Myriam C. Sander

Contralateral Delay Activity Reveals Life-Span Age Differences in Top-Down Modulation of Working Memory Contents

Estimates of working memory (WM) capacity increase in children, peak in young adulthood, and decline thereafter. Despite this symmetry, the mechanisms causing capacity increments in childhood may differ from those causing decline in old age. The contralateral delay activity (CDA) of the electroencephalogram, an event-related difference wave with a posterior scalp distribution, has been suggested as a neural marker of WM capacity. Here, we examine 22 children (10-12 years), 12 younger adults (20-25 years), and 22 older adults (70-75 years) in a cued change detection paradigm. Load levels and presentation times were varied within subjects. Behaviorally, we observed the expected life-span peak in younger adults and better performance with longer presentation times. With short presentation times, task load increased CDA amplitude and decreased behavioral performance in younger adults. Both effects were less pronounced in older adults. Children showed a unique pattern: Their behavioral load effects were as strong as those of younger adults, but their CDA was unaffected by load. With long presentation times, task load modulated the CDA in children and older adults but not in younger adults. These findings suggest that age-related differences in CDA reflect changes in the top-down control over WM representations.

Amplitude modulations and inter-trial phase stability of alpha-oscillations differentially reflect working memory constraints across the lifespan

Working memory (WM) capacity increases across childhood, peaks in young adulthood, and declines thereafter. Developmental and aging theories suggest that deficient inhibitory control processes in children and older adults may underlie the lower performance relative to younger adults. Recently, oscillatory alpha power (7-13 Hz) of the electroencephalogram (EEG) has been suggested as a neural marker of inhibition processes contributing to WM performance (Sauseng et al., 2009). We examined 20 children (10-13 years), 12 younger adults (20-26 years), and 20 older adults (70-76 years) in a cued change-detection paradigm. Behaviorally, we observed the expected lifespan peak in younger adults. EEG alpha power was generally reduced in older adults compared to children and younger adults. In line with previous research, hemispheric differences in alpha power related to attention and WM processes during the retention interval increased with load in younger adults. In children and older adults, lateralized alpha power increased from low to medium load conditions, but decreased for high load conditions. Furthermore, older adults showed higher inter-trial phase stability shortly after stimulus onset compared to children and younger adults. Our results show that inhibitory control processes as indexed by local alpha power modulations can be observed in children and older adults but seem to break down when WM load is high. In addition, older adults are more entrained by external stimulation what may increase a need for inhibitory control during later processing. We conclude that differences in inhibitory control processes and information uptake as reflected in amplitude modulations and inter-trial phase stability of alpha rhythms interactively determine WM constraints across the lifespan.

Binding and strategic selection in working memory: a lifespan dissociation.

Working memory (WM) shows a gradual increase during childhood, followed by accelerating decline from adulthood to old age. To examine these lifespan differences more closely, we asked 34 children (10-12 years), 40 younger adults (20-25 years), and 39 older adults (70-75 years) to perform a color change detection task. Load levels and encoding durations were varied for displays including targets only (Experiment 1) or targets plus distracters (Experiment 2, investigating a subsample of Experiment 1). WM performance was lower in older adults and children than in younger adults. Longer presentation times were associated with better performance in all age groups, presumably reflecting increasing effects of strategic selection mechanisms on WM performance. Children outperformed older adults when encoding times were short, and distracter effects were larger in children and older adults than in younger adults. We conclude that strategic selection in WM develops more slowly during childhood than basic binding operations, presumably reflecting the delay in maturation of frontal versus medio-temporal brain networks. In old age, both sets of mechanisms decline, reflecting senescent change in both networks. We discuss similarities to episodic memory development and address open questions for future research.

Age Differences in Short-Term Memory Binding Are Related to Working Memory Performance Across the Lifespan

Memory performance increases during childhood and adolescence, and decreases in old age. Among younger adults, better ability to bind items to the context in which they were experienced is associated with higher working memory performance (Oberauer, 2005). Here, we examined the extent to which age differences in binding contribute to life span age differences in short-term memory (STM). Younger children (N = 85; 10 to 12 years), teenagers (N = 41; 13 to 15 years), younger adults (N = 84; 20 to 25 years), and older adults (N = 86; 70 to 75 years) worked on global and local short-term recognition tasks that are assumed to measure item and item-context memory, respectively. Structural equation models showed that item-context bindings are functioning less well in children and older adults compared with younger adults and teenagers. This result suggests protracted development of the ability to form and recollect detailed short-term memories, and decline of this ability in aging. Across all age groups, better item-context binding was associated with higher working memory performance, indicating that developmental differences in binding mechanisms are closely related to working memory development in childhood and old age.

Inter-individual performance differences in younger and older adults differentially relate to amplitude modulations and phase stability of oscillations controlling working memory contents

Efficient encoding of relevant information and suppression of irrelevant information influence working memory (WM) performance, which is limited and declines in adulthood. A cued Sternberg WM task and electroencephalographic recordings (EEG) were used to investigate encoding and control operations in response to to-be-remembered (REM) and not-to-be-remembered (NREM) stimuli in younger and older adults. Younger and older adults selectively remembered REM items in a final recognition memory test. During early stages of stimulus processing, inter-trial phase stability was higher for REM than for NREM items in younger and older adults, presumably reflecting preferential encoding of REM items. At later stages, the oscillatory power of oscillations in the alpha/beta frequency range was higher for NREM than for REM, presumably reflecting the inhibitory top-down suppression of task-irrelevant information. Early phase stability was selectively related to working memory performance in younger adults and high-functioning older adults. The results of this study reveal the differential contributions of low-level feature binding and strategic control components to adult age differences in WM, and show that older adults with more youth-like processing dynamics tend to achieve higher levels of performance.

The two-component model of memory development, and its potential implications for educational settings

We recently introduced a two-component model of the mechanisms underlying age differences in memory functioning across the lifespan. According to this model, memory performance is based on associative and strategic components. The associative component is relatively mature by middle childhood, whereas the strategic component shows a maturational lag and continues to develop until young adulthood. Focusing on work from our own lab, we review studies from the domains of episodic and working memory informed by this model, and discuss their potential implications for educational settings. The episodic memory studies uncover the latent potential of the associative component in childhood by documenting childrens ability to greatly improve their memory performance following mnemonic instruction and training. The studies on working memory also point to an immature strategic component in children whose operation is enhanced under supportive conditions. Educational settings may aim at fostering the interplay between associative and strategic components. We explore possible routes towards this goal by linking our findings to recent trends in research on instructional design.

Using within-subject pattern classification to understand lifespan age differences in oscillatory mechanisms of working memory selection and maintenance

In lifespan studies, large within-group heterogeneity with regard to behavioral and neuronal data is observed. This casts doubt on the validity of group-statistics-based approaches to understand age-related changes on cognitive and neural levels. Recent progress in brain-computer interface research demonstrates the potential of machine learning techniques to derive reliable person-specific models, representing brain behavior mappings. The present study now proposes a supervised learning approach to derive person-specific models for the identification and quantification of interindividual differences in oscillatory EEG responses related to working memory selection and maintenance mechanisms in a heterogeneous lifespan sample. EEG data were used to discriminate different levels of working memory load and the focus of visual attention. We demonstrate that our approach leads to person-specific models with better discrimination performance compared to classical person-nonspecific models. We show how these models can be interpreted both on an individual as well as on a group level. One of the key findings is that, with regard to the time dimension, the between-person variance of the obtained person-specific models is smaller in older than in younger adults. This is contrary to what we expected because of increased behavioral and neuronal heterogeneity in older adults.

Age differences in false memory: The importance of retrieval monitoring processes and their modulation by memory quality.

Older adults are more likely than younger adults to falsely recall past episodes that occurred differently or not at all. We examined whether older adults’ propensity for false associative memory is related to declines in postretrieval monitoring processes and their modulation with varying memory representations. Younger (N = 20) and older adults (N = 32) studied and relearned unrelated scene-word pairs, followed by a final cued recall that was used to distribute the pairs for an associative recognition test 24 hours later. This procedure allowed individualized formation of rearranged pairs that were made up of elements of pairs that were correctly recalled in the final cued recall (“high-quality” pairs), and of pairs that were not correctly recalled (“low-quality” pairs). Both age groups falsely recognized more low-quality than high-quality rearranged pairs, with a less pronounced reduction in false alarms to high-quality pairs in older adults. In younger adults, cingulo-opercular activity was enhanced for false alarms and for low-quality correct rejections, consistent with its role in postretrieval monitoring. Older adults did not show such modulated recruitment, suggesting deficits in their selective engagement of monitoring processes given variability in the fidelity of memory representations. There were no age differences in hippocampal activity, which was higher for high-quality than low-quality correct rejections in both age groups. These results demonstrate that the engagement of cingulo-opercular monitoring mechanisms varies with memory representation quality and contributes to age-related deficits in false associative memory.

Youth-like precision of slow oscillation-spindle coupling promotes memory consolidation across the adult lifespan

Memory consolidation during sleep relies on the precisely timed interaction of rhythmic neural events. Here, we investigate differences in slow oscillations (SO) and sleep spindles (SP) and their coupling across the adult human lifespan and ask whether observed alterations relate to the ability to retain associative memories across sleep. We demonstrate that the fine-tuned SO–SP coupling that is present in younger adults diffuses with advanced age and shifts both in time and frequency. Crucially, we show that the tight precision of SO–SP coupling promotes memory consolidation in younger and older adults, and that brain integrity in source regions for the generation of SOs and SPs reinforces this beneficial SO–SP coupling in old age. Our results reveal age-related differences in SO–SP coupling in healthy elderly individuals. Furthermore, they broaden our understanding of the conditions and the functional significance of SO–SP coupling across the entire adult lifespan.Memory consolidation during sleep relies on the precisely timed interaction of rhythmic neural events. Here, we investigate differences in slow oscillations (SO) and sleep spindles (SP) and their coupling across the adult human lifespan and ask whether observed alterations relate to the ability to retain associative memories across sleep. We demonstrate that the fine-tuned SO-SP coupling that is present in younger adults diffuses with advanced age and shifts both in time and frequency. Crucially, we show that a 9youth-like9 precision of SO-SP coupling promotes memory consolidation across the entire adult lifespan, and that brain integrity in source regions for the generation of SOs and SPs reinforces this beneficial SO-SP coupling in old age. Our results reveal age-related differences in SO-SP coupling in healthy elderly individuals. Furthermore, they broaden our understanding of the conditions and the functional significance of SO-SP coupling across the entire adult lifespan.

Cue-related phase reset accounts for age differences in phasic alerting

Alertness is fundamental for the efficiency of information processing. A person’s level of alertness refers to the system’s state of general responsiveness, and can be temporarily increased by presenting a neutral warning cue shortly before an event occurs (Posner & Petersen, 1990). However, effects of alerts on subsequent stimulus processing are less consistent in older than in younger individuals. In this study, we investigated the neural underpinnings of age differences in processing of auditory alerting cues. We measured electroencephalographic power and phase locking in response to alerting cues in a visual letter report task, in which younger but not older adults showed a cue-related behavioral advantage. Alerting cues evoked a significant increase in power as well as in inter-trial phase locking, with a maximum effect in the alpha frequency (8–12 Hz) in both age groups. Importantly, these cue-related increases in phase locking and power were stronger in older than in younger adults and were negatively correlated with the behavioral alerting effect in the older sample. Our results are in accordance with the assumption that older adults’ neural responses may be more strongly driven by external input and less variable than younger adults’. A stronger resetting of the system in response to the auditory cue may have hindered older adults’ effective use of the warning signal to foster processing of the following visual stimulus.