Age-related differences in the temporal dynamics of prospective memory retrieval: a lifespan approach

The efficiency of prospective memory (PM) typically increases from childhood to young adulthood and then decreases in later adulthood. The current study used event-related brain potentials (ERPs) to examine the development of the neural correlates of processes associated with the detection of a PM cue, switching from the ongoing activity to the prospective task, retrieval of the intention from memory or task set configuration, and strategic monitoring of the environment. The study included 99 participants that were 7.5-83 years of age. Slow wave activity related to strategic monitoring was reliable across the lifespan suggesting that all ages were able to allocate attentional resources to facilitate PM. Additionally, components of the ERPs related to cue detection, switching, and task configuration were reliable across the lifespan, suggesting that similar processes contribute to PM at all ages. In children, PM errors may have resulted from a decoupling of processes supporting cue detection and switching from the ongoing activity to the prospective element of the task. In younger and older adults, PM errors appeared to result from the failure to detect PM cues in the environment. These findings lead to the conclusion that different processes may contribute to variation in PM across the lifespan.     

The temporal dynamics of prospective memory: a review of the ERP and prospective memory literature

This review article examines the literature using event-related brain potentials (ERPs) to study the temporal dynamics of the neurocognitive processes underpinning event-based prospective memory (PM). The successful encoding of delayed intentions is associated with slow wave activity over the frontal region in younger adults and this activity is attenuated in older adults. The realization of delayed intentions is associated with distinct components of the ERPs that are associated with the detection of a PM cue in the environment (N300), the retrieval of an intention from memory (recognition old-new effect), signaling the need to switch from the ongoing activity (frontal positivity), and configuration of the PM task set (parietal positivity). The development of prospective memory across the lifespan appears to reflect development of processes associated with retrieval of the cue-intention association from memory, and executive processes related to cue detection. The final section of the review examines the nature of executive processes that support PM within the context of a theory of the supervisory attentional system.     

Neural correlates of prospective and retrospective memory

This study examines the event-related brain potential (ERP) correlates of retrieval processes in prospective and retrospective memory (i.e., recognition and cued-recall). In contrast to previous research that has compared performance on tasks measuring prospective and retrospective memory, the stimulus materials and encoding and response demands of the prospective and retrospective components of the tasks were reasonably well matched for the two forms of memory. This resulted in the primary difference between the assessments of prospective and retrospective memory being the requirement for self-initiated retrieval in prospective memory. Analyses of mean amplitude measures revealed modulations of the ERPs typically associated with prospective memory (i.e., N300 and prospective positivity) and retrospective memory (i.e., FN400, parietal positivity and frontal slow waves). Partial least squares analyses revealed one latent variable related to the retrieval of a previously studied item that contrasted retrospective hits and prospective hits from ongoing activity trials and prospective lures; and one latent variable uniquely associated with prospective hits. These findings indicate that similar neural processes support retrieval in prospective and retrospective memory and that the realization of intentions is additionally dependent on processes that are uniquely related to prospective memory.     

The role of episodic memory in controlled evaluative judgments about attitudes: an event-related potential study

Event-related potentials (ERPs) are unique in their ability to provide information about the timing of activity in the neural networks that perform complex cognitive processes. Given the dearth of extant data from normal controls on the question of whether attitude representations are stored in episodic or semantic memory, the goal here was to study the nature of the memory representations used during conscious attitude evaluations. Thus, we recorded ERPs while participants performed three tasks: attitude evaluations (i.e., agree/disagree), autobiographical cued recall (i.e., You/Not You) and semantic evaluations (i.e., active/inactive). The key finding was that the parietal episodic memory (EM) effect, a well-established correlate of episodic recollection, was elicited by both attitude evaluations and autobiographical retrievals. By contrast, semantic evaluations of the same attitude items elicited less parietal activity, like that elicited by Not You cues, which only access semantic memory. In accord with hemodynamic results, attitude evaluations and autobiographical retrievals also produced overlapping patterns of slow potential (SP) activity from 500 to 900 ms preceding the response over left and right inferior frontal, anterior medial frontal and occipital brain areas. Significantly different patterns of SP activity were elicited in these locations for semantic evaluations and Not You cues. Taken together, the results indicate that attitude representations are stored in episodic memory. Retrieval timing varied as a function of task, with earlier retrievals in both evaluation conditions relative to those in the autobiographical condition. The differential roles and timing of memory retrieval in evaluative judgment and memory retrieval tasks are discussed.     

Thalamic mediodorsal nucleus and working memory

Working memory is a dynamic neural system for temporarily maintaining and processing information. The prefrontal cortex (PFC) plays an important role in working memory. However, several evidences indicate that the thalamic mediodorsal nucleus (MD) also participates in working memory. Neurophysiological studies revealed that MD neurons exhibit sustained delay activity, which is considered to be a neural correlate of the temporary maintenance of information. Most MD neurons with delay activity represented information regarding motor responses, whereas some represented information regarding visual cues, suggesting that the MD participates more in prospective aspects of working memory, in contrast to the PFC, in which a minority participates in prospective aspects of working memory. A population vector analysis revealed that the transformation of sensory-to-motor information occurred during the earlier phase of the delay period in the MD compared with the PFC. These results indicate that reverberating neural circuits constructed by reciprocal connections between the MD and the PFC could be an important component for constructing prospective information in the PFC.     

Neural correlates of prospective memory across the lifespan

OVERVIEW: Behavioural data reveal an inverted U-shaped function in the efficiency of prospective memory from childhood to young adulthood to later adulthood. However, prior research has not directly compared processes contributing to age-related variation in prospective memory across the lifespan, hence it is unclear whether the same factors explain the 'rise and fall' of prospective remembering from childhood to later adulthood. The present study examined this question using a paradigm that allowed us to consider the behavioural and neural correlates of processes associated with the prospective and retrospective components of prospective memory. METHODS: We compared 14 adolescents, 14 young adults, and 14 old adults in a paradigm where the prospective memory task was embedded in a semantic categorization task. RESULTS: The behavioural data revealed an inverted U-shaped function with adolescents and old adults performing poorly relative to young adults. Analyses of the error data revealed that different processes may have contributed to failures of prospective memory in adolescents and older adults. This finding was supported by age differences in ERP-components for cue detection and post-retrieval processes. Additionally, source localization using LORETA revealed different patterns of neural recruitment for adolescents and older adults relative to younger adults. CONCLUSION: Our findings demonstrate that adolescents and older adults show different patterns of behavioural errors and neural recruitment for successful prospective remembering indicating that different processes may contribute to the 'rise and fall' of prospective memory across the lifespan.     

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

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.     

Frontal theta event-related synchronization: comparison of directed attention and working memory load effects

Summary. Early studies showed that long-term encoding and retrieval of new information is associated with modulation of the theta rhythm. More recently, changes in theta power amplitude over frontal electrode sites were reported during working memory, yet their relative significance in regard to attentional and memory processes remains unclear. Event-related synchronisation responses in the 4–7.5 Hz theta EEG frequency band was studied in 12 normal subjects performing four different tasks: two working memory tasks in which load varied from one (1-back task) to two (2-back task) items, an oddball detection (attention) task and a passive fixation task. A phasic theta increase was observed following stimulus apparition on all electrode sites within each task, with longer culmination peak and maximal amplitude over frontal electrodes. Frontal theta event-related synchronization (ERS) was of higher amplitude in the 1-back, 2-back and detection tasks as compared to the passive fixation task. Additionally, the detection task elicited a larger frontal and central theta ERS than the 2-back task. By analyzing theta ERS characteristics in various experimental conditions, the present study reveals that early phasic theta response over frontal regions primarily reflects the activation of neural networks involved in allocation of attention related to target stimuli rather than working memory processes.     

Word imageability affects the hippocampus in recognition memory

Concrete words, whose meanings are readily imagined, are better remembered than abstract words. However, the neural correlates of this effect are poorly understood. Here, we investigated the effect of imageability on brain activity in the medial temporal lobe (MTL) processes underlying recognition memory. We recorded event-related potentials (ERPs) via depth electrodes from within the MTL in 14 patients with drug-resistant epilepsy. Patients performed a continuous word recognition task with words of high and low imageability (controlled for word frequency). Behaviorally, recognition performance was better for high, compared to low, imageable words. Two ERP components associated with recognition memory, the AMTL-N400 and the hippocampal late negative component, showed an old/new effect, but only the hippocampal P600 showed a main effect of imageability. We suggest that the hippocampal effect of imageability in recognition memory may be associated with conceptual or pictorial information processing of concrete words.     

Getting ready to remember: the neural correlates of task set during recognition memory

Event-related potentials (ERPs) were employed to investigate the neural correlates of episodic and semantic task sets. ERPs elicited by cues signalling an upcoming recognition memory test trial showed a sustained positivity relative to those signalling an upcoming semantic test trial, lasting from 500 ms post-cue until the arrival of the test item. However, this effect was present only on the second successive trial on which subjects performed the recognition task. Thus, when episodic vs semantic tasks vary trial-by-trial, the establishment of a recognition memory task-set is not achieved within a single trial. The findings are discussed in relation to the notion of episodic retrieval mode.     

Modulation of the electrophysiological correlates of retrieval cue processing by the specificity of task demands

Retrieval orientation refers to the differential processing of retrieval cues according to the type of information sought from memory (e.g., words vs. pictures). In the present study, event-related potentials (ERPs) were employed to investigate whether the neural correlates of differential retrieval orientations are sensitive to the specificity of the retrieval demands of the test task. In separate study-test phases, subjects encoded lists of intermixed words and pictures, and then undertook one of two retrieval tests, in both of which the retrieval cues were exclusively words. In the recognition test, subjects performed 'old/new' discriminations on the test items, and old items corresponded to only one class of studied material (words or pictures). In the exclusion test, old items corresponded to both classes of study material, and subjects were required to respond 'old' only to test items corresponding to a designated class of material. Thus, demands for retrieval specificity were greater in the exclusion test than during recognition. ERPs elicited by correctly classified new items in the two types of test were contrasted according to whether words or pictures were the sought-for material. Material-dependent ERP effects were evident in both tests, but the effects onset earlier and offset later in the exclusion test. The findings suggest that differential processing of retrieval cues, and hence the adoption of differential retrieval orientations, varies according to the specificity of the retrieval goal.     

Short-term memory storage and retention: an event-related brain potential study.

This experiment was concerned with event-related brain potential (ERP) activity related to short-term storage and retention of information in working memory. Our approach was to record the ERPs elicited by a stimulus that had to be memorized while varying the number of items (1, 3 or 6) in the task stimulus. In order to distinguish between ERP effects associated with perceptual complexity and retention of information, there was a second condition in which subjects were required to search the task stimulus for a match with a previously presented item. Thus, in the search condition subjects only had to remember one item (match or mismatch). ERP activity was recorded for 2450 msec after task stimulus offset. Two long-duration components varied as a function of task and memory load: a posterior positive wave and a frontal negative wave. Posterior positive wave amplitude was directly related to information load in the memory task but was negligible in the search task. Following the posterior positive wave was a frontal negative wave which occurred at the highest load level in the memory task but was totally absent in the search task. A P3b was elicited in both tasks. P3b was sensitive to information acquisition processes, but it did not distinguish between memory retention and visual search processes. While P3b amplitude did not vary with task or load, its latency increased with load in both tasks.     

Social working memory and its distinctive link to social cognitive ability: an fMRI study

Engaging social working memory (SWM) during effortful social cognition has been associated with neural activation in two neurocognitive systems: the medial frontoparietal system and the lateral frontoparietal system. However, the respective roles played by these systems in SWM remain unknown. Results from this study demonstrate that only the medial frontoparietal system supports the social cognitive demands managed in SWM. In contrast, the lateral frontoparietal system supports the non-social cognitive demands that are needed for task performance, but that are independent of the social cognitive computations. Moreover, parametric increases in the medial frontoparietal system, but not the lateral frontoparietal system, in response to SWM load predicted performance on a challenging measure of perspective-taking. Thus, the medial frontoparietal system may uniquely support social cognitive processes in working memory and the working memory demands afforded by effortful social cognition, such as the need to track another person’s perspective in mind.     

Music training and working memory: an ERP study

While previous research has suggested that music training is associated with improvements in various cognitive and linguistic skills, the mechanisms mediating or underlying these associations are mostly unknown. Here, we addressed the hypothesis that previous music training is related to improved working memory. Using event-related potentials (ERPs) and a standardized test of working memory, we investigated both neural and behavioral aspects of working memory in college-aged, non-professional musicians and non-musicians. Behaviorally, musicians outperformed non-musicians on standardized subtests of visual, phonological, and executive memory. ERPs were recorded in standard auditory and visual oddball paradigms (participants responded to infrequent deviant stimuli embedded in lists of standard stimuli). Electrophysiologically, musicians demonstrated faster updating of working memory (shorter latency P300s) in both the auditory and visual domains and musicians allocated more neural resources to auditory stimuli (larger amplitude P300), showing increased sensitivity to the auditory standard/deviant difference and less effortful updating of auditory working memory. These findings demonstrate that long-term music training is related to improvements in working memory, in both the auditory and visual domains and in terms of both behavioral and ERP measures.     

Cortical network dynamics during source memory retrieval: current density imaging with individual MRI

We investigated the neural correlates of source memory retrieval using low-resolution electromagnetic tomography (LORETA) with 64 channels EEG and individual MRI as a realistic head model. Event-related potentials (ERPs) were recorded while 13 healthy subjects performed the source memory task for the voice of the speaker in spoken words. The source correct condition of old words elicited more positive-going potentials than the correct rejection condition of new words at 400-700 ms post-stimulus and the old/new effects also appeared in the right anterior region between 1,000 and 1,200 ms. We conducted source reconstruction at mean latencies of 311, 604, 793, and 1,100 ms and used statistical parametric mapping for the statistical analysis. The results of source analysis suggest that the activation of the right inferior parietal region may reflect retrieval of source information. The source elicited by the difference ERPs between the source correct and source incorrect conditions exhibited dynamic change of current density activation in the overall cortices with time during source memory retrieval. These results indicate that multiple neural systems may underlie the ability to recollect context.     

Neurophysiological correlates of memory illusion in both encoding and retrieval phases

False recognition of a critical lure at retrieval in the Deese-Roediger-McDermott (DRM) paradigm depends on different processing of its corresponding associates in the encoding phase. The current study recorded ERPs in both the encoding and retrieval phases to investigate the neural correlates of differential processing of true and false memories, and the roles of encoding and retrieval in eliciting memory illusion. The ERPs recorded at the study phase were characterized by a smaller N170 component and a larger amplitude late positive component (LPC) for associates that elicited later memory illusion than those that did not elicit later memory illusion. These ERP results suggest that increased active semantic associative processing or a gist representation was established for those items that elicited later memory illusion. This interpretation was supported by the serial-position analysis of the ERPs at encoding. Three ERP components were identified at retrieval. The equal early ERP old/new effects for true and false recognition reflected similar semantic priming. The parietal ERP old/new effect was greater for true than for false recognition, reflecting the recollection processes. A late slow negativity ERP distributed at the parietal and right frontal electrode sites differentiated between true and false recognition. The ERP results confirmed that both encoding and retrieval processes are involved in eliciting false memory. The parietal and frontal distributions of LPC at encoding and the late negativity at retrieval may imply a common neural mechanism in monitoring memory encoding and retrieval.     

Prospective memory and working memory: Asymmetrical effects during frontal lobe TMS stimulation

The role of working memory (WM) for the realization of an intended action (prospective memory, PM) has been debated in recent neuropsychological literature. The present study aimed to assess whether WM and PM share resources or are, alternatively, two distinct mechanisms. A verbal task was used, which manipulated the cognitive demand of both WM and PM dimensions on an event-based prospective task. Transcranial magnetic stimulation (TMS) was also employed to clarify the causal contribution of frontal areas previously related to WM, to the PM process. The prospective task required the participant to respond whenever a word appeared which had been presented before the beginning of the task. Two ongoing tasks were administered: an updating WM task (in two conditions of medium and high WM demands) and a lexical decision task (representing a low WM demand). In the first two experiments, higher PM demand affected WM only at higher loads, but the PM load effect was independent of WM, showing asymmetrical behavioural effects. In the third experiment, single pulse TMS was applied to left and right dorsolateral prefrontal cortices. When applied to the experimental sites, stimulation increased error rates of the PM task, while the effect was only marginal in the WM task. The effect was bilateral, since there was no difference between left and right stimulation sites. These findings demonstrated, from both behavioural and neurofunctional perspectives, that WM and PM processes are not based on the same memory system, but PM may require WM resources at high demand.     

Neural mechanisms of interference control in working memory capacity

The extent to which one can use cognitive resources to keep information in working memory is known to rely on (1) active maintenance of target representations and (2) downregulation of interference from irrelevant representations. Neurobiologically, the global capacity of working memory is thought to depend on the prefrontal and parietal cortices; however, the neural mechanisms involved in controlling interference specifically in working memory capacity tasks remain understudied. In this study, 22 healthy participants completed a modified complex working memory capacity task (Reading Span) with trials of varying levels of interference control demands while undergoing functional MRI. Neural activity associated with interference control demands was examined separately during encoding and recall phases of the task. Results suggested a widespread network of regions in the prefrontal, parietal, and occipital cortices, and the cingulate and cerebellum associated with encoding, and parietal and occipital regions associated with recall. Results align with prior findings emphasizing the importance of frontoparietal circuits for working memory performance, including the role of the inferior frontal gyrus, cingulate, occipital cortex, and cerebellum in regulation of interference demands.     

Interference of working memory load with long-term memory formation

Traditionally, it has been assumed that the medial temporal lobe (MTL) is indispensable for long-term memory (LTM) encoding, but only plays a minor role for working memory (WM) maintenance. Recently, however, an increasing number of studies questioned this seemingly clear distinction by showing that the MTL does participate in some WM processes, especially if multiple items are being maintained. This would predict that WM maintenance of multiple items interferes with simultaneous LTM encoding. Here, we tested this idea in a functional magnetic resonance imaging paradigm that required subjects to encode stimuli into LTM during simultaneous WM maintenance of either single or multiple items. Indeed, we found that maintenance of multiple items deteriorates simultaneous LTM encoding as compared with maintenance of single items. WM-related activation of the hippocampus was more pronounced in the condition with high WM load; in contrast, hippocampal activation related to LTM encoding was stronger in the low WM load condition. Successful LTM encoding was associated with a high level of activity in the adjacent parahippocampal cortex (PHC), leading to pronounced parahippocampal subsequent memory effects in the high load condition. This suggests that the PHC is a locus of WM–LTM interaction. Functional connectivity analysis with a seed in the PHC confirmed this result by revealing strong connectivity with the medial frontal cortex, which was only active in the high WM load condition. Taken together, these findings suggest that high WM demands interfere with LTM encoding and thus support the idea that WM and LTM processes interact in the MTL.