Elsevier

Neuropsychologia

Volume 93, Part A, December 2016, Pages 289-300
Neuropsychologia

The role of cue detection for prospective memory development across the lifespan

https://doi.org/10.1016/j.neuropsychologia.2016.11.008Get rights and content

Highlights

  • Cue detection is a relevant key mechanism for prospective memory development.

  • Cue detection is associated with multiple ERP components (N1, N300, P3b).

  • Adolescents and young adults outperformed old adults in the prospective memory task.

  • Adolescents showed efficient cue detection in early (N1) but not later ERPs (P3b).

  • Old adults showed reduced attentional processing of prospective memory cues.

Abstract

Behavioral findings suggest an inverted U-shaped pattern of prospective memory development across the lifespan. A key mechanism underlying this development is the ability to detect cues. We examined the influence of cue detection on prospective memory, combining behavioral and electrophysiological measures, in three age groups: adolescents (12–14 years), young (19–28 years), and old adults (66–77 years). Cue detection was manipulated by varying the distinctiveness (i.e., how easy it was to detect the cue based on color) of the prospective memory cue in a semantic judgment ongoing task. Behavioral results supported the pattern of an inverted U-shape with a pronounced prospective memory decrease in old adults. Adolescents and young adults showed a prospective memory specific modulation (larger amplitudes for the cues compared to other trials) already for the N1 component. No such specific modulation was evident in old adults for the early N1 component but only at the later P3b component. Adolescents showed differential modulations of the amplitude also for irrelevant information at the P3b, suggesting less efficient processing. In terms of conceptual implications, present findings underline the importance of cue detection for prospective remembering and reveal different developmental trajectories for cue detection. Our findings suggest that cue detection is not a unitary process but consists of multiple stages corresponding to several ERP components that differentially contribute to prospective memory performance across the lifespan. In adolescents resource allocation for detecting cues seemed successful initially but less efficient at later stages; whereas we found the opposite pattern for old adults.

Introduction

Prospective memory describes the ability to remember and execute delayed intentions. Typical prospective memory tasks in real life are, for example, calling a friend on his birthday or taking medication every morning before breakfast. These examples highlight the importance of intact prospective remembering in everyday life (cf. Crovitz and Daniel, 1984; Kliegel and Martin, 2003). Remembering delayed intentions requires the fulfillment of several sub-processes. Before its execution, the intention has to be encoded and then stored in memory while other activities—the so-called ongoing task—are being performed. At the appropriate moment, the intention has to be retrieved from memory, the ongoing task has to be inhibited, and the person has to switch to executing the intention (Kliegel et al., 2011). Within this complex process, the detection of the appropriate moment plays a key role in successfully remembering delayed intentions and seems to crucially influence the development of prospective memory performance on both ends of the lifespan. Therefore, the present study will focus specifically on this part of the process. Detecting the appropriate moment is labeled the prospective component by Einstein and McDaniel (1990). They also conceptualized a second component, the retrospective component, that characterizes processes of retrieving the intention from memory (Einstein et al., 1992). Both components are associated with different neurocognitive domains. The prospective component is related to executive functioning whereas the retrospective component is linked to episodic memory (McDaniel and Einstein, 2011, McDaniel et al., 1999). In behavioral experiments it is difficult to isolate the prospective component because the correct task response (e.g., pressing a specific button on the keyboard) requires both detection of the cue and retrieval of the action. To focus on the prospective component, we therefore manipulated this component directly in our experimental task. As well, we used the electroencephalogram (EEG) to investigate cue detection at a high temporal resolution and isolate it from retrieval processes.

Previous research on the development of prospective memory performance suggests an inverted U-shaped function over the lifespan. There is a rise in performance from childhood to adulthood and a later decline with increasing age in old adulthood (Kliegel et al., 2008a, Mattli et al., 2014, Mattli et al., 2011, Maylor and Logie, 2010, Zimmermann and Meier, 2006, Zöllig et al., 2010, Zöllig et al., 2007). Early indications of successful prospective memory are already evident in preschoolers aged three years (Kliegel and Jäger, 2007). During school age (Kliegel et al., 2013) and adolescence (Wang et al., 2011) prospective memory performance improves further. The development of prospective memory is linked to the development of executive functions (Kerns, 2000, Kliegel et al., 2013, Mahy et al., 2014, Shum et al., 2008, Ward et al., 2005), which could indicate improved efficiency of the prospective component and more efficient cue detection over the course of childhood. However, there is also empirical evidence for the relevance of the retrospective component for the development of prospective memory abilities during childhood (Kliegel and Jäger, 2007, Mattli et al., 2014, Smith et al., 2010, Zöllig et al., 2007). A few studies targeted development of prospective memory in adolescence (Altgassen et al., 2014, Bowman et al., 2015; Wang et al., 2011; Zimmermann and Meier, 2006; Zöllig et al., 2007) which generally found lower prospective memory performance in adolescents compared to young adults when there were high attentional and strategic demands (see Zimmermann and Meier, 2006 for an opposite finding). This indicates that the prospective component is not fully functioning in adolescents compared to young adults.

During adulthood, prospective memory performance starts to decrease again (Maylor, 1998, Maylor and Logie, 2010). In old adulthood, the decline in prospective memory performance is accompanied by the general age-related decline of executive functions and episodic memory (Maylor and Logie, 2010, Park and Reuter-Lorenz, 2009, Shing et al., 2008) suggesting decreases in both the prospective and retrospective component. However, it seems that the impact of the prospective component on the reduction of prospective memory performance is stronger than that of the retrospective component (Cohen et al., 2003, Cohen et al., 2001). Support for this hypothesis comes from studies investigating the effects of focality. Focality is a task characteristic that indicates whether an ongoing task and a prospective memory task share the same processes (focal) or rely on different processes (non-focal). Non-focal tasks are considered to demand more resources and impede cue detection (McDaniel and Einstein, 2000), given that the detection of the cue requires increased monitoring—in the sense of more resources being allocated to detect the cue—compared to focal tasks. Meta-analytic studies consistently showed stronger age-related decline for non-focal tasks than focal tasks (Ihle et al., 2013, Kliegel et al., 2008b).

An inverted U-shaped pattern of prospective memory development is strongly suggested by studies focusing either on the development in children and adolescents or old adults. However, less than a handful of studies have implemented an actual lifespan approach. In order to understand better the developmental mechanisms that drive the course of prospective memory ability across life, it is therefore instrumental to consider both ends of the lifespan within the same study. Moreover, by studying multiple age groups on the same task paradigm, variance due to differences in task specific processes—and which complicates comparisons between different studies—can be avoided (Craik and Bialystok, 2006).

From a descriptive perspective, the existing lifespan studies (Mattli et al., 2014, Mattli et al., 2011, Zimmermann and Meier, 2006, Zöllig et al., 2007) confirmed an inverted U-shaped pattern of prospective memory development across the lifespan. However, they disagreed on the possible underlying mechanisms of this trajectory suggesting a different impact of the prospective versus the retrospective component for the rise and fall of prospective memory across the lifespan: In young children, the prospective component seems to be not yet fully developed compared to young adults and might contribute to the age-related differences (Mattli et al., 2014, Zimmermann and Meier, 2006). More precisely, young children showed difficulties in identifying the correct prospective memory cue. Regarding the retrospective component in children, the results are mixed showing reduced functioning (Mattli et al., 2014) or no differences (Zimmermann and Meier, 2006) compared to young adults. In adolescents the prospective component seemed already well developed showing no differences in cue detection compared to young adults (Mattli et al., 2014, Zimmermann and Meier, 2006). Similarly, Zöllig et al. (2007) demonstrated that the attenuated performance in adolescents in their study was attributable to the retrospective component and not to processes of the prospective component. For old adults, the studies showed a decline in prospective memory performance compared to young adults that was attributable to both components. However, although Mattli et al. (2014) found reduced performance rates for the retrospective component in some age groups, they argued that the decrease in the prospective component was stronger for prospective memory development across the lifespan, emphasizing the role of cue detection. To date however the prospective component has not itself been manipulated experimentally in a lifespan sample.

In addition to behavioral results, Zöllig et al. (2007) and Mattli et al. (2011) investigated the electrophysiological correlates of prospective memory. Two main event-related potentials (ERPs'; for an overview see West, 2011) were targeted in these studies with respect to prospective memory: the N300 (representing the prospective component) and the parietal positivity (linked to the retrospective component). The N300 is a negativity over occipital electrodes that occurs within 300 ms and 500 ms after stimulus onset, and shows higher amplitudes for prospective memory hits compared to ongoing task hits (West et al., 2001, West and Ross-Munroe, 2002). At about the same time as the N300 the frontal positivity is elicited, which is assumed to be a correlate of switching from the ongoing task to the prospective memory task (Bisiacchi et al., 2009). Together, the N300 and the linked frontal positivity are assumed to be neural correlates of cue detection, and thus represent the prospective component (West, 2011). The second ERP component that appears to be related to (mostly retrospective) aspects of prospective memory is the parietal positivity, which occurs between 400 ms and 1200 ms after stimulus onset. The parietal positivity also differentiates prospective memory cues and ongoing task trials (West and Ross-Munroe, 2002, West et al., 2003b) indicating its relevance for prospective remembering. The parietal positivity is assumed to represent the neural processes of realizing delayed intentions (i.e., retrospective component). It consists of three subcomponents: P3b, parietal old-new effect and the prospective positivity (West, 2011). The P3b is a sustained positivity from the P3 family that reflects the detection of low probability cues like oddball targets and prospective memory cues (Donchin and Fabiani, 1991, West, 2011). Moreover, the P3b is sensitive to the task relevance of an event (Kok, 2001). Therefore it is not as specific to prospective memory cues as the other components like the prospective positivity (West and Wymbs, 2004). The prospective positivity is a sustained positivity occurring after the P3b. It is assumed to be associated with the configuration of the prospective memory task set after cue detection (Bisiacchi et al., 2009, West, 2011). Finally, the parietal old-new effect, an enlargement of the P3b, is assumed to reflect the recognition of the prospective memory cue (West and Krompinger, 2005, West et al., 2007).

Results of earlier developmental studies on these ERP components—including the two lifespan studies—suggest a differential influence of cue detection (expressed as N300) and retrieval processes (expressed as parietal positivity) on age differences (Bowman et al., 2015, Mattli et al., 2011, West and Bowry, 2005, West and Covell, 2001, West et al., 2003a, Zöllig et al., 2007). Whereas amplitudes of the N300 seem to be higher in children compared to young adults (Mattli et al., 2011), no differences were found between adolescents and young adults (Bowman et al., 2015, Zöllig et al., 2007). Thus, processes of cue detection (i.e., prospective component) might still be developing during childhood reaching adult-like levels in adolescents. On the other end of the lifespan, in old adults, results regarding the N300 are mixed with some studies reporting attenuated amplitudes in older compared to younger adults (West and Bowry, 2005, West and Covell, 2001, West et al., 2003a) and others not finding any age-related differences (Mattli et al., 2011, Zöllig et al., 2007). However, when focusing only on missed prospective memory cues, Mattli et al. (2011) found a modulation of the N300 in old compared to young adults, suggesting that prospective memory errors—or reduced performance—might be linked to difficulties in cue detection. Amplitudes of the parietal positivity (representing retrieval processes), specifically of the prospective positivity subcomponent, are consistently higher in children (Mattli et al., 2011) and adolescents (Bowman et al., 2015, Zöllig et al., 2007) compared to young adults. Smaller amplitudes were shown in old adults compared to young adults in some studies (West and Bowry, 2005, West and Covell, 2001, Zöllig et al., 2007; however, see Mattli et al., 2011; West et al., 2003a for no age differences for the parietal positivity). Thus, retrieval processes (i.e., retrospective component) are implicated in both the rise and the decrease of prospective memory across the lifespan. In summary, the current literature indicates mostly converging results regarding the parietal positivity that is the neural correlate for intention retrieval (i.e., retrospective component) but contradictory results for the N300 that is the neural correlate for cue detection (i.e., prospective component). Cue detection may involve different age-related processes that are more difficult to uncover by only comparing variations in the amplitudes of the N300. Using a principal component approach it has been suggested that different neural generators are involved in the N300 and that these generators vary between young and old adults (West and Bowry, 2005, Zöllig et al., 2007). However, all of these studies lack an experimental manipulation of cue detection to directly disentangle the different processes involved in cue detection and how these processes may vary across the lifespan.

In order to clarify the precise role of cue detection in the development of prospective memory abilities, we manipulated the distinctiveness of the prospective memory cue in our study. A distinct cue is one that is either special based on prior knowledge or in contrast to the environment within which the cue is embedded (e.g., the ongoing task). Conceptually, the manipulation of distinctiveness was motivated by McDaniel and Einstein (2000), who propose in their multiprocess theory that more distinct cues should capture attention more easily than less distinct cues (see also Schmidt, 1991). Distinctiveness should therefore affect cue detection directly, as well as associated processes such as shifting attention towards intention retrieval. These processes concern the prospective component rather than the retrospective component. Three studies have previously manipulated prospective memory cue distinctiveness and analyzed the corresponding ERPs in young adults (Chen et al., 2009, Cona et al., 2015, West et al., 2003b). For example, Cona et al. (2015) investigated the influence of emotional valence of prospective memory cues which has been shown to reduce age differences in a similar way as perceptually distinct cues (e.g., Altgassen et al., 2010). Cona et al. (2015) found increased processing of emotional prospective memory cues on the neural level by an early frontal positivity and the parietal positivity. Similarly, Chen et al. (2009) found larger sustained positive frontal activation for distinct compared to non-distinct prospective memory cues. They argued that working memory demands might have allocated more resources in the non-distinct condition resulting in a smaller positivity. In the study by West et al. (2003b), the authors manipulated the perceptual distinctiveness of the prospective memory cue within the ongoing task. They found reduced amplitudes for the N300 and the P3b in task conditions with non-distinct cues compared to distinct cues, indicating reduced cue detection and cue categorization processes in the non-distinct condition.

The present study was aimed at two objectives. Firstly, to explore the development of prospective memory across the lifespan by investigating adolescents, young and old adults within one study using the same paradigm. Secondly, to investigate developmental differences in prospective memory by experimentally manipulating the prospective component—in particular cue detection—by systematically varying the distinctiveness of prospective memory cues. Previous research suggests two possibilities of how cue detection could be affected by distinctiveness in different age groups. According to the results by Zöllig et al. (2007), the manipulation of distinctiveness should mainly impact old adults, especially in the non-distinct condition. However, according to Zimmermann and Meier (2006), distinctiveness should influence cue detection in both adolescents and old adults. Furthermore, the study by Wang et al. (2011) suggests that adolescents should show reduced prospective memory especially in the non-distinct condition that involves more controlled attention to detect the prospective memory cue.

One critical aspect in assessing behavior and ERPs of prospective memory is the imbalance between the frequent ongoing task trials and the rare prospective memory task trials. Specific prospective memory modulations could also be caused by the pure rareness of the prospective memory cues. To avoid this limitation we implemented deviant but irrelevant ongoing task control trials with the same frequency as the prospective memory task. Thus, differences in prospective memory specific modulations should be detectable independently of perceptual stimuli features, which allows for a more detailed exploration of processes of prospective cue detection.

In order to examine in detail the process underlying cue detection we used electrophysiological methods to isolate the N300 related previously with prospective memory cue detection. We expected that if cue detection is responsible for age differences in prospective memory performance, the N300 should be especially modified in the non-distinct condition in adolescents and old adults compared to young adults.

Moreover, we aimed at investigating the P3b associated with the processing of rare stimuli and distinctiveness (Donchin, 1981, Donchin and Fabiani, 1991, Gajewski et al., 2008). However, the P3b is not only evoked by rare events but it is consistently enhanced by task-relevant events or actions which are intentionally controlled and its amplitude is affected by priority or emphasis instruction (Kok, 2001). In order to distinguish between event frequency and task relevance impact on the P3b prospective and control trials were compared. If the P3b is responsive to event frequency only, we expect the same P3b pattern in prospective and control cues as both events occur with the same frequency. If task relevance predominantly affects the P3b amplitude, we expect larger amplitudes in prospective memory than control trials.

Extending previous approaches, we also analyzed the visual N1 component for top-down visual discrimination processes that should be related to cue detection. The visual N1 is an early occipito-temporal component occurring about 150 ms that reflects processes of stimulus discrimination within the focus of attention (Vogel and Luck, 2000). Based on the reported literature, we would expect an increase of the N1 amplitude from adolescents to old adults (De Sanctis et al., 2008, Schapkin et al., 2014, Wild-Wall et al., 2008, Yordanova et al., 2004). Moreover, an enhanced N1 was related to larger amount of attentional resources towards a relevant stimulus (Vogel and Luck, 2000). Therefore, whenever a prospective cue has been recognized as a task relevant stimulus the N1 amplitude should be amplified relative to less relevant events like frequency control trials.

Section snippets

Participants

In total, 80 participants took part in the study: 26 adolescents aged 12–14 years, 27 young adults aged 19–28 years and 27 old adults aged 66–77 years. Like in other lifespan studies, the adolescent sample covered a smaller age range than both adults sample to ensure homogeneous groups and comparable task demands for all age groups. One old adult had to be excluded because of low cognitive abilities and one young adult discontinued the experimental session because of headaches. The final sample

Behavioral results

Fig. 2 depicts the behavioral performance rates for the prospective memory task and the ongoing task.

Discussion

The aim of the present study was to investigate the development of prospective memory across the lifespan and to examine the underlying neural mechanisms that might explain the age differences obtained across the lifespan. In particular, we targeted cue detection as a key process for remembering delayed intentions that may be especially prone to age-related effects. Cue detection refers to discovering the prospective memory cue in the environment (e.g., during an ongoing task) and conceptually

Acknowledgments

The preparation of this manuscript was supported by a grant (KL2303/6-1) from the German Research Foundation (DFG) awarded to Matthias Kliegel, Michael Falkenstein and Nele Wild-Wall. We thank Ben Meuleman (Swiss Center for Affective Sciences, Université de Genève, Geneva, Switzerland) for statistical help, Ludger Blanke (Leibniz Research Centre for Working Environment and Human Factors, Dortmund, Germany) for technical support and Manuela Einert, Franziska Berg, Claudia Meischneider, Rahel

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