Elsevier

Neuropsychologia

Volume 86, June 2016, Pages 66-79
Neuropsychologia

Age-related deficits in selective attention during encoding increase demands on episodic reconstruction during context retrieval: An ERP study

https://doi.org/10.1016/j.neuropsychologia.2016.04.009Get rights and content

Highlights

  • We measure the effect of selective attention at encoding on source memory retrieval.

  • Age-related suppression deficits lead to hyper-binding in source accuracy.

  • Older adults show enhanced late posterior negativity (LPN) ERPs during retrieval.

  • Suppression deficits increase demands on post-retrieval reconstruction processes.

  • Older adults’ source memory ability may be especially impaired in noisy situations.

Abstract

Previous event-related potential (ERP) and neuroimaging evidence suggests that directing attention toward single item-context associations compared to intra-item features at encoding improves context memory performance and reduces demands on strategic retrieval operations in young and older adults. In everyday situations, however, there are multiple event features competing for our attention. It is not currently known how selectively attending to one contextual feature while attempting to ignore another influences context memory performance and the processes that support successful retrieval in the young and old. We investigated this issue in the current ERP study. Young and older participants studied pictures of objects in the presence of two contextual features: a color and a scene, and their attention was directed to the object's relationship with one of those contexts. Participants made context memory decisions for both attended and unattended contexts and rated their confidence in those decisions. Behavioral results showed that while both groups were generally successful in applying selective attention during context encoding, older adults were less confident in their context memory decisions for attended features and showed greater dependence in context memory accuracy for attended and unattended contextual features (i.e., hyper-binding). ERP results were largely consistent between age groups but older adults showed a more pronounced late posterior negativity (LPN) implicated in episodic reconstruction processes. We conclude that age-related suppression deficits during encoding result in reduced selectivity in context memory, thereby increasing subsequent demands on episodic reconstruction processes when sought after details are not readily retrieved.

Introduction

Healthy aging is typically accompanied by episodic memory decline. This decline is disproportionately greater for context memory than item memory (Mitchell and Johnson, 2009, Spencer and Raz, 1995). Memory for contextual details of encoded events is believed to rely on frontally-mediated cognitive control processes to a greater extent than item memory (Mitchell and Johnson, 2009). These processes include elaboration of relational information during encoding and monitoring of retrieved information during retrieval. As cognitive control processes are widely believed to be disrupted by normal aging, we and others have argued that memory tasks placing high demands on cognitive control (e.g., context memory) are more likely to reveal age-related impairments (Cohn et al., 2008, Duarte et al., 2008).

Emerging evidence suggests that context memory accuracy improves for both young and older adults when their attention is directed toward task-relevant associations during encoding (Dulas and Duarte, 2013, Dulas and Duarte, 2014, Glisky and Kong, 2008, Glisky et al., 2001, Hashtroudi et al., 1994, Naveh-Benjamin et al., 2007). For example, when participants are directed to attend to the item-context associations during encoding (i.e., “Does this chair (item) suit the room (context)?”), context memory improves for both age groups, relative to attending to item-only features (i.e., “How comfortable is this chair likely to be?”) (Glisky et al., 2001). While the mechanisms supporting this benefit are not entirely clear, it is likely that focusing attention on a specific relationship between an item and its context allows for the formation of a stronger association. Because the item and context are tightly bound in memory, they are easier to recover during a memory test. Consequently, demands on cognitive control operations, which are engaged when sought after contextual details are difficult to recover, should be reduced (Cohn et al., 2008).

Event-related potentials (ERPs) are useful for investigating the time-course of neural activity associated with processes that aid in the recovery of contextual details. During retrieval, previously studied items correctly recognized as old (i.e., hits) typically show more positive-going activity than new items correctly identified as new (i.e., correct rejections). Several “old-new” effects have been linked with different aspects of memory retrieval. An early (~300–500 ms post-stimulus) effect, the “FN400,” or “mid-frontal” old-new is maximal over frontal regions and is thought to reflect familiarity-based processes (for reviews Curran, 2000, Friedman and Johnson, 2000, Rugg and Curran, 2007). A later occurring (~500–800 ms post-stimulus) “parietal old-new effect” is maximal over left parietal electrodes, greater for correct than incorrect context judgments, and thought to reflect recollection-based processing (Friedman and Johnson, 2000, Rugg and Curran, 2007 for reviews). A late onsetting (~1000 ms post-stimulus) “late-frontal old-new effect” is often right lateralized, maximal over frontal channels, and sustained for several hundred milliseconds or until the end of the trial (Cruse and Wilding, 2009, Friedman and Johnson, 2000, Senkfor and Van Petten, 1998, Wilding and Rugg, 1996). This effect is particularly evident in tasks, like context memory tasks, in which participants must evaluate retrieved information in order to make a specific memory decision. The effect is larger when judgments of memory confidence are low and when memory details are difficult to recover (Cruse and Wilding, 2009, Senkfor and Van Petten, 1998). Given its onset after ERPs of item familiarity and recognition, the late-frontal old-new effect has been associated with post-retrieval monitoring (Swick, Senkfor, and Van Petten, 2006). Finally, a late posterior-maximal negativity (new>old) “LPN” effect has additionally been observed in some context retrieval studies (see Johansson and Mecklinger, 2003 for review). The LPN is suggested to reflect processes that act to reconstruct the original episode associated with recognized items. These processes are engaged when contextual attributes are not readily recovered or require continued evaluation until or even after response.

Several studies have investigated the effects of aging on old-new effects during context retrieval with the most common observation being later onsetting and/or smaller magnitude effects in the old (Duarte et al., 2006; Dulas and Duarte, 2011; Mark and Rugg, 1998; Trott et al., 1997; Wang et al., 2012a; Wegesin et al., 2002). Interestingly, some evidence shows that even when FN400 and parietal old-new effects are relatively intact, late frontal old-new effects are reduced in older adults (Gutchess et al., 2007, Wegesin et al., 2002). This suggests that cognitive control operations such as post-retrieval monitoring may be impaired even when recollection and familiarity processes are intact. In these studies, however, no means were taken to control large group differences in performance. Consequently, the neural activity differences between age groups may have been due, at least in part, to differences in performance rather than aging, per se (reviewed in Rugg and Morcom, 2005).

Recent findings from our lab (Dulas and Duarte, 2013) and others’ (Kuo and Van Petten, 2006) have shown that context memory accuracy is enhanced and frontal old-new ERP effects are reduced when participants are explicitly directed to attend to item-context relationships during encoding. In our study, we directed young and older adults to attend to either objects only or to object-color (context) relations during encoding and measured late right frontal old-new ERPs during retrieval. Importantly, we attempted to match overall memory performance between groups by halving the memory load for older adults. We found context memory improvements and reduced right late frontal old-new effects following directed attention for both age groups, albeit with a smaller benefit in the old. In a parallel fMRI study, we identified a similar pattern of attenuation in right lateral PFC for both age groups (Dulas and Duarte, 2014). From these studies we concluded that when attention is directed toward task relevant features during encoding, context memory improves in both young and older adults. Furthermore, older adults can engage in right PFC mediated post-retrieval monitoring like young adults when performance levels are roughly similar and object – context associations are difficult to recover. Interestingly, only older adults showed a large LPN in our ERP study (Dulas and Duarte, 2013). Given the hypothesized relationship between the LPN and sensory search or episodic reconstruction processes (Cycowicz et al., 2001, Johansson and Mecklinger, 2003), we reasoned that older adults additionally engaged in these operations to support context memory performance.

Directing attention toward single item-context associations compared to non-contextual feature at encoding improves context memory performance and reduces demands on strategic retrieval operations in young and older adults (Dulas and Duarte, 2013). In everyday situations, however, we likely have multiple event features competing for our attention and our ability to successfully recover some features may vary depending on where we focused our attention during encoding. Older adults are prone to failures of selective attention originating from reduced inhibitory control (Hasher and Zacks, 1988). These failures can lead to increased binding of task-irrelevant distractors. For example, findings from paired associate learning tasks show that older adults have greater memory for picture-word pairs that are re-presented despite the words having been previously presented as task irrelevant distractors (Campbell et al., 2010). This ‘hyper-binding’ effect in which older adults are more likely to bind together irrelevant distractors and targets presented in close spatial or temporal proximity has implications for context memory tasks. In a context memory task, optimal performance is likely dependent on the ability to limit attention toward the relevant item- context relationship while ignoring and consequently not encoding irrelevant event details. Hyper-binding can adversely affect performance in traditional tests of associative memory (Campbell et al., 2010).

It is not currently known how selectively attending to one contextual feature while attempting to ignore another influences context memory performance and the processes that support successful retrieval in the young and old. The current study seeks to address this issue. During study, participants were presented with black and white objects flanked by two contextual features: a color and a scene. They were asked to attend to one of the object – context relationships (attended context) while ignoring the other (unattended context). During test, they were asked to judge each object as old or new and to determine if the color and scene contexts matched those with which the object was presented during encoding. Participants were asked to judge the confidence with which they recognized each feature. Importantly, the memory load was halved for older adults in order to more closely match performance between age groups (Rugg and Morcom, 2005).

If subjects successfully restrict their attention to the target object-context relationship, then memory accuracy and confidence for the attended context will be higher than for the unattended context. Prior research documents that the parietal old-new effect varies in magnitude with the number of episodic details retrieved (Vilberg et al., 2006). If participants successfully encode both attended and unattended contexts, the magnitude of the parietal old-new effect should be larger for those “both correct” trials. In contrast, if unattended context accuracy is very low, and participants are effectively guessing, we should not find differences in parietal old-new effect magnitude between the Attended only context correct and Both contexts correct trials. If older adults bind too many event details due to a limited ability to suppress distraction, they may show reduced selectivity in their context memory performance manifesting in greater co-dependence in accuracy for attended and unattended contexts compared to young adults. The consequence of this ‘hyper’ encoding for older adults may be reduced recollection and increased post-retrieval monitoring (right frontal) and episodic reconstruction (LPN) processes that are needed when sought after associations are not readily retrieved.

Section snippets

Participants

Participants were 22 young adults, ages 18–35 and 21 older adults, ages 60–80, recruited from the Georgia Institute of Technology and the Atlanta community and compensated with $10 per hour or class credit. All participants were right-handed, native English speakers, had normal or corrected to normal vision, with no reports of psychiatric or neurological disorders, vascular disease, use of psychiatric drugs, or any drugs affecting the central nervous system. All participants signed consent

Neuropsychological assessment results

Group characteristics and results for neuropsychological tests are shown in Table 1. Older adults exhibited significantly poorer performance as compared to the young on several tasks, including Trails A and B, Visual Recognition, Visual Reproduction, and Delayed Visual Recognition [t(41)'s>2.16, p's<0.04, d's>0.72]. There were no other significant group differences [t(41)'s<1.48, p's>0.15, d's<0.49].

Behavioral results

Table 2 presents the mean proportion of hits, false alarms, and correct context judgments for

Discussion

In the current study participants selectively attended to a target contextual feature while ignoring a co-occurring distractor feature during encoding. Thus, we investigated the effect of selective attention with competition at encoding on the processes supporting successful context retrieval in the young and old. Both young and older adults were generally successful in selectively attending to the context during encoding, as evidenced by greater memory accuracy and confidence for attended than

Acknowledgements

This study was supported by National Science Foundation Grant # 1125683 awarded to Audrey Duarte. We thank all of our research participants.

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    These authors contributed equally to the work.

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