Examining the role of stimulus complexity in item and associative memory.

Episodic memory comprises memory for individual information units (item memory) and for the connections among them (associative memory). In two experiments using an object pair learning task, we examined the effect of visual stimulus complexity on memory encoding and retrieval mechanisms and on item and associative memory performance. Subjects encoded pairs of black monochrome object images (low complexity, LC condition) or color photographs of objects (high complexity, HC condition) via interactive imagery, and subsequently item and associative recognition were tested. In Experiment 1, event-related potentials (ERPs) revealed an enhanced frontal N2 during encoding and an enhanced late posterior negativity (LPN) during item recognition in the HC condition, suggesting that memory traces containing visually more complex objects elicited a stronger effort in reconstructing the past episode. Item memory was consistently superior in the HC compared to the LC condition. Associative memory was either statistically unaffected by complexity (Experiment 1) or improved (Experiment 2) in the HC condition, speaking against a tradeoff between resources allocated to item versus associative memory, and hence contradicting results of some prior studies. In Experiment 2, in both young and older adults, both item and associative memory benefitted from stimulus complexity, such that the magnitude of the age-related associative deficit was not influenced by stimulus complexity. Together, these results suggest that if familiar objects are presented in a form that exhibits a higher visual complexity, which may support semantic processing, complexity can benefit both item and associative memory. Stimulus properties that enhance item memory can scaffold associative memory in this situation.

Pre-associative item encoding influences associative memory: Behavioral and ERP evidence.

It is unknown whether the manner with which an item is encoded in isolation, immediately before it is encoded into an inter-inter association, influences associative memory. We therefore presented the items of to-be-encoded associative pairings sequentially and manipulated how each first item of a pair was encoded (before associative encoding could begin). Furthermore, we recorded ERPs during memory encoding to investigate the neurocognitive processes that might relate pre-associative item encoding to subsequent associative memory performance. Behaviorally, we found that pre-associative item elaboration (vs. no elaboration) led to a memory tradeoff-enhanced item memory relative to impaired associative memory. This tradeoff likely reflected that item elaboration reduced cognitive resources for ensuing associative encoding, indexed by a reduced P300 and frontal slow wave at the time of associative encoding. However, frontal slow wave subsequent memory effects measured during pre-associative item encoding revealed that, for a given item, greater semantic elaboration was related to better item and associative memory while greater visual elaboration was related to better item and worse associative memory. Thus, there are likely two opposing ways in which pre-associative item encoding can influence associative memory: (1) by depleting encoding resources to impair associative memory and (2) by scaffolding inter-item associations to enhance associative memory. When item encoding occurs immediately before associative encoding, it appears that the temporary depletion of encoding resources is more important in determining later memory performance. Future research should compare the independent effects of resource depletion and encoding strategy during pre-associative item encoding.

Reliability and stability of oddball P300 amplitude in older adults: The role of stimulus sequence effects.

The P300 may be an individual difference marker of neuro-cognitive function, which due to age-related cognitive decline may be particularly useful in older adults. Recently, we reported effects of the local stimulus sequence in an oddball task (i.e., the number of non-targets that preceded a target) on P300 amplitude in young and older adults. The same older adults completed a second session of the task 4-8 months after the first session. Here, we examined the effect of the stimulus sequence on the between- and within-session reliability and stability of P300 amplitude and RT, and their intertrial variability, in this sample of older adults. The sequence effects - an inverted U-shape effect of the number of standards preceding a target on parietal P300, and a linear effect on frontal P300 - were stable within and across sessions on the group level. Within individuals, P300 amplitude at frontal and parietal electrodes was generally very reliable and stable, mostly independently of sequence effects, encouraging its use as an individual difference marker of neuro-cognitive function in older adults. However, measures of the strength of the sequence effects themselves showed unacceptable reliability, speaking against their use as individual difference markers, at least in older adults.

On the role of item encoding mechanisms in associative memory in young and older adults: A mass univariate ERP study.

We examined the role of item encoding mechanisms in older adults' disproportionate deficit in memory for associations and individual differences therein. Young and older adults encoded sequentially presented object pairs via interactive imagery while their EEG was recorded. Compared to the young adults, older adults exhibited a reduction in associative, but not in item memory performance. Young adults showed frontal slow wave subsequent memory effects (SME) in both an item encoding contrast and an associative encoding contrast, presumably reflecting elaborative item processing, as well as the elaboration of an internal interactive image. Based on their performance in the subsequent associative memory test, older adults were subdivided into a high and a low performing group. In low performers, instead of a frontal slow wave SME a polarity-reversed, early parietal item SME was prominent, whose magnitude was negatively correlated with associative memory performance, potentially reflecting shallow, perceptual item encoding processes that are not well-suited for the formation of new associations. The present findings suggest that age-related deficits in elaboration of item information and an emphasis on the encoding of perceptual, item-specific details may contribute to reduced associative memory performance in older adults.

Survival processing modulates the neurocognitive mechanisms of episodic encoding.

Memories formed in the context of an imagined survival scenario are more easily remembered, but the mechanisms underlying this effect are still under debate. We investigated the neurocognitive processes underlying the survival processing effect by examining event-related potentials (ERPs) during memory encoding. Participants imagined being either stranded in a foreign land and needing to survive, or in an overseas moving (control) scenario, while incidentally encoding a list of words. Words encountered in the survival context were associated with improved recall and reduced false-memory intrusions during a later memory test. Survival processing was associated with an increased frontal slow wave, while there was no effect on the overall P300 amplitude, relative to the control scenario. Furthermore, a subsequent memory effect in the P300 time window was found only in the control scenario. These findings suggest that survival processing leads to a shift away from lower level encoding processes, which are sensitive to motivation and stimulus salience and which were evident in the control scenario, to more active and elaborative forms of encoding. The results are consistent with a richness of encoding account of the survival processing effect and offer novel insights into the encoding processes that lead to enhanced memory for fitness-relevant information.

The neurocognitive basis of metamemory: Using the N400 to study the contribution of fluency to judgments of learning.

Metamemory is crucial for monitoring, evaluating, and optimizing memory performance. The basis of metamemory, however, is a matter of considerable debate. In the present study, we examined the contribution of processing fluency-the ease of processing information during learning-to metamemory judgments. We recorded event-related potentials (ERPs) while participants studied related and unrelated word pairs across two study-test cycles in a judgment of learning (JOL) task. In the first study-test cycle, related pairs were associated with better cued recall, higher JOLs, and a reduced N400 amplitude than unrelated pairs. Crucially, between- and within subject correlational analyses indicated that reduced N400 amplitudes, indexing more fluent processing, were associated with higher JOLs. Furthermore, single-trial N400 mediated a small but significant portion of the relatedness effect on JOLs. In the second study-test cycle, relatedness still increased recall and JOLs. However, related and unrelated pairs did not differ in N400 amplitude. Rather, unrelated pairs elicited a parietal positivity in a later time window that partially mediated the relatedness effect on JOLs. Together, these results suggest that processing fluency, indexed by the N400, contributes to the relatedness effect on JOLs when novel word pairs are learned, but not when previously studied pairs are relearned. Our results also imply that aspects of fluency not captured by the N400 and/or explicit beliefs about memory contribute to JOLs. This study demonstrates the utility of ERPs in gaining new insights into the neurocognitive mechanisms of metamemory.

Neurocognitive mechanisms of guided item and associative encoding in young and older adults.

A hallmark of aging is a decline in episodic memory that is especially pronounced for memory for associations. To examine the neurocognitive mechanisms, young and older adults completed an item encoding task involving a semantic judgment on individual objects and an associative encoding task involving a judgment whether one of two objects could fit into the other, while their EEG was recorded. Item and associative recognition were equally reduced in older adults, unexpectedly yielding no disproportionate age-related associative deficit. A behavioral follow-up experiment did reveal an associative deficit when item and associative memory were both tested for the stimuli encoded in an easier version of the associative task, although this effect tended to be smaller than the deficit in an interactive imagery task. The behavioral and ERP results together suggest that in the item task, older adults failed to bind together perceptual object features, leading to low item memory performance. In the association task, both age groups engaged shallow, perceptual encoding processes, which appeared to be less efficient in older adults. These results suggest that the age-related associative deficit is modulated by the extent to which both item and associative memory depend on low-level feature binding and higher-level strategic processes.

Effects of acute psychosocial stress on the neural correlates of episodic encoding: Item versus associative memory.

Acute stress is known to modulate episodic memory, but little is known about the extent to, and the circumstances under, which stress affects encoding of item vs. inter-item associative information for words of different valences. Furthermore, the precise neuro-cognitive mechanisms underlying stress effects on episodic encoding in humans are largely unknown. To address these questions, in the present study we recorded EEG activity while male participants encoded neutral, negative and positive words, each paired with another word that was always neutral. Immediately before encoding, half of the participants experienced a psychosocial stressor, the Trier Social Stress Test, while the other half underwent a control procedure. Twenty-four hours later, participants completed separate item and associative recognition tests. Pre-learning stress enhanced item recognition accuracy for the positive, but not for the negative words. By contrast, there was no evidence for stress effects on associative recognition. The increase in item recognition was accompanied by a higher familiarity-, but not recollection-, based item retrieval of positive and neutral, but not negative words. Crucially, in the event-related potential (ERP) stress affected the amplitude of the frontal slow wave in general, and the frontal slow wave subsequent memory effect for positive words in specific, and the subsequent memory effect was correlated with cortisol levels after the stress manipulation. Our results suggest that positive words are encoded more elaboratively under stress, leading to a higher likelihood of subsequent item retrieval. An interaction of cortisol with frontal-lobe dependent control processes as well as a shift in attentional biases may contribute to this stress-induced modulation of episodic encoding.

On the role of retrieval processes in the survival processing effect: Evidence from ROC and ERP analyses.

Memory is enhanced for words encoded in the context of an imagined survival scenario, an effect modulated by word imageability or concreteness. However, the mechanisms underlying this "survival processing effect" are still controversial. To address this issue, we used receiver operating characteristic (ROC) curves and event-related potentials (ERPs) to examine the recognition retrieval processes associated with words previously encoded in either a survival or a control scenario. More specifically, we investigated how recollection- and familiarity-based retrieval are influenced by survival processing of high- and low-imageability words. Participants incidentally encoded words and then completed a surprise recognition test while their EEG was recorded. The encoding of concrete, high-imageability words in a survival context lead to improved recognition memory compared to the control context, and this improvement was associated with an increase in both the ROC and ERP measures of recollection-based memory retrieval. Survival processing was also associated with an increase in the ERP familiarity signal for these words, but the ROC analysis indicated that recognition judgments relied upon recollection rather than familiarity. These findings provide evidence that survival processing increases elaboration during encoding, leading to greater recollection at retrieval and, in turn, enhanced memory.

Subjective cognitive decline in healthy older adults is associated with altered processing of negative versus positive feedback in a probabilistic learning task.

Older adults who worry about their own cognitive capabilities declining, but who do not show evidence of actual cognitive decline in neuropsychological tests, are at an increased risk of being diagnosed with dementia at a later time. Since neural markers may be more sensitive to early stages of cognitive decline, in the present study we examined whether event-related potential responses of feedback processing, elicited in a probabilistic learning task, differ between healthy older adults recruited from the community, who either did (subjective cognitive decline/SCD-group) or did not report (No-SCD group) worry about their own cognition declining beyond the normal age-related development. In the absence of group differences in learning from emotionally charged feedback in the probabilistic learning task, the amplitude of the feedback-related negativity (FRN) varied with feedback valence differently in the two groups: In the No-SCD group, the FRN was larger for positive than negative feedback, while in the SCD group, FRN amplitude did not differ between positive and negative feedback. The P3b was enhanced for negative feedback in both groups, and group differences in P3b amplitude were not significant. Altered sensitivity in neural processing of negative versus positive feedback may be a marker of SCD.

The survival processing effect in episodic memory in older adults and stroke patients.

In the present study, we tested whether processing information in the context of an ancestral survival scenario enhances episodic memory performance in older adults and in stroke patients. In an online study (Experiment 1), healthy young and older adults rated words according to their relevance to an ancestral survival scenario, and subsequent free recall performance was compared to a pleasantness judgment task and a moving scenario task in a within-subject design. The typical survival processing effect was replicated: Recall rates were highest in the survival task, followed by the moving and the pleasantness judgment task. Although older adults showed overall lower recall rates, there was no evidence for differences between the age groups in the condition effects. Experiment 2 was conducted in a neurological rehabilitation clinic with a sample of patients who had suffered from a stroke within the past 5 months. On the group level, Experiment 2 revealed no significant difference in recall rates between the three conditions. However, when accounting for overall memory abilities and executive function, independently measured in standardized neuropsychological tests, patients showed a significant survival processing effect. Furthermore, only patients with high executive function scores benefitted from the scenario tasks, suggesting that intact executive function may be necessary for a mnemonic benefit. Taken together, our results support the idea that the survival processing task - a well-studied task in the field of experimental psychology - may be incorporated into a strategy to compensate for memory dysfunction.

Observing memory encoding while it unfolds: Functional interpretation and current debates regarding ERP subsequent memory effects.

Our ability to remember the past depends on neural processes set in train in the moment an event is experienced. These processes can be studied by segregating brain activity according to whether an event is later remembered or forgotten. The present review integrates a large number of studies examining this differential brain activity, labeled subsequent memory effect (SME), with the ERP technique, into a functional organization and discusses routes for further research. Based on the reviewed literature, we suggest that memory encoding is implemented by multiple processes, typically reflected in three functionally different subcomponents of the ERP SME elicited by study stimuli, which presumably interact with preparatory SME activity preceding the to be encoded event. We argue that ERPs are a valuable method in the SME paradigm because they have a sufficiently high temporal resolution to disclose the subcomponents of encoding-related brain activity. Implications of the proposed functional organization for future studies using the SME procedure in basic and applied settings will be discussed.

Reduced concentration performance and heartbeat-evoked potential in individuals with a history of a SARS-CoV-2 infection.

The goal of characterizing long-term psychological and neural consequences of a SARS-CoV-2 infection has recently gained importance. Here, we examined the effect of a prior SARS-CoV-2 infection on neural markers of exteroceptive (P300) and interoceptive (heartbeat-evoked potential; HEP) signal processing, as well as on neuropsychological tests of attention, inhibition and episodic memory, in 23 adults with a self-reported history of SARS-CoV-2 infection versus 23 healthy controls. We found that the group with a prior infection showed decreased HEP (but not P300) amplitudes, as well as reduced attention/concentration performance. These results suggest that SARS-CoV-2 may damage neural structures of cardiac interoception, thereby potentially contributing to cognitive and psychological long-term deficits. Modulations of interoceptive processing after a SARS-CoV-2 infection are thus a promising target for future research.

An examination of task factors that influence the associative memory deficit in aging.

Aging is accompanied by a decline in associative memory, whereas item memory remains relatively stable compared to young adults. This age-related associative deficit is well replicated, but its mechanisms and influencing factors during learning are still largely unclear. In the present study, we examined mediators of the age-related associative deficit, including encoding intentionality, strategy instructions, the timing of the memory test (immediate vs. 24 h delayed) and the material being learned (words vs. pictures) in a within-subject design. Older and younger adults performed seven encoding tasks on word pairs and picture pairs on two consecutive days, followed by item and associative recognition tests. The associative deficit was evident after all encoding tasks. We found no evidence for a difference in the magnitude of the associative deficit between incidental vs. intentional learning conditions. However, there was some evidence for a larger associative memory deficit with pictures versus words when the encoding task was held equal. Sentence generation and interactive imagery instructions in which participants generated their own mediators reduced the magnitude of the associative deficit. However, increased encoding guidance through the provision of mediators did not lead to an alleviation of the deficit, potentially because the specified mediators were implausible or difficult for the older adults to reconcile with prior knowledge. Finally, we found some evidence for a reduced age-related associative deficit with a test delay of 24 h. These results contribute to a better understanding of the factors affecting the relative difficulty of older adults with encoding and retrieving novel associations.

Realistic context doesn't amplify the survival processing effect: Lessons learned from Covid-19 scenarios.

Imagining being stranded in the grasslands of an unknown territory without basic survival materials and subsequently rating the relevance of words for this situation leads to exceptionally good memory for these words. This survival processing effect has received much attention, primarily because it has been argued to disclose the evolutionary foundations of human memory. So far, only fictitious scenarios were used to demonstrate this effect. To provide a fairer test of emotional response against richness-of-encoding explanations of the effect, we aimed at increasing everyday relevance and realism of the survival scenarios. For this purpose, we created two new Covid-19 scenarios, one focusing on emotional response (Covid-19-emotion) and the other on survival strategy (Covid-19-strategy). Both new scenarios were compared to the classical grassland and moving scenarios typically used to investigate the survival processing effect. In Experiment 1, we observed better memory for the grassland and Covid-19-strategy scenarios compared to the other two, but no significant difference between the former. A descriptively similar result pattern emerged in Experiment 2 for the number of ideas generated on how to use objects in the four scenarios. Theoretical implications are discussed.

Stress effects on the oddball P300 and N2 in males and females.

We examined the effect of psychosocial stress on electrophysiological markers of novelty and deviance processing, the N2 and P300, as well as sex differences therein. Participants underwent the Trier Social Stress Test (TSST) or a control procedure, followed by an oddball paradigm. A physiological stress response was induced in both sexes in the TSST condition. Furthermore, a reduced target P300 amplitude was elicited in the TSST condition in fronto-central electrodes, an effect that did not differ in magnitude between both sexes. By contrast, stressor effects on N2 amplitude differed by sex: In females, N2 amplitude was decreased in the TSST condition, while in males, no stress effects were observed. Exploratory correlational analyses suggested that a stress-induced P300 amplitude reduction, at least in males, could be due to a modulation of adrenergic activity. These results are consistent with sex differences in the manner in which stress affects lower-level, stimulus-driven vs. higher-level, more controlled processing stages.

Older adults show a higher heartbeat-evoked potential than young adults and a negative association with everyday metacognition.

The ability to monitor internal bodily and cognitive processes is essential for everyday functioning and independence in older adults, because it allows for adjustments when lapses in performance are imminent. In the present study, age-related morphological changes to the heartbeat evoked potential (HEP), an electrophysiological cortical representation of cardiac signals, and its association with self-reported everyday cognition were examined. A community sample of older adults showed an increased HEP amplitude, which could reflect a stronger representation of early stages of cardiac interoception, and a more anterior scalp distribution of the HEP, suggesting a more widespread configuration of the underlying neural generators, compared to a group of young adults. Furthermore, in older adults, HEP amplitude was negatively correlated with self-estimated everyday cognitive functioning. Older adults with pronounced cortical representations of peripheral signals may thus be more likely to take note of lapses in their own bodily and cognitive function, leading to lower estimates of their cognitive abilities. These results provide novel insights into age-related changes in interoceptive processing and their association with metacognitive judgments, with potentially far-reaching implications for cognitive aging and age-related cognitive decline.

How can I use it? The role of functional fixedness in the survival-processing paradigm.

After imagining being stranded in the grasslands of a foreign land without any basic survival material and rating objects with respect to their relevance in this situation, participants show superior memory performance for these objects compared to a control scenario. A possible mechanism responsible for this memory advantage is the richness and distinctiveness with which information is encoded in the survival-scenario condition. When confronted with the unusual task of thinking about how an object can be used in a life-threatening context, participants will most likely consider both common and uncommon (i.e., novel) functions of this object. These ideas about potential functions may later serve as powerful retrieval cues that boost memory performance. We argue that objects differ in their potential to be used as novel, creative survival tools. Some objects may be low in functional fixedness, meaning that it is possible to use them in many different ways. Other objects, in contrast, may be high in functional fixedness, meaning that the possibilities to use them in non-standard ways is limited. We tested experimentally whether functional fixedness of objects moderates the strength of the survival-processing advantage compared to a moving control scenario. As predicted, we observed an interaction of the functional fixedness level with scenario type: The survival-processing memory advantage was more pronounced for objects low in functional fixedness compared to those high in functional fixedness. These results are in line with the richness-of-encoding explanation of the survival-processing advantage.

Preceding stimulus sequence effects on the oddball-P300 in young and healthy older adults.

The present study examined the mechanisms underlying stimulus sequence effects on the parietal P300 and frontal P3a elicited by infrequent targets in an oddball paradigm and compared these effects between young and older adults. Fifty young and 50 healthy older adults completed a simple visual oddball task including an infrequent (20%) target stimulus. A temporo-spatial principal component (PCA) analysis was used to disentangle the parietal P300 and frontal P3a from overlapping ERP components. The typical age-related anterior-shift of the P300 was, according to the PCA, due to a disproportionately large contribution of a frontal P3a in older adults. Up to about five successive standards preceding a target, the results replicated the typical increase in parietal P300 amplitude to targets with increases in preceding standards. A novel finding was that with further increases in preceding standards, P300 amplitude to targets gradually decreased. This pattern is consistent with a combination of relatively automatic, temporary expectations and higher level, conscious expectations driving P300 sequential effects, with different dynamics over the course of successively presented standards. However, an expectancy-based account of these sequential effects was challenged by an analogous analysis of RTs. Sequential effects on the frontal P3a differed from the parietal P300: The P3a was largest when a target followed another target and continually decreased with the number of intervening standards. Notably, sequential effects were strikingly similar for young and older adults, and implications for the functional significance of morphological changes in P300 due to aging are discussed.

Adaptive Memory: Independent Effects of Survival Processing and Reward Motivation on Memory.

Humans preferentially remember information processed for their survival relevance, a memorial benefit known as the survival processing effect. Memory is also biased towards information associated with the prospect of reward. Given the adaptiveness of these effects, they may depend on similar mechanisms. We tested whether motivation drives both effects, with reward incentives that are known to boost extrinsic motivation and survival processing perhaps stimulating intrinsic motivation. Accordingly, we manipulated survival processing and reward incentive independently during an incidental-encoding task in which participants chose between pairs of words concerning their relevance for a scenario, and examined the effects on encoding event-related potentials (ERP) activity and later performance on a surprise recall test. We hypothesized that if survival processing fosters intrinsic motivation, it should reduce the beneficial effects of extrinsic motivation (reward incentive). In contrast to this prediction, we found that reward incentive and survival processing independently improved memory and that the P300, a measure of lower-level cognitive resource allocation, was increased by reward incentive independent of survival processing. Further, survival processing and reward incentive independently increased the frontal slow wave (FSW), a measure of higher-level elaboration. These findings suggest that while survival processing and reward incentive may both increase encoding elaboration, the memory-enhancing effect of survival processing does not depend on increased intrinsic motivation. Additionally, we replicated a recent finding whereby the survival processing effect generalizes to a choice-based encoding task and further showed that the beneficial effect of choice on memory likely does not interact with either survival processing or reward.