant Number BCS-1125683 awarded to Audrey Duarte, as well as an APA Dissertation Award awarded to Michael Robert Dulas.

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