Elsevier

Neuropsychologia

Volume 50, Issue 11, September 2012, Pages 2692-2704
Neuropsychologia

Age-related differences in the neural correlates of remembering time-based intentions

https://doi.org/10.1016/j.neuropsychologia.2012.07.033Get rights and content

Abstract

The present study used event-related potentials (ERPs) to explore the effect of age on the neural correlates of monitoring processes involved in time-based prospective memory.

In both younger and older adults, the addition of a time-based prospective memory task to an ongoing task led to a sustained ERP activity broadly distributed over the scalp. Older adults, however, did not exhibit the slow wave activity observed in younger adults over prefrontal regions, which is considered to be associated with retrieval mode. This finding indicates that age-related decline in intention maintenance might be one source of the impaired prospective memory performance displayed by older adults. An ‘anterior shift’ in scalp distribution of the P3 was observed in older adults, and was related to lower levels of accuracy in prospective memory performance. This relationship suggests that possible factors responsible for age-related decline in prospective memory performance include the decreased efficiency of executive/frontal functions as well as the reduced amount of resources available for the prospective memory task.

Highlights

► We compare the ERP modulations related to time-based PM in younger and older adults. ► The prefrontal ERP modulation was observed in younger but not in older adults. ► Posterior ERP modulations were mainly expressed in older than in younger adults. ► In older adults, greater frontal P3 amplitude was related to poorer PM performance. ► Older adults had fewer resources to maintain the intentions active in memory.

Introduction

One of the cognitive functions of increasing interest in the literature on aging is prospective memory (PM), which consists of remembering to accomplish actions at the appropriate time in the future (Brandimonte, Einstein, & McDaniel, 1996). Remembering to take medication or to monitor the parameters of physical functions (e.g., blood sugar levels) are only two examples of PM activities, and underline the importance of PM for successful independent life of elderly adults.

As many theorists have noted, PM tasks involve several phases (e.g., planning an intended action, and retrieving, initiating and executing that action; Kliegel, McDaniel, & Einstein, 2000), most of which are mediated by the prefrontal system (Burgess, Gonen-Yaacovi, & Volle, 2011). As alterations in the prefrontal system have been shown to characterise cognitive aging (Raz, 2000, West, 1996), they have been assumed also to have a role in determining the age-related decline in PM (McDaniel & Einstein, 2011). Although this hypothesis seems plausible and intriguing, only a handful of studies have directly investigated the neural correlates of age-related differences in PM (Mattli et al., 2011, West and Bowry, 2005). Moreover, to our knowledge, no neuroimaging or electrophysiological study has ever explored age-related neural differences associated with the particular kind of PM known as time-based PM. Thus, the present study used event-related potentials (ERPs) to better clarify the neural correlates underpinning age-related decline in time-based PM tasks.

In general, PM tasks have been classified into two main categories: event-based and time-based tasks (Brandimonte et al., 1996). In event-based PM tasks, individuals execute an action in response to a certain event (e.g., posting a letter when a post-box is seen), whereas in time-based tasks individuals carry out the intended action at a particular time or after a time interval (e.g., taking medication at noon or every twelve hours). In both kinds of tasks, the intended actions are accomplished during performance of other ongoing activities and are retrieved without an explicit prompt from the environment.

Several models have been proposed to describe the mechanisms needed to fulfil a PM intention. The majority of these, however, focus on event-based PM (e.g., Einstein et al., 2005, Guynn, 2003, McDaniel and Einstein, 2000, Moscovitch, 1994, Smith and Bayen, 2004), whereas there is still no clear framework that completely explains the processes underlying time-based PM.

The retrieval mode plus target checking model of PM (Guynn, 2003, Guynn, 2008) was developed in the context of event-based PM and then proposed for time-based PM. According to this model, PM is supported by strategic monitoring, which entails two different mechanisms: retrieval mode and target checking. Retrieval mode is conceptualised as a neurocognitive set, continuously required to maintain the intentions activated in memory. On the other hand, target checking is a more intermittent mechanism, and consists of monitoring the environment to identify the right occasion to accomplish the intention. In the case of time-based tasks, target checking is carried out by monitoring the passage of time (e.g., by checking a clock).

Laboratory studies on PM generally agree on the deleterious effect of aging on time-based PM performance (Bastin and Meulemans, 2002, Henry et al., 2004, Jäger and Kliegel, 2008, Park et al., 1997, Uttl, 2008). One of the factors determining age-related differences in time-based PM tasks seems to be the greater involvement of self-initiated retrieval and monitoring processes relative to other kinds of memory tasks (e.g., Craik, 1986, d'Ydewalle et al., 2001, Einstein et al., 1995, Jäger and Kliegel, 2008, Mäntyla et al., 2009, McFarland and Glisky, 2009).

Craik (1986) suggested that prospective remembering is particularly sensitive to aging because it is characterised by less environmental support (e.g., explicit reminders) and more self-initiated retrieval processes. As older adults suffer a reduction in the availability of attentional and self-initiated resources, they would have insufficient resources to accomplish a PM task successfully.

An alternative, although not opposing, theory for the age-related deficits in PM tasks is the ‘goal maintenance account’ (Braver & West, 2008). According to this view, older adults have difficulties in the representation and maintenance of goal information over an extended period of time. In the case of time-based PM tasks, difficulties in maintaining the goal (i.e., the intention) can lead to failure to execute clock checks at the appropriate time and consequently to failure in correct execution of the intended action (McFarland & Glisky, 2009). Furthermore, the goal maintenance account postulates that the possible age-related problems in goal maintenance are mediated by a decline in the prefrontal cortex (PFC; Braver & West, 2008), which has been shown to play a key role in PM (e.g., Bisiacchi et al., 2011, Costa et al., 2011, Gilbert et al., 2009, Reynolds et al., 2009, Uretzky and Gilboa, 2010; for a review, see Burgess et al., 2011).

Some studies also focused on age-related differences in strategic monitoring as potential determinants of impaired time-based PM performance. To this end, they have investigated two specific measures of monitoring processes: the frequency of clock checks and the ‘PM interference effect’, which are considered to index target checking and retrieval mode, respectively (Guynn, 2003).

A series of studies found that the number of clock checks was lower for older adults relative to younger adults (Einstein et al., 1995, Park et al., 1997), whereas other studies failed to find age-related differences in the frequency of clock checking (Gonneaud et al., 2011, Jäger and Kliegel, 2008), or even observe an increased number of clock checks for older adults (Logie et al., 2004, Maylor et al., 2002). Recently Mäntyla et al. (2009) showed that the resource demands of the ongoing task might affect the number of clock checks executed by older adults. Indeed, as compared with younger adults, older adults checked the clock more frequently when the ongoing task was low demanding, but less frequently when the ongoing task was high demanding, probably because they had no sufficient resources available for time monitoring.

Another index of strategic monitoring is the PM interference effect, which represents the decline in ongoing performance when a PM task is concurrently accomplished (Marsh et al., 2003, Smith, 2010). The studies that have compared the PM interference effect between younger and older adults provided inconsistent findings (Bastin and Meulemans, 2002, Jäger and Kliegel, 2008, Logie et al., 2004, Park et al., 1997). In fact, Bastin and Meulemans (2002), Jäger and Kliegel (2008) and Park et al. (1997) did not observe age-related differences in PM interference effect. d'Ydewalle et al. (2001) found that the PM interference effect was greater for older adults relative to younger adults, whereas Logie et al. (2004) reported the reverse pattern, with older adults exhibiting a smaller PM interference effect.

A number of studies also took into account the inter-individual differences in frontal-mediated processes to explain age-related deficits in PM tasks (Bisiacchi et al., 2008, Gonneaud et al., 2011, Martin et al., 2003, McDaniel and Einstein, 2011, McFarland and Glisky, 2009). McFarland and Glisky (2009) provided, although only indirectly, a link between decline in frontal functioning and age-related impairments in time-based PM performance. Indeed, older adults characterised by low frontal functioning demonstrated lower PM performance and less frequent clock checks compared to older adults with high frontal functioning. This pattern of results suggests that functions mediated by frontal regions might be particularly involved in strategic monitoring mechanisms.

The idea that activity in the anterior PFC is associated with strategic monitoring in time-based PM tasks is consistent with recent findings with clinical populations (Kliegel et al., 2008, Troyer and Murphy, 2007, Volle et al., 2011), as well as with results from an imaging (Okuda et al., 2007) and an electrophysiological (Cona, Arcara, Tarantino, & Bisiacchi, 2012) study. Surprisingly, so far no neuroimaging evidence has been provided on age-related differences in brain activity during time-based PM tasks.

The majority of electrophysiological studies investigated the ERPs elicited by the occurrence of PM events (see West, 2011 for a review), whereas only a few studies focused on the ERPs in ongoing trials, which are reflective of monitoring processes (Chen et al., 2007, Czernochowski et al., 2012, Knight et al., 2010, West and Bowry, 2005, West et al., 2006, West et al., 2007, West et al., 2011). Most of the latter kind of studies compared the electrical brain activity elicited by ongoing trials in two conditions: when individuals merely have to perform the ongoing task (i.e., baseline block) versus when they have to concurrently fulfil a PM task. A sustained ERP activity has been found to be expressed over the frontal and posterior sites and is considered to be associated with strategic monitoring (e.g., Chen et al., 2007, Cona et al., 2012, Czernochowski et al., 2012, Knight et al., 2010, West et al., 2006, West et al., 2007, West et al., 2011).

Recent studies tried to identify the ERPs reflecting the different mechanisms that contribute to strategic monitoring (Cona et al., 2012, Czernochowski et al., 2012, West et al., 2011). Cona et al. (2012) observed that a sustained and positive activity, which was particularly pronounced over prefrontal and frontal sites, characterised the ERPs not only in an event-based task but also in a time-based task. Since such ERP activity was similarly expressed in the two PM tasks, it was thought to reflect retrieval mode. On the other hand, an enhanced positivity over occipital and parietal regions at 400 ms post-stimulus was shown selectively in the event-based task, hence it was interpreted as reflecting the allocation of attentional resources for target checking. Indeed, it is possible that time-based and event-based tasks share a similar retrieval mode mechanism but differ in the type of target checking engaged. Target checking can be closely locked to ongoing stimuli in event-based tasks, whereas it is independent from them in time-based tasks. Interestingly, Czernochowski et al. (2012) found a very similar pattern of ERP modulations using an event-based task. These were represented by an early increased positivity occurring over central sites between 160 and 210 ms post-stimulus, and a more sustained positivity distributed over frontal regions in the 600–900 ms time-window. Such sustained frontal modulation was not influenced by frequency of PM cue, thus it was considered to be associated mainly with retrieval mode. Furthermore, given that retrieval mode is a tonic state, West et al. (2011) chose to examine the ERP data in the response-to-stimulus interval showing that retrieval mode was related to slow wave activity over the frontal as well as the parietal and occipital regions.

The effect of age on ERP correlates of strategic monitoring has been examined only with respect to event-based PM and the two studies that have investigated this issue obtained partially contrasting results (Mattli et al., 2011, West and Bowry, 2005). In both studies, younger and older adults were found to exhibit slow wave activity related to strategic monitoring. West and Bowry (2005), however, showed some age-related differences in the temporal dynamic and scalp distribution of these slow waves. Specifically, as revealed by electrode saliences obtained by Partial Least Squares (PLS) analysis, in younger adults the sustained ERP modulations were expressed over frontopolar and parietal sites. In contrast, in older adults, these modulations were shown mainly over central sites. The authors suggested that younger and older adults recruited different neural generators to cope with the increased demand to support strategic monitoring. Unlike West and Bowry's findings, those from the PLS analysis carried out by Mattli et al. (2011) suggested that the sustained ERP modulations were similarly expressed in terms of timing and scalp distribution between younger and older adults.

The present study was designed to investigate age-related differences in the ERP correlates of strategic monitoring in a time-based PM task. As described in Section 1.2, several studies hypothesised that age-related deficits in monitoring processes might contribute to the impaired PM performance often displayed by older individuals (McFarland & Glisky, 2009). However, the studies that have examined age-related differences in behavioural indexes of strategic monitoring provided an inconsistent pattern of findings.

In light of this, the analysis of the ERP modulations related to strategic monitoring might represent an alternative and powerful method for investigating the effect of aging on monitoring processes. Moreover, it allows us to better clarify the neural pattern associated with the age-related decline in PM performance and monitoring behaviour. To this end, we explored the ERPs elicited by an ongoing task in younger and older adults by comparing them in two conditions: in a baseline block, where the ongoing task was performed alone, and in a PM block, in which a time-based PM task was simultaneously performed during the ongoing activity. Similar to a previous study (Cona et al., 2012), we hypothesised that an efficient retrieval mode, as assumed to be in younger adults, would be associated with a positive sustained activity, occurring roughly in the 180–800 ms time window after ongoing stimulus onset and, although broadly distributed, particularly expressed over frontal and prefrontal sites (see also Czernochowski et al., 2012).

On the other hand, if older adults have a decline in retrieval mode – i.e., in intention maintenance as conceptualised by the goal maintenance account (Braver & West, 2008) – then we expected that the amplitude of such prefrontal ERP modulations would be attenuated in older adults.

Moreover, the examination of the ERPs elicited by the ongoing task might provide new information about how younger and older differently approach to the ongoing activity, given that this seems to have an impact in modulating the effect of aging on PM performance, as observed by Mäntyla et al. (2009).

Section snippets

Ethics statement

The study was approved by the ethical committee of the Faculty of Psychology of the University of Padua and was conducted according to the principles expressed in the Declaration of Helsinki. All the participants were informed about the general procedure of the experiment and signed a written consent form.

Participants

Fifteen younger adults1

Behavioural results

The analysis of PM accuracy revealed a significant effect of Group [t(31)=2.19, p<0.05, η2=0.13], with older adults (M=55%, SD=39.92, range=0 to 100%) showing lower accuracy compared with younger adults (M=81%, SD=25.60, range=20 to 100%, Table 2). All participants were able to recall the PM instruction at the end of the experiment, and all participants gave at least one PM response during the experiment. Nevertheless, four older participants forgot to execute some PM responses and executed all

Discussion

In line with previous studies (see Henry et al., 2004, Uttl, 2008 for reviews), the present research showed a detrimental effect of age on the accuracy of time-based PM performance. The worse performance shown by older adults was accompanied by an equivalent number of clock checks between older and younger adults, as similarly found by Gonneaud et al. (2011) and Jäger and Kliegel (2008). These findings also mirrored the pattern of results observed in the high demanding ongoing condition of the

Conclusions

This study highlighted several age-related differences in neural correlates of monitoring processes employed during a time-based PM task. Importantly, older adults did not show the prefrontal sustained ERP modulation exhibited by younger adults and interpreted as reflecting retrieval mode in previous studies (Cona et al., 2012, Czernochowski et al., 2012). This finding suggests that older adults have difficulties in intention maintenance, which could be responsible for their impaired PM

Acknowledgement

This study was supported by a Grant from the Bial Foundation (146/08) to P.S.B, and by a Grant from the Italian Government MIUR no. 200879eb93_002, to P.S.B. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank Caterina Corasaniti for helping in data collection.

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