Elsevier

Cortex

Volume 91, June 2017, Pages 40-55
Cortex

Special issue: Research report
Age-related changes in neural oscillations supporting context memory retrieval

https://doi.org/10.1016/j.cortex.2017.01.020Get rights and content

Abstract

Recent evidence suggests that directing attention toward single item-context associations during encoding improves young and older adults' context memory performance and reduces demands on executive functions during retrieval. In everyday situations, there are many event features competing for our attention, and our ability to successfully recover those details may depend on our ability to ignore others. Failures of selective attention may contribute to older adults' context memory impairments. In the current electroencephalogram (EEG) study, we assessed the effects of age on processes supporting successful context memory retrieval of selectively attended features as indexed by neural oscillations. During encoding, young and older adults were directed to attend to a picture of an object and its relationship to one of two concurrently presented contextual details: a color or scene. At retrieval, we tested their memory for the object, its attended and unattended context features, and their confidence for both the attended and unattended features. Both groups showed greater memory for attended than unattended contextual features. However, older adults showed evidence of hyper-binding between attended and unattended context features while the young adults did not. EEG results in the theta band suggest that young and older adults recollect similar amounts of information but brain-behavior correlations suggest that this information was supportive of contextual memory performance, particularly for young adults. By contrast, sustained beta desynchronization, indicative of sensory reactivation and episodic reconstruction, was correlated with contextual memory performance for older adults only. We conclude that older adults' inhibition deficits during encoding reduced the selectivity of their contextual memories, which led to reliance on executive functions like episodic reconstruction to support successful memory retrieval.

Introduction

Healthy aging is commonly associated with declines in episodic memory (for review: Craik and Rose, 2012, Spencer and Raz, 1995). In studies of source or context memory (for review: Mitchell and Johnson, 2009, Spencer and Raz, 1995), where the memory for an item and a property of the item or initial encoding experience (e.g., location, orienting question, item color) are assessed (Johnson, Hashtroudi, & Lindsay, 1993), young adults outperform their older counterparts. This decline is found even when item memory is matched (James et al., 2016, Kensinger and Schacter, 2006, Mitchell and Johnson, 2009). Context memory is thought to rely on frontally mediated executive functions to a greater extent than item memory during encoding and retrieval (Mitchell & Johnson, 2009). This is consistent with evidence suggesting that aging is associated with greater declines in cognitive processes reliant on the prefrontal cortex (e.g., the frontal aging hypothesis) (West, 1996).

Emerging evidence suggests that explicitly instructing both younger and older adults to attend to the relationship between an item and its context increases memory for the item-context association in both groups (Dulas and Duarte, 2013, Dulas and Duarte, 2014, Glisky and Kong, 2008, Glisky et al., 2001, Hashtroudi et al., 1994, Kuo and Van Petten, 2006, Naveh-Benjamin et al., 2007). For example, directing attention to an item-color association (e.g., “Is this a likely color for this item?”) increases memory for that association over directing attention to the item alone (e.g., “Is this item smaller than a shoebox?”) (Dulas & Duarte, 2013). One possible mechanism for the memory improvement is that explicit attention strengthens the relationship between the item and its context at encoding (Uncapher, Otten, & Rugg, 2006). Another, non-mutually exclusive possibility is that the strengthened relationship reduces demands on executive functions at retrieval (Cohn et al., 2008, Kuo and Van Petten, 2006).

While many experimental tasks assess memory for an item and a single contextual feature, in the real world we are likely to have multiple features competing for our attention. The ability to recover these contextual features at retrieval is likely a product of where we directed our attention at encoding. The ability to selectively attend to relevant features and ignore the irrelevant features is reduced in older adults (Kim, Hasher, & Zacks, 2007). This reduction in selective attention is suggestive of reduced inhibitory control (Hasher & Zacks, 1988). A reduced ability to selectively attend to a specific relationship may lead older adults to hyper-bind (Campbell, Hasher, & Thomas, 2010) and show a conditional dependence (Boywitt et al., 2012, Meiser et al., 2008, Peterson and Naveh-Benjamin, 2016, Starns and Hicks, 2008) between relevant and irrelevant features during memory retrieval. A consequence of hyper-binding, in typical memory tasks, may be an impoverished memory representation for relevant contextual features. This in turn may lead to increased demands on executive functions at retrieval, such as episodic reconstruction and post-retrieval monitoring, in order to make accurate context memory decisions.

In a previous event related potential (ERP) study from our lab (James et al., 2016) we investigated contextual memory in both young and older adults where, at encoding, we directed attention to the relationship between one of two presented contexts: a color and a scene. Participants were required to direct attention to the appropriate (i.e., attended) context and ignore the other (i.e., unattended) context. At retrieval, we tested their memory for both the attended and unattended context features. We found that both groups demonstrated better memory for the attended feature, suggesting they were able to selectively attend to the appropriate context during encoding. Older adults showed conditional dependence between the two contextual features, indicative of hyper-binding, which we concluded was due to a reduced ability to inhibit the unattended context at encoding. The FN400 and parietal old-new effects were found to be similar across age groups. The FN400 has been linked to familiarity-based memory (Duarte, Ranganath, Winward, Hayward, & Knight, 2004; for review: Friedman and Johnson, 2000, Rugg and Curran, 2007) and conceptual priming (Voss, Lucas, & Paller, 2009). The parietal-old new effect is associated with recollection-based memory (Curran, 2000, Friedman and Johnson, 2000, Wilding, 2000), and can be modulated by the amount of information recollected (Vilberg, Moosavi, & Rugg, 2006). The similarity of these effects suggests that both young and older adults had intact recollection and familiarity. We found differences between young and older adults in the late posterior negativity (LPN), in which a reliably larger LPN was found for the older adults, compared to the young adults. The LPN has been linked to episodic reconstruction of the encoding episode through reactivation of context-specifying information (Cycowicz et al., 2001, Johansson and Mecklinger, 2003). We concluded that while young and older adults recollected a similar amount of information, more of this information was likely irrelevant with respect to context memory decisions for the older adults. Consequently, older adults relied on episodic reconstructive processes to a greater extent than the young in order to recover relevant contextual information.

The current study uses the data from our previous ERP study to investigate the relationships between aging and context retrieval, with neural oscillations. An advantage of investigating neural oscillations over ERPs, is that they are thought to represent both local and long range communication between cell assemblies and reflect the synchronized inhibitory and excitatory firing rates (Jacobs et al., 2007, Lee et al., 2005). These synchronized fluctuations are thought to be critical for both encoding and retrieval of long-term memory (for review: Axmacher et al., 2006, Duzel et al., 2010, Nyhus and Curran, 2010). Another advantage of investigating neural oscillations is that they may contain more information about the underling cognitive processes, as ERPs only reflect a summation of power across all frequencies, and only those that are phase locked (i.e., synchronize at the same time across all individual trials) (Makeig, Debener, Onton, & Delorme, 2004). The current study capitalizes on the additional information provided by neural oscillations to investigate age-related differences in contextual memory retrieval.

Neural oscillations are commonly grouped into specific frequency bands of interest, such as theta (4–7 Hz), alpha (8–12 Hz), and beta (12–30 Hz). Event related synchronization and desynchronization refers to an increase or decrease in power from a resting, or prestimulus, interval (Pfurtscheller & Aranibar, 1977). Both synchronization and desynchronization within these frequency bands have been shown to reflect memory performance during both encoding and retrieval (for review: Hanslmayr and Staudigl, 2014, Klimesch, 1999). Greater theta synchronization, indexed by greater mean power, for correctly identified old items compared to both forgotten items and correctly rejected new items, is consistently found within the first 1000 msec post-stimulus, although the exact latency and topography varies by study. In contrast, for both alpha and beta, greater desynchronization is commonly found ∼600 msec post-stimulus and continues through the end of the epoch (for review: Hanslmayr and Staudigl, 2014, Hanslmayr et al., 2012). Accumulating evidence suggests that these frequency bands reflect separable memory related processes (for review Hanslmayr & Staudigl, 2014). Theta increases at encoding and retrieval for remembered events have been shown to be invariant to various kinds of stimuli and task conditions (for review: Klimesch, 1999, Nyhus and Curran, 2010). It seems likely that theta rhythms reflect domain general operations that contribute to episodic memory (Guderian, Schott, Richardson-Klavehn, & Duzel, 2009). Both human and rodent research suggests that oscillations in the theta frequency band reflect interactions between the hippocampus and cortical areas including the prefrontal cortex, which facilitate encoding and retrieval (for review: Klimesch, 1999, Nyhus and Curran, 2010).

In contrast to the increases in theta synchrony that contributes to successful encoding and retrieval, alpha and beta desynchronization following stimulus onset has been associated with memory success (reviewed in Hanslmayr et al., 2012, Sederberg et al., 2003). Furthermore, alpha and beta responses are often correlated, suggesting that they reflect similar cognitive processes. Studies manipulating the strategies with which events were encoded have shown that decreases in alpha/beta power may be particularly related to semantic encoding rather than shallow encoding or other forms of elaborative processing during encoding (Fellner et al., 2013, Hanslmayr et al., 2009). Intracranial evidence suggests that the left inferior frontal gyrus and hippocampus are at least two generators of these alpha and beta encoding effects (Sederberg et al., 2003). Alpha and beta power decreases have also been linked to successful episodic memory retrieval in several studies (Duzel et al., 2010, Hanslmayr et al., 2012 for reviews). Alpha and beta power decreases as the number of retrieved items increases and varies spatially across the scalp according to the type of perceptual features associated with prior encoded events (Khader and Rosler, 2011, Waldhauser et al., 2016, Waldhauser et al., 2012).

Very little work has been done to study the effects of aging on episodic memory with neural oscillations. Some EEG evidence from a visuospatial associative encoding task suggests that age-related reductions in theta synchronization following event onset may contribute to older adults' memory impairments (Crespo-Garcia, Cantero, & Atienza, 2012). Similarly, magnetoencephalography (MEG) evidence suggests that increased stimulus-related theta power during encoding predicts relational binding success for the young but not the old in a short-term memory task (Rondina et al., 2015). By contrast, alpha and beta desynchronization was greater for the old than the young but did not support memory performance. These results are consistent with findings from short-term memory tasks showing age-related decreases in theta synchronization (Kardos et al., 2014, Karrasch et al., 2004) and increases in alpha and beta power during memory task performance (Karrasch et al., 2004, Sebastian and Ballesteros, 2012), in both encoding and retrieval. It is important to note that these studies assessed stimulus-induced changes in oscillatory power relative to baseline but did not compare oscillatory power for successful and unsuccessful memory trials (i.e., subsequent memory and old-new effects). Thus, it remains unclear how aging affects neural oscillations that underlie retrieval success.

In the current study, we assessed effects of age on neural oscillations during context memory retrieval with the data from our previously published ERP study (James et al., 2016). As discussed above, participants were directed to attend to a gray scale object and one of two concurrent contextual details (i.e., color and scene) at encoding. At retrieval, we tested their memory for the object, its attended and unattended features, and their confidence in both context judgments. Given that we found ERP evidence that older adults relied on episodic reconstructive processes at retrieval to support memory performance to a greater extent than the young, we expected to find age differences within frequency bands that reflect episodic reconstruction. A likely frequency band in which reconstructive processes might be reflected is the alpha/beta band, given its association with sensory reactivation during retrieval (Khader and Rosler, 2011, Waldhauser et al., 2012). Additionally, neural oscillations allow for investigation of non-phased locked activity, and the separation of frequency bands may reveal age-related effects in the time series that are masked by the ERP analysis.

Section snippets

Participants

The current study included the same participants from our previously published ERP study (James et al., 2016). This included 22 young (18–35) and 21 older (60–80) healthy, right-handed adults. All participants were native English speakers and had normal or corrected vision, were compensated with course credit or $10 per hour, and were recruited from the Georgia Institute of Technology and surrounding community. None of the participants reported neurological or psychiatric disorders, vascular

Behavior

Results from the neuropsychological battery can be found in Table 1, and full behavioral results and analysis can be found in James et al. (2016). In consideration of our current results, mean proportion of item hits, false alarms, and item hits associated with correct context judgments for attended and unattended features can be found in Table 2. Item memory for object stimuli was assessed with Pr: p(hits) – p(false alarms) (Snodgrass and Corwin, 1988). Pr for young adults was .67 (SD = .15),

Discussion

The current study is the first, to our knowledge, to investigate age-related differences in context memory retrieval with neural oscillations. Participants selectively attended to one of two contextual features presented concurrently during encoding, allowing us to examine the effect of selective attention during encoding on the processes supporting context memory retrieval. Both groups showed greater memory for attended than unattended contextual features. Older adults showed evidence of

Conclusion

This study provides the first evidence that age-related changes in oscillatory EEG signals during retrieval contribute to older adults' contextual memory impairments. Using a selective encoding design, we show that young and older adults can selectively attend to and encode target contextual features. Consistent with the inhibition deficit hypothesis of aging, older adults are less able to suppress co-occurring distractor features, which in turn leads to less selective and less confident

Acknowledgements

This study was supported by National Science Foundation grant # 1125683 awarded to Audrey Duarte. This research was also supported in part by a NIA Ruth L. Kirschstein National Research Service Award (NRSA) Institutional Research Training Grant, Grant # 5T32AG000175. We thank all of our research participants.

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