Episodic Memory Traces Research Articles

Distinct mechanisms and functions of episodic memory.

The concept of episodic memory (EM) faces significant challenges by two claims: EM might not be a distinct memory system, and EM might be an epiphenomenon of a more general capacity for mental time travel (MTT). Nevertheless, the observations leading to these arguments do not preclude the existence of a mechanically and functionally distinct EM system. First, modular systems, like cognition, can have distinct subsystems that may not be distinguishable in the system's final output. EM could be such a subsystem, even though its effects may be difficult to distinguish from those of other subsystems. Second, EM could have a distinct and consistent low-level function, which is used in diverse high-level functions such as MTT. This article introduces the scenario construction framework, proposing that EM crucially rests on memory traces containing the gist of an episodic experience. During retrieval, EM traces trigger the reconstruction of semantic representations, which were active during the remembered episode, and are further enriched with semantic information, to generate a scenario of the past experience. This conceptualization of EM is consistent with studies on the neural basis of EM and resolves the two challenges while retaining the key properties associated with EM. This article is part of the theme issue 'Elements of episodic memory: lessons from 40 years of research'.

To update or to create? The influence of novelty and prior knowledge on memory networks.

Schemas are foundational mental structures shaped by experience. They influence behaviour, guide the encoding of new memories and are shaped by associated information. The adaptability of memory schemas facilitates the integration of new information that aligns with existing knowledge structures. First, we discuss how novel information consistent with an existing schema can be swiftly assimilated when presented. This cognitive updating is facilitated by the interaction between the hippocampus and the prefrontal cortex. Second, when novel information is inconsistent with the schema, it likely engages the hippocampus to encode the information as part of an episodic memory trace. Third, novelty may enhance hippocampal dopamine through either the locus coeruleus or ventral tegmental area pathways, with the pathway involved potentially depending on the type of novelty encountered. We propose a gradient theory of schema and novelty to elucidate the neural processes by which schema updating or novel memory traces are formed. It is likely that experiences vary along a familiarity-novelty continuum, and the degree to which new experiences are increasingly novel will guide whether memory for a new experience either integrates into an existing schema or prompts the creation of a new cognitive framework. This article is part of the theme issue 'Long-term potentiation: 50 years on'.

Bound to a spider without its web: Task-type modulates the retrieval of affective information in subsequent responses

Action control theories assume that upon responding to a stimulus response and stimulus features are integrated into a short episodic memory trace; repeating any component spurs on retrieval, affecting subsequent performance. The resulting so-called “binding effects” are reliably observed in discrimination tasks. In contrast, in localization performance, these effects are absent and only inhibition of return (IOR) emerges – a location change benefit. Affective information has been found to modulate binding effects; yet a modulation of IOR has led to mixed results, with many finding no influence at all. In the current study, participants discriminated letters (Experiment 1) or localized dots (Experiment 2) on a touchpad in prime-probe sequences. During the prime display two images – one with fruits and one with a spider – appeared, one of which spatially congruent with the to-be-touched area. In the discrimination task, previously touching a spider compared to a fruit slowed down response repetitions. In contrast, the localization task only showed IOR. This suggests that task-irrelevant valence is integrated with the response and affects subsequent responses due to retrieval. However, this is not ubiquitous but depends on task type. The results shed further light on the impact of affective information on actions.

Instructional load induces functional connectivity changes linked to task automaticity and mnemonic preference

Learning new rules rapidly and effectively via instructions is ubiquitous in our daily lives, yet the underlying cognitive and neural mechanisms are complex. Using functional magnetic resonance imaging we examined the effects of different instructional load conditions (4 vs. 10 stimulus-response rules) on functional couplings during rule implementation (always 4 rules). Focusing on connections of lateral prefrontal cortex (LPFC) regions, the results emphasized an opposing trend of load-related changes in LPFC-seeded couplings. On the one hand, during the low-load condition LPFC regions were more strongly coupled with cortical areas mostly assigned to networks such as the fronto-parietal network and the dorsal attention network. On the other hand, during the high-load condition, the same LPFC areas were more strongly coupled with default mode network areas. These results suggest differences in automated processing evoked by features of the instruction and an enduring response conflict mediated by lingering episodic long-term memory traces when instructional load exceeds working memory capacity limits. The ventrolateral prefrontal cortex (VLPFC) exhibited hemispherical differences regarding whole-brain coupling and practice-related dynamics. Left VLPFC connections showed a persistent load-related effect independent of practice and were associated with ‘objective’ learning success in overt behavioral performance, consistent with a role in mediating the enduring influence of the initially instructed task rules. Right VLPFC's connections, in turn, were more susceptible to practice-related effects, suggesting a more flexible role possibly related to ongoing rule updating processes throughout rule implementation.

0043 Modulation of ultra-slow calcium oscillation in the dentate gyrus during Non-REM sleep

Abstract Introduction The function of sleep in memory consolidation has been well established. Hippocampal CA1 and CA3 subregions are thought to be particularly important in this process. The current working hypothesis postulates that episodic memory traces captured during waking hours are replayed in the hippocampal CA1-CA3 areas and transferred to the cortex for long-term storage during sleep. Even though the sensory and spatial information from higher-order cortical areas such as the entorhinal cortex primarily enters the hippocampus via the dentate gyrus (DG), this structure has always been considered as the “silent partner” in memory consolidation. Whether and how the captured memory traces are transferred from the DG toward the downstream hippocampal areas is less known. Methods Here, we used fiber photometry, two-photon calcium imaging, and EEG recording to examine the activity of DG during sleep. Results Strikingly, we found that DG cells are even more active during sleep than wakefulness and the calcium activity in the DG slowly oscillates during non-REM (NREM) sleep epochs. Furthermore, we also found that the cycles of this activity coinciding with microarousals are tightly locked to brief serotonin (5-HT) release during NREM sleep. Pharmacological blockade of 5-HT1a receptors abolished the calcium oscillations in the DG. Furthermore, genetic knockdown of 5-HT1a receptors in the DG leads to memory impairment in spatial and contextual memory tasks. Conclusion Together, our results indicate that ultra-slow calcium oscillations in the DG during NREM sleep are driven by serotonin fluctuations and they are required for memory consolidation. Support (if any)

Attentional Biases Toward Spiders Do Not Modulate Retrieval.

When responding to stimuli, response and stimulus' features are thought to be integrated into a short episodic memory trace, an event file. Repeating any of its components causes retrieval of the whole event file leading to benefits for full repetitions and changes but interference for partial repetitions. These binding effects are especially pronounced if attention is allocated to certain features. We used attentional biases caused by spider stimuli, aiming to modulate the impact of attention on retrieval. Participants discriminated the orientation of bars repeating or changing their location in prime-probe sequences. Crucially, shortly before probe target onset, an image of a spider and that of a cub appeared at one position each - one of which was spatially congruent with the following probe target. Participants were faster when responding to targets spatially congruent with a preceding spider, suggesting an attentional bias toward aversive information. Yet, neither overall binding effects differed between content of preceding spatially congruent images nor did this effect emerge when taking individual fear of spiders into account. We conclude that attentional biases toward spiders modulate overall behavior, but that this has no impact on retrieval.

Investigating the Role of Response Codes in Masked Priming Lexical Decision Tasks: The Case of Repeated Presentations

The masked priming technique is considered a gold standard among experimental psychologists who specialize in the field of visual word recognition. Typically, this method entails a comparison between two or more critical conditions (e.g., the target word MOUSE being preceded by either the identity prime mouse or the unrelated prime fence). It is noteworthy that, unlike other masked priming tasks, prior experiments examining the properties of unrelated primes (e.g., their frequency as words [high or low] or their legality as nonwords [orthographically legal or illegal]) do not have an impact on the processing of the target item. However, two lexical decision studies reported faster responses to target words when the unrelated prime is a word rather than a nonword (i.e., a response congruency effect). One possible explanation for this discrepancy is a difference in methodology, as these two studies are the only ones to have used repeated presentation of stimuli, which could lead to the creation of an episodic memory trace that amplifies response congruency effects. To examine this hypothesis, we used a set of materials that did not show any congruency effect in a previous experiment with unique presentations, except that here we included repeated presentations. Results showed a response congruency effect, with participants responding faster to word targets when they were preceded by an unrelated word prime as opposed to an unrelated nonword prime. These findings suggest that the activation of response codes in masked priming is contingent upon the nature of cognitive resources required for processing the target stimuli.

How does Working Memory Promote Traces in Episodic Memory?

A longstanding research question in cognitive psychology concerns how the underlying mechanisms of working memory impact long-term episodic memory. In this series of six experiments, we manipulated three different factors within a complex span task that interleaves memoranda and distractors to investigate the contribution of these factors to the creation of episodic traces: (1) the cognitive load of processing the distractors, (2) the number of distractors, and (3) the free time following the distractors. All three factors have been identified in the prior literature as important to maintenance in working memory and, consequently, later retrieval from episodic memory. Thus, it is important to understand their unique and joint effects to the long-term durability of memory traces. Across six experiments, delayed recall (i.e., episodic memory) of the items studied during the complex span tasks (i.e., working memory) was best accounted for by accumulated free time, whereas the effects of cognitive load and number of distractors were inconsistent or negligible. These results conflict with prior work suggesting that cognitive load and the number of distractors impact episodic memory. However, the current results replicate and extend those suggesting that time spent processing items in working memory promotes the creation of episodic memory traces.

Where was the toaster? A systematic investigation of semantic construction in a new virtual episodic memory paradigm.

Retrieved memories of past events are often inaccurate. The scenario construction model (SCM) postulates that during encoding, only the gist of an episode is stored in the episodic memory trace and during retrieval, information missing from that trace is constructed from semantic information. The current study aimed to find behavioural evidence for semantic construction in a realistic, yet controlled setting by introducing a completely new paradigm and adjusted memory tests that measure semantic construction. Using a desktop virtual reality (VR), participants navigated through a flat in which some household objects appeared in unexpected rooms, creating conflicts between the experienced episode and semantic expectations. The manipulation of congruence enabled us to identify influences from semantic information in cases of episodic memory failure during recall. Besides, we controlled for objects to be task-relevant or task-irrelevant to the sequence of action. In addition to an established old/new recognition task we introduced spatial and temporal recall measures as possible superior memory measures quantifying semantic construction. The recognition task and the spatial recall revealed that both congruence and task-relevance predicted correct episodic memory retrieval. In cases of episodic memory failure, semantic construction was more likely than guessing and occurred more frequently for task-irrelevant objects. In the temporal recall object-pairs belonging to the same semantic room-category were temporally clustered together compared with object-pairs from different semantic categories (at the second retrieval delay). Taken together, our findings support the predictions of the SCM. The new VR paradigm, including the new memory measures appears to be a promising tool for investigating semantic construction.

Long-term learning and forgetting of feature binding in verbal free recall.

Temporary feature bindings can be learned under specific experimental conditions. However, how this learning occurs and how it is forgotten over long intervals is unclear. We addressed this question with repeated presentation of an array of coloured shapes followed by verbal free recall after delays of 1 day, 1 week, and 1 month. A total of 120 participants viewed 24 repetitions of the same study array of six objects each with two features (shape and colour). After 24 trials, 61 participants reported becoming aware of the repetition while 59 reported being unaware. Memory performance improved across trials, with aware participants showing faster learning than unaware participants whose performance appeared to reflect the capacity of short-term visual memory across all repetitions. Both aware and unaware participants recalled some of the array after their allocated delay, showing that learning had occurred during repetition trials, even for unaware participants who showed little or no improvement across 24 repetition trials. Memory for binding showed no change after 1 day compared with performance on the 24th repetition trial, was significantly lower for participants tested after 1 week, and was lower still for those tested after 1 month. Findings are interpreted as consistent with both a short-term, limited capacity visual cache that supports performance during early repetition trials, before learning can have occurred, and gradual strengthening across trials of an episodic long-term memory trace that supports learning. If the episodic trace exceeds the threshold of awareness, this accelerates learning.

Oscillatory Correlates of Intentional Forgetting: The Role of Theta and Alpha Power in Item-Method Directed Forgetting.

Results from item-method directed forgetting suggest that individuals are able to intentionally forget processed information. Most research suggests that either selective rehearsal of to-be-remembered or inhibitory control of to-be-forgotten information is accountable for the effects of intentional forgetting. Some research, however, hypothesized that the time to process information mediates the underlying mechanism. To test this hypothesis, the current study investigated associations between oscillatory power in theta (3–7.5 Hz) and alpha frequencies (8–13 Hz) and intentional forgetting in human participants and explored whether or not these mechanisms depended on processing time. Previously, theta power was shown to be associated with the creation of episodic memory traces and alpha power with inhibition. We therefore expected to find associations between these neural signatures and behavioral effects. Consistent with our hypotheses, we revealed increased theta power for to-be-remembered and increased alpha power for to-be-forgotten information and that the effects of activity in both frequency bands were influenced by the time individuals were given for processing the memory cue. These results suggest that not one but two mechanisms, rehearsal and inhibitory control, are accountable for item-method directed forgetting, both with different temporal profiles.

Varying demands for cognitive control reveals shared neural processes supporting semantic and episodic memory retrieval

The categorisation of long-term memory into semantic and episodic systems has been an influential catalyst for research on human memory organisation. However, the impact of variable cognitive control demands on this classical distinction remains to be elucidated. Across two independent experiments, here we directly compare neural processes for the controlled versus automatic retrieval of semantic and episodic memory. In a multi-session functional magnetic resonance imaging experiment, we first identify a common cluster of cortical activity centred on the left inferior frontal gyrus and anterior insular cortex for the retrieval of both weakly-associated semantic and weakly-encoded episodic memory traces. In an independent large-scale individual difference study, we further reveal a common neural circuitry in which reduced functional interaction between the identified cluster and ventromedial prefrontal cortex, a default mode network hub, is linked to better performance across both memory types. Our results provide evidence for shared neural processes supporting the controlled retrieval of information from functionally distinct long-term memory systems.

Offset-related brain activity in the left ventrolateral prefrontal cortex promotes long-term memory formation of verbal events

BackgroundRecent evidence suggests that brain activity following the offset of a stimulus during encoding contributes to long-term memory formation, however the exact mechanisms underlying offset-related encoding are still unclear. ObjectivesHere, in three repetitive transcranial magnetic stimulation studies (rTMS) we investigated offset-related activity in the left ventrolateral prefrontal cortex (VLPFC). rTMS was administered at different points in time around stimulus offset while participants encoded visually-presented words or pairs of words. The analyses focused on the effects of the stimulation on subsequent memory performance. ResultsrTMS administered at the offset of the stimuli, but not during online encoding, disrupted subsequent memory performance. In Experiment 1 we found that rTMS specifically disrupted encoding mechanisms initiated by the offset of the stimuli rather than general, post-stimulus processes. Experiment 2 showed that this effect was not dependent upon rTMS-induced somatosensory effects. In a third rTMS experiment we further demonstrated a robust decline in associative memory performance when the stimulation was delivered at the offset of the word pairs, suggesting that offset-related encoding may contribute to the binding of information into an episodic memory trace. ConclusionsThe offset of the stimulus may represent an event boundary that promotes the reinstatement of the previously experienced event and episodic binding.

Is Activity Silent Working Memory Simply Episodic Memory?

Working memory (WM) maintains task-relevant information in a state ready for processing. While traditional theories assume that sustained neuronal activity is responsible for WM, the Activity Silent WM (ASWM) account proposes that maintenance can also be supported by short-term synaptic weight changes. Here, we argue that the evidence for ASWM can be explained more parsimoniously by the involvement of episodic memory (EM) in WM tasks. Like ASWM, EM relies on rapid synaptic modification that is also activity silent; however, while ASWM posits transient synaptic modifications, EM traces persist over longer time periods. We discuss how, despite this difference, well-established EM mechanisms can account for the key findings attributed to ASWM, and describe predictions of this account.

Retraction Note to: The effect of gamma-enhancing binaural beats on the control of feature bindings.

Binaural beats represent the auditory experience of an oscillating sound that occurs when two sounds with neighboring frequencies are presented to one’s left and right ear separately. Binaural beats have been shown to impact information processing via their putative role in increasing neural synchronization. Recent studies of feature-repetition effects demonstrated interactions between perceptual features and action-related features: repeating only some, but not all features of a perception–action episode hinders performance. These partial-repetition (or binding) costs point to the existence of temporary episodic bindings (event files) that are automatically retrieved by repeating at least one of their features. Given that neural synchronization in the gamma band has been associated with visual feature bindings, we investigated whether the impact of binaural beats extends to the top-down control of feature bindings. Healthy adults listened to gamma-frequency (40 Hz) binaural beats or to a constant tone of 340 Hz (control condition) for ten minutes before and during a feature-repetition task. While the size of visuomotor binding costs (indicating the binding of visual and action features) was unaffected by the binaural beats, the size of visual feature binding costs (which refer to the binding between the two visual features) was considerably smaller during gamma-frequency binaural beats exposure than during the control condition. Our results suggest that binaural beats enhance selectivity in updating episodic memory traces and further strengthen the hypothesis that neural activity in the gamma band is critically associated with the control of feature binding.

Frontal ERP slow waves during memory encoding are associated with affective attitude formation

A neutral stimulus can acquire valence by being paired with a valenced stimulus, leading to a new attitude towards the previously neutral stimulus. There is, however, considerable debate about the mechanisms that underlie this process of affective attitude formation. Therefore, in the present study we employed a single-trial, intentional learning procedure that paired neutral with valenced words while recording ERP activity, and measured subsequent memory and subsequent attitudes for the pre-experimentally neutral words immediately following learning. Using traditional as well as single-trial ERP analyses, we found that frontal slow wave (FSW) activity, elicited while stimuli were being paired, was associated with both subsequent memory for the word pairs and subsequent attitudes towards the pre-experimentally neutral words. Specifically, FSW activity during the pairing of neutral with positive words was related to more positive subsequent attitudes, while during the pairing of neutral with negative words, it was associated with more negative subsequent attitudes, towards the pre-experimentally neutral words. Given that this FSW activity was also related to successful subsequent episodic memory retrieval for the word pairs, these findings provide evidence that the transfer of valence may depend on a process that supports associative episodic encoding during word paring. Further, a single-trial, mixed-effects model indicated that the relationship between encoding FSW activity and subsequent attitudes depended on the strength of the episodic memory trace. Thus, the present study provides novel evidence that a common mechanism contributes to both episodic memory encoding and affective attitude formation.

Episodic memory in nonhuman animals?

Experimental psychologist Jonathan Crystal and evolutionary psychologist Thomas Suddendorf debate with nonhuman animals experience human-like episodic memory.

Timing is crucial for the integration of angry facial expressions with motor responses: Investigation of subliminal and supraliminal emotion–action bindings.

Our brain codes perceptual features and actions in a distributed fashion, causing a binding problem: How does the brain recognize that information pertains to a specific object and not to other concurrently processed objects? Hommel (1998) suggested the event file concept: An episodic memory trace binding perceptual features and actions related to an event. By adapting Hommel's paradigm to emotional faces in a previous series of studies (Coll & Grandjean, 2016), we revealed that emotion could take part in an event file with motor responses when emotion is task relevant and in specific situations when emotion is task irrelevant. In the latter case, we supposed that such integration occurs because of the importance of emotion-action coupling for our survival, even when the task is not specifically related to emotion. To date, emotion-action binding has been studied only with faces presented for 500 ms. In continuation with the hypothesis that humans developed adaptive mechanisms to allow fast responses to emotions, we designed 2 experiments to investigate the influence of the duration of angry and neutral face presentation on binding with motor responses. Results showed that emotion-action integration was possible in a 100-, 250-, and 500-ms presentation, but not when the faces were subliminally (14 ms) or supraliminally (28 ms) displayed. Timing is crucial in emotion-action binding, and although reaction to emotional stimuli might take place rapidly, its integration, as shown by the present studies, seems to require at least 100 ms. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Feature binding in short-term memory and long-term learning.

In everyday experience, we encounter visual feature combinations. Some combinations are learned to support object recognition, and some are arbitrary and rapidly changing, so are retained briefly to complete ongoing tasks before being updated or forgotten. However, the boundary conditions between temporary retention of fleeting feature combinations and learning of feature bindings are unclear. Logie, Brockmole, and Vandenbroucke demonstrated that 60 repetitions of the same feature bindings for change detection resulted in no learning, but clear learning occurred with cued recall of the feature names. We extended those studies in two new experiments with the same array of colour-shape-location combinations repeated for 120 trials. In Experiment 1, change detection was well above chance from Trial 1, but improved only after 40 to 60 trials for participants who subsequently reported becoming aware of the repetition, and after 100 to 120 trials for participants reporting no awareness. Performance improved rapidly in Experiment 2 when participants reconstructed the array by selecting individual features from sets of colours, shapes, and locations. All participants subsequently reported becoming aware of the repetition. We conclude that change detection involves a visual cache memory that functions from the first trial, and retains feature bindings only for the duration of a trial. In addition, a weak residual episodic memory trace accumulates slowly across repetitions, eventually resulting in learning. Reconstructing feature combinations generates a much stronger episodic memory trace from trial to trial, and so learning is faster with performance supported both by the limited capacity visual cache and learning of the array.

Brain Signatures of New (Pseudo-) Words: Visual Repetition in Associative and Non-associative Contexts.

The contribution of two different training contexts to online, gradual lexical acquisition was investigated by event-related potentials (ERPs) elicited by new, word-like stimuli. Pseudowords were repeatedly preceded by a picture representing a well-known object (semantic-associative training context) or by a hash mark (non-associative training context). The two training styles revealed differential effects of repetition in both behavioral and ERPs data. Repetition of pseudowords not associated with any stimulus gradually enhanced the late positive component (LPC) as well as speeded lexical categorization of these stimuli, suggesting the formation of episodic memory traces. However, repetition under the semantic-associative context caused higher reduction in N400 component and categorization latencies. This result suggests the facilitation in the lexico-semantic processing of pseudowords as a consequence of their progressive associations to picture-concepts, going beyond the visual memory trace that is generated under the non-associative context.