Elsevier

Neuropsychologia

Volume 48, Issue 12, October 2010, Pages 3540-3553
Neuropsychologia

Individual differences in executive functioning modulate age effects on the ERP correlates of retrieval success

https://doi.org/10.1016/j.neuropsychologia.2010.08.003Get rights and content

Abstract

The present study aimed to investigate whether the level of executive functioning modulated the effects of aging on episodic memory performance and on the electrophysiological correlates of retrieval success (‘old/new effect’). We used a differential approach in which young and older adults were divided into four groups of 14 participants according to their scores on a composite executive index: young-high, young-low, old-high and old-low. ERPs were recorded while participants performed a word-stem cued-recall task. Behavioral results demonstrated that age-related deficits in memory performance were reduced but not eliminated in individuals with a higher executive functioning level. Young participants exhibited ERP old/new effects on frontal and parietal areas. At posterior sites, the effect was entirely left-sided for young-low adults while for young-high participants it was bilateral, maximal at left sites and of greater amplitude. For the old-low group, both frontally-based and parietally-based processes appeared to be affected by the aging process. They also demonstrated a late frontal negative component, which might indicate an unsuccessful additional attempt to cope with retrieval difficulties. In the old-high group, ERP effects on frontal areas were relatively intact while the parietal effect was impaired compared to young adults. However, old-high subjects exhibited earlier, larger and more symmetrical effects than did old-low adults, which was in line with their better memory performance. These findings provide some support for the executive decline hypothesis of cognitive aging by showing that neural correlates of retrieval success in episodic memory are differentially affected by aging according to executive functioning level. They are consistent with the view that a high executive functioning level may help older adults recruit a cerebral pattern which enables them to perform a memory task more efficiently.

Research highlights

▶ High executive abilities reduce age effects on episodic memory performance. ▶ Executive functioning modulates age differences on the old/new effect. ▶ Old/new effects are less affected by aging in adults with high executive abilities.

Introduction

The aim of the present experiment was to examine how executive functioning, involved in the coordination and control of cognitive operations, may modulate age-related differences in episodic memory and in the electrophysiological correlates of episodic retrieval.

Previous studies in the aging literature have consistently reported a decline in episodic memory abilities with increasing age (for reviews, see Balota et al., 2000, Craik and Jennings, 1992, Light, 1991, McDaniel et al., 2008, Zacks et al., 2000). However, age differences in episodic memory are not uniform across tasks or processes. Indeed, age-related deficits in episodic memory performance are particularly pronounced in free-recall or cued-recall tasks that require subjects to retrieve studied information in absence of or with only a fragment of the item in comparison to recognition tasks in which subjects have to identify previously presented items among new items. In addition, aging differentially alters familiarity and recollection processes that are supposed to underlie memory abilities. Familiarity processes reflect an acontextual sense that an item has been previously encountered whereas recollection involves retrieval of contextual details associated with the encoding episode. These processes can be dissociated using the Remember/Know procedure (where participants judge the subjective state of consciousness associated with the retrieved information) or source memory tasks (where participants have to recollect specific contextual details about the item such as study modality, temporal source, speaker's voice). These paradigms revealed that recollection processes are strongly impaired in older adults whereas familiarity processes are relatively intact (Yonelinas, 2002). This dissociation between familiarity and recollection explains why older adults’ memory performance is more impaired in free recall or cued-recall tasks than recognition tasks. Indeed, in recall tasks, subjects have to self-initiate the necessary processes to retrieve stored information, which requires the implementation of recollection processes that are strongly affected by aging. By contrast, in recognition tests, the judgement can be based solely on relatively intact familiarity processes since old items are re-presented in their integrality, resulting in smaller deficits. Hence, the age-related memory loss primarily affects recollection while familiarity-based judgement is relatively preserved.

Moreover, elderly adults seem to be affected by the aging process differently. The reserve hypothesis has been proposed to explain this remarkable variability in elderly adults (Christensen et al., 2008, Stern, 2002, Stern, 2003, Stern, 2009, Whalley et al., 2004). Certain older individuals exhibit severe memory impairments while others are able to maintain a high level of cognitive functioning (Christensen et al., 1999, Wilson et al., 1999, Wilson et al., 2002). In brief, the reserve hypothesis postulates that some individual characteristics provide a reserve protecting people against the deleterious effects of brain damage or the negative effects of aging on the brain. At a cognitive level, a high level of reserve may be expressed by a wide repertoire of cognitive strategies from which the individual can draw to perform a challenging task when classical strategies are no longer efficient. One important question which needs to be addressed is which brain mechanisms are involved enabling this reserve to mitigate age-related cognitive decline. Structural models propose that a high reserve might be reflected in a more extensive dendritic field or more synaptic connections (Kramer, Bherer, Colcombe, Dong, & Greenough, 2004). A more functional interpretation is that a reorganization of brain functioning may help counteract the effect of the aging process in older adults with a high reserve (Christensen et al., 2008).

Numerous neuroimaging studies have demonstrated that brain functioning is modified with increasing age. Certain older adults sometimes exhibit greater activations in some brain areas than young adults or recruit alternative brain areas and networks (for reviews, see Dennis and Cabeza, 2008, Grady, 2008, Park and Gutchess, 2005, Park and Reuter-Lorenz, 2009). For instance, the PASA model (for Posterior Anterior Shift in Aging; Davis et al., 2007, Dennis and Cabeza, 2008) has proposed that deficits of activation in posterior areas in older adults’ brain are accompanied by greater recruitment of anterior areas. Based on the finding of a positive correlation between prefrontal activity and memory performance, Davis et al. (2007) have suggested that the increase of frontal activity is a compensatory mechanism but this interpretation is still debated. In this context compensation is seen as the result of additional effort or different mechanisms, which are beneficial to performance, in older compared to young adults.

Furthermore, certain older adults sometimes tend to show a bilateral recruitment pattern in memory tasks in which the cerebral activations of young adults are strongly lateralized (see Dennis & Cabeza, 2008 for a review). This controlateral recruitment pattern in older individuals has been conceptualized in the HAROLD model (Hemispheric Asymmetry Reduction in OLDer adults; Cabeza, 2002). The age-related asymmetry reduction has been initially described on frontal regions but Cabeza (2002) has suggested that it could also be applied to temporal and parietal areas. The functional significance of this increased symmetry is still under debate. The compensation hypothesis suggests that it could reflect beneficial mechanisms serving to mitigate for age-related impairments. Indeed, symmetrical patterns of activation have mostly been observed for older adults with a high cognitive level, whereas low-performing older adults, like young adults, tend to demonstrate unilateral activations (Cabeza et al., 2002, Daselaar et al., 2003, Rosen et al., 2002). However, an alternative interpretation is that increased symmetrical distribution reflects inefficient mechanisms associated with aging (Buckner and Logan, 2002, Duverne et al., 2008, Persson et al., 2006). Even though further research is needed, an intriguing possibility is to suggest that overactivation or additional recruitment of controlateral areas may be one of the mechanisms that underlies the influence of reserve during aging. In sum, the reserve hypothesis postulates that individuals with a high level of reserve exhibit less important cognitive deficits during aging. These high-level older adults might exhibit specific brain patterns that could reflect the compensation of neurocognitive deficits observed during aging.

Several individual factors could underlie this reserve capacity. In this experiment, we focused on one specific potential factor which is the level of executive functioning. Executive functions are high level cognitive processes which supervise and control other cognitive sub-processes. They include a wide range of cognitive actions such as planning, inhibiting task-irrelevant information, mental set switching, implementing strategies, and adjusting behavior according to a feedback. Executive processes have been associated with the functioning of the frontal lobes, and more specifically, the prefrontal cortex (Luria, 1966). The executive decline hypothesis is one of the main models in the field of cognitive aging (Albert and Kaplan, 1980, Daigneault et al., 1992, Dempster, 1992, Moscovitch and Winocur, 1992, Raz, 2000, West, 1996). This hypothesis postulates that the decline in executive functioning is a hallmark of cognitive aging and may be the main mediator of age differences in cognitive abilities, particularly in episodic memory. It is based on three main lines of evidence from neurobiological and neuropsychological research. First, age-related cerebral changes (volume, resting activations and white matter atrophy) appear to be earlier and greater for the frontal cortex than other brain areas (Braver and West, 2008, Raz, 2000, West, 1996). Second, older adults exhibit large deficits in tests supposed to assess frontal executive functioning (for a review, see Zelazo, Craik, & Booth, 2004). Third, the pattern of cognitive deficits is qualitatively similar between older adults and patients with frontal damage (Spencer & Raz, 1994). For instance, both older adults and patients are strongly impaired in free-recall, source memory tasks, conscious recollection and metamemory. These findings highlight the close link between executive functions and cognitive functioning during aging.

The executive decline hypothesis seems to be particularly useful to account for episodic memory deficits during aging (Velanova, Lustig, Jacoby, & Buckner, 2007). Indeed, as explained by Moscovitch and Winocur (1992), executive functions are involved in the conscious and strategic aspects of memory performance which may operate at both encoding and retrieval phases and may thus be considered as “working-with-memory processes”, processes that improve memory functioning through the use of efficient strategies. Several studies have demonstrated that performance on executive tests is a powerful mediator of age-related deficits in episodic memory (Crawford et al., 2000, Taconnat et al., 2007, Troyer et al., 1994). The influence of executive functioning level on age-related memory differences seems particularly pronounced in resource-dependent and strategic memory conditions (Bugaiska et al., 2007, Taconnat et al., 2007). For instance, Taconnat et al. (2007) have shown that executive deficits account for the decrement of strategic retrieval in a cued-recall task. Interestingly, Glisky, Polster, and Routhieaux (1995) used a differential approach to investigate the link between executive functions and memory decrements during aging by dividing elderly individuals according to their score on a composite index of executive function. The two groups did not differ in their performance on an item recognition memory test. Conversely, older adults who had a poorer executive functioning level were impaired in the source memory task, so their recollection abilities were impaired compared to the high-executive functioning participants. Thus, in the framework of the executive decline hypothesis, executive functions appeared as a central factor accounting for memory aging, especially for recollection abilities. However, little is known about the brain mechanisms that may underlie the influence of executive functioning on memory abilities in old age.

In the present experiment, we addressed this question by investigating how executive functioning may influence age-related differences in episodic memory performance and in the electrophysiological correlates of episodic retrieval. Episodic memory abilities were assessed using a word-stem cued-recall task in which subjects had to generate the old items with only the first three letters of the item and then to give a recognition judgement on their completion. Such operations require the implementation of resource-dependent recollection processes that are impaired in older adults (Yonelinas, 2002) and that are closely related to executive functions (Bugaiska et al., 2007) so it appeared as better appropriate than recognition to explore the influence of age and executive functioning on episodic memory performance and its neural correlates.

Due to their precise temporal resolution, event-related potentials (ERPs) have been demonstrated to be a well-suited method to examine the neural correlates of age differences in episodic memory (for reviews, see Friedman, 2003, Friedman, 2008, Friedman and Johnson, 2000, Friedman et al., 2007). A consistent finding in ERP studies of memory is that ERPs elicited during a recognition memory test by previously studied and recognized items are more positive than those elicited by correctly rejected unstudied items (for reviews, see Allan et al., 1998, Friedman and Johnson, 2000, Johnson, 1995; Rugg, 1995; Rugg and Allan, 2000, Wilding and Sharpe, 2003). This so-called “old/new effect” is considered as an ERP correlate of retrieval success in episodic memory.

The old/new effect has been observed in different memory tasks and has been dissociated into several components. A great majority of ERP studies have used recognition tasks. Three main modulations have been described in recognition memory tests, assumed to index functionally distinct processes: an early frontal effect, a parietal effect and a late frontal effect, and that are differentially affected by aging. First, the early frontal effect appears bilaterally on fronto-central electrode sites, peaking at about 300–400 ms. It has been associated with familiarity-based retrieval processes. Most studies have suggested that the early frontal effect is relatively unaffected by age (Ally et al., 2008, Duarte et al., 2006, Langeslag and Van Strien, 2008, Morcom and Rugg, 2004, Nessler et al., 2007, Trott et al., 1999, Wegesin et al., 2002 but see Ally et al., 2008, Duarte et al., 2006, Guillaume et al., 2009, Gutchess et al., 2007, Wolk et al., 2009 for divergent results), which is consistent with age-invariant familiarity mechanisms during aging (Yonelinas, 2002).

Second, the parietal old/new effect onsets around 400 ms post-stimulus, persists for several hundred milliseconds, is maximal at parietal scalp sites, and is sometimes predominant on the left hemisphere. It is thought to reflect recollection processes. The effects of aging on the parietal effect have been extensively studied. Studies in which participants are only required to perform a simple recognition task have mostly reported a reduction in the magnitude of the parietal effect for older participants (Ally et al., 2008, Guillaume et al., 2009, Langeslag and Van Strien, 2008, Morcom and Rugg, 2004, Wolk et al., 2009). Conversely, the parietal effect has generally been found to be of similar magnitude in the two age groups when a contextual retrieval is explicitly requested following the recognition judgement (source memory judgement, remember/know response) (Ally et al., 2008, Li et al., 2004, Wegesin et al., 2002). These findings have been interpreted as suggesting that older adults have difficulties to spontaneously engage in recollection-based retrieval processing when not necessary for the completion of the task. However, they would be able to implement such recollection operations if they are explicitly requested. In addition, a recent study has shown that the parietal old/new effect is predominant over the left hemisphere for young adults but more symmetrically distributed over the two hemispheres for older adults when carrying out a recognition task (Duverne, Motamedinia, & Rugg, 2009). This finding is consistent with the HAROLD model (Cabeza, 2002).

Third, another component of the old/new effect, which could be related to post-retrieval processes, is sometimes present on frontal areas but begins later, generally from around 600 to 1000 ms, and in some studies with an asymmetry in favor of the right hemisphere. Results are also inconclusive about age effects on the late frontal effect with some studies reporting similar effects in both age groups (Ally et al., 2008, Li et al., 2004, Mark and Rugg, 1998, Wolk et al., 2009) while others have found reduced amplitude or even no significant effect in the waveforms of older adults (Senkfor and Van Petten, 1998, Trott et al., 1999, Wegesin et al., 2002). These divergences are not surprising since the functional significance of this component is still debated. In addition to these classical components of the old/new effect, several age-related ERP studies have reported a late inversed activity (ERPs from old items more negative than ERPs from new items) on left frontal areas in older adults’ waveforms (Langeslag and Van Strien, 2008, Li et al., 2004, Nessler et al., 2007, Swick et al., 2006). Some authors have suggested that this activity may reflect the implementation of age-specific additional retrieval attempt to compensate memory deficits (Langeslag and Van Strien, 2008, Nessler et al., 2007).

The old/new effect has also been reported in word-stem cued-recall tasks (Allan et al., 1996, Allan and Rugg, 1997, Allan and Rugg, 1998, Allan et al., 2001, Angel et al., 2009, Fay et al., 2005, Johnson et al., 1998). The sustained positivity can begin as early as 300 ms after the stimulus onset and can last one second or longer. Few studies have explored the precise components of this ERP cued-recall effect. Using a source memory paradigm, Allan and Rugg (1998) suggested the existence of at least two spatially and temporally distinct modulations: a sustained old/new effect over the anterior scalp and an effect on posterior areas, predominant on the left hemisphere. The functional significance of these components of the ERP cued-recall effect cannot be firmly claimed. A likely hypothesis is that the parietal component reflects recollection processes. The interpretation is still unclear for the frontal component but it may possibly reflect familiarity processes, at least on early periods. Thus, one may note that while the old/new effect has been described in several memory tests, it appeared also as task-dependent (Allan & Rugg, 1997). A recent study (Angel et al., 2009) investigated the ERP correlates of young and older adults in a word-stem cued-recall task. Old/new effects on frontal and parietal electrode sites were of similar amplitude in both age groups. However, at parietal electrode sites, the ERP effect was predominant over the left hemisphere in the young group, while it was symmetrical in the older group, in line with the HAROLD model (Cabeza, 2002). The finding showing that age had an impact on the old/new effect observed on parietal but not on frontal areas confirms the dissociation between frontal and parietal old/new effects (Angel et al., 2009) and also supports the idea that the parietal component reflects recollection processes. To sum up, old/new effects, in both recognition and cued-recall tasks, seem to be altered in some way during aging, in particular the parietal component supposed to reflect recollection processes. Further exploration is needed to understand the causes of the disparities between studies concerning age differences on the old/new effects. One possibility is that this inconsistency may be due to differences in participants’ characteristics across studies.

Indeed, as suggested by recent studies (Czernochowski et al., 2008, Duarte et al., 2006, Riis et al., 2008, Wolk et al., 2009), the degree of age differences in ERP memory effects is unlikely to be uniform between individuals. The influence of age on the ERPs elicited during episodic memory tasks has been found to be modulated by socio-economic status (Czernochowski et al., 2008), global cognitive efficiency (Riis et al., 2008) and memory performance (Duarte et al., 2006, Friedman et al., 2010, Wolk et al., 2009). These ERP individual differences parallel the behavioral findings of great variability in cognitive performance among older adults. In the present experiment, we focused on the individual executive functioning level as a critical factor involved in the age-related differences in the old/new effect. To date, only one ERP study has investigated the executive decline hypothesis of cognitive aging with a differential approach (Fabiani & Friedman, 1995). Using an oddball paradigm, these authors demonstrated that the scalp distribution of the P3 component, elicited in response to the detection of a deviant stimulus, varied in older participants with their performance on executive tests. Older adults with poorer executive functioning exhibited a frontal-maximal P3 distribution, whereas for those with a higher executive functioning level and for young adults the P3 was predominant on parietal areas. These findings have been interpreted as suggesting that older adults with poorer executive functioning level need to recruit frontal areas to try to compensate for their deficit. Thus, ERP activity may be altered by the individual executive functioning level. However, no previous study has investigated the impact of executive functioning on the ERP correlates of episodic memory during aging.

To sum up, our experiment aimed to investigate whether age-related differences in episodic memory performance and in the ERP correlates of retrieval success (old/new effect) would be modulated by individual differences in the age-related decrement of performance on executive tests. This was the first ERP study testing the validity of the executive decline hypothesis to explain age differences in episodic memory. We used a differential approach by contrasting subgroups of young adults and older adults according to their executive functioning level. ERPs were recorded while participants performed a word-stem cued-recall task. At a behavioral level, we expected to find age-related deficits in memory performance but which would be smaller for individuals with a high executive functioning level. At an electrophysiological level, we expected that the ERP effects would be markedly affected by aging but to a greater extent for individuals with a low executive functioning level. Numerous studies have demonstrated that old/new effects have reduced magnitude and larger latencies in older adults than young adults, thus we expected that the ERP effects would be generally delayed and of smaller magnitude for older than young participants. Given that cognitive reserve, through a high executive functioning level, is supposed to be a protective factor against neurocognitive changes, one may assume that age-related differences in the latency and magnitude of the old/new effect should be less pronounced for older adults with a high executive functioning. We also hypothesized that ERP effects observed at parietal sites would be less left-lateralized in the group of high-performing older adults than in the other groups. This prediction is consistent with our previous ERP study using a word-stem cued-recall paradigm (Angel et al., 2009) and with the compensation hypothesis of the HAROLD model (Cabeza, 2002) which postulates that high level elderly adults may recruit both hemispheres symmetrically to compensate for their neurocognitive deficits. Additionally, we used correlational and regression approaches to examine directly the mediating role of age and executive functions on memory performance and on the magnitude of the old/new effect, in competition with other potential contributing factors (processing speed, educational level, vocabulary, logical memory). According to our hypothesis, we expected that executive functioning would be the main predictor of memory performance and of the magnitude of the old/new effect.

Section snippets

Participants

Participants were 28 young adults between the ages of 20 and 30, and 28 older adults between the ages of 60 and 80. All were right-handed (as assessed by the Edinburgh Inventory; Oldfield, 1971) native French speakers, with normal or corrected-to-normal vision. They all reported to be in good physical and mental health, and to be free from medication known to affect the central nervous system. Older adults who obtained a score below 27 (maximal score: 30) on the Mini Mental State Examination

Behavioral data

Behavioral performance as function of age and executive functioning level is summarized in Table 3. Corrected recognition rates were significantly above chance in each group (Young-high: t(13) = 17.07, p < .001; Young-low: t(13) = 11.33, p < .001; Old-high: t(13): 7.93, p < .001; Old-low: t(13) = 3.19, p < .01). Analyses revealed that participants with a high level of executive functioning performed better in the cued-recall task than those with a low level of executive functioning (Corrected completion rate

Discussion

The aim of this study was to investigate whether the level of executive functioning modulated the effects of aging on episodic memory performance and on the neural correlates of processes contributing to episodic retrieval success.

From a behavioral perspective, older adults performed less well than younger subjects on the word-stem cued-recall task. The memory performance of the two groups of younger adults did not differ. However, this age-related memory deficit was reduced for individuals

Acknowledgements

This research was supported by two grants from the French Agence Nationale de la Recherche (ANR): ANR-06-Blan-0241-01; ANR-FrBr-05-008 Recollection Workshop grant (2006-2008).

The authors thank the anonymous reviewers for their helpful comments.

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