Memory Trace Research Articles

Divergent recruitment of developmentally defined neuronal ensembles supports memory dynamics.

Memories are dynamic constructs whose properties change with time and experience. The biological mechanisms underpinning these dynamics remain elusive, particularly concerning how shifts in the composition of memory-encoding neuronal ensembles influence the evolution of a memory over time. By targeting developmentally distinct subpopulations of principal neurons, we discovered that memory encoding resulted in the concurrent establishment of multiple memory traces in the mouse hippocampus. Two of these traces were instantiated in subpopulations of early- and late-born neurons and followed distinct reactivation trajectories after encoding. The divergent recruitment of these subpopulations underpinned gradual reorganization of memory ensembles and modulated memory persistence and plasticity across multiple learning episodes. Thus, our findings reveal profound and intricate relationships between ensemble dynamics and the progression of memories over time.

Inter fragmenta nare: Leon Battista Alberti and the Wreck of Memory

As it is well known, rhetoric serves as a theoretical framework for the foundation of artistic practices in the works of Leon Battista Alberti. The structural significance of rhetoric also concerns the conceptualization of the relationship between time, space, and memory. In Alberti's perspective, ruins and fragments from the past are material incarnations of rhetorical-mnemonic imagines agentes: their power to affect the mind depends on the ability of the observer to put them in the right places (loci). Against this background, Alberti partially overturns the classical model of the ars memoriae: the a priori architectural order of loci becomes the result of an activity of composition and combination, in which the imagines/ruins disrupt the flow of time and the continuum of space by displaying their specific nature as memory traces.

Discrimination of semantically similar verbal memory traces is affected in healthy aging

Mnemonic discrimination of highly similar memory traces is affected in healthy aging via changes in hippocampal pattern separation—i.e., the ability of the hippocampus to orthogonalize highly similar neural inputs. The decline of this process leads to a loss of episodic specificity. Because previous studies have almost exclusively tested mnemonic discrimination of visuospatial stimuli (e.g., objects or scenes), less is known about age-related effects on the episodic specificity of semantically similar traces. To address this gap, we designed a task to assess mnemonic discrimination of verbal stimuli as a function of semantic similarity based on word embeddings. Forty young (Mage = 21.7 years) and 40 old adults (Mage = 69.8 years) first incidentally encoded adjective-noun phrases, then performed a surprise recognition test involving exactly repeated and highly similar lure phrases. We found that increasing semantic similarity negatively affected mnemonic discrimination in both age groups, and that compared to young adults, older adults showed worse discrimination at medium levels of semantic similarity. These results indicate that episodic specificity of semantically similar memory traces is affected in aging via less efficient mnemonic operations and strengthen the notion that mnemonic discrimination is a modality-independent process supporting memory specificity across representational domains.

Individual differences in working memory capacity and temporal preparation: A secondary reanalysis.

The ability to prepare and maintain an optimal level of preparedness for action, across some unknown duration, is critical for human behavior. Temporal preparation has historically been analyzed in the context of reaction time (RT) experiments where the interval varies between the start of the trial, or foreperiod (FP), and the required response. Two main findings have come out of such paradigms: the variable FP effect (longer RTs to shorter vs. longer FPs) and the sequential FP effect (longer RTs when shorter FPs follow longer FPs). Several theoretical views of these FP effects have been proposed with some suggesting a dissociation while others argue for an implicit process driven by memory traces. One possible method to test these views of FP effects is to examine how individual differences in working memory capacity (WMC) moderate such effects. To this end, I reanalyzed data from three studies in which participants completed measures of WMC and a simple RT task with a variable FP. Results suggest that individual differences in WMC were related to the magnitude of the variable FP and the sequential FP effect in two of three individual studies. A "mega-analysis" provided supportive evidence for a relationship between WMC and both forms of FP effects. The present combined experimental-individual differences study provides a novel approach to better understand how and why individuals vary in temporal preparation ability. Through leveraging several large-scale databases unseen in FP research, I provide a new way of understanding FP effects and response timing more generally.

Chromatin plasticity predetermines neuronal eligibility for memory trace formation.

Memories are encoded by sparse populations of neurons but how such sparsity arises remains largely unknown. We found that a neuron's eligibility to be recruited into the memory trace depends on its epigenetic state prior to encoding. Principal neurons in the mouse lateral amygdala display intrinsic chromatin plasticity, which when experimentally elevated favors neuronal allocation into the encoding ensemble. Such chromatin plasticity occurred at genomic regions underlying synaptic plasticity and was accompanied by increased neuronal excitability in single neurons in real time. Lastly, optogenetic silencing of the epigenetically altered neurons prevented memory expression, revealing a cell-autonomous relationship between chromatin plasticity and memory trace formation. These results identify the epigenetic state of a neuron as a key factor enabling information encoding.

Epigenetic control of memory formation.

A neuron's suitability to participate in a memory trace is modulated by its epigenetic state.

Dynamic retrieval of events and associations from memory: An integrated account of item and associative recognition.

Memory theories distinguish between item and associative information, which are engaged by different tasks: item recognition uses item information to decide whether an event occurred in a particular context; associative recognition uses associative information to decide whether two events occurred together. Associative recognition is slower and less accurate than item recognition, suggesting that item and associative information may be represented in different forms and retrieved using different processes. Instead, I show how a dynamic model (Cox & Criss, 2020; Cox & Shiffrin, 2017) accounts for accuracy and response time distributions in both item and associative recognition with the same set of representations and processes. Item and associative information are both represented as vectors of features. Item and associative recognition both depend on comparing traces in memory with probes of memory in which item and associative features gradually accumulate. Associative features are slower to accumulate, but largely because they emerge from conjunctions of already-accumulated item features. I apply the model to data from 453 participants, each of whom performed an item and performed associative recognition following identical study conditions (Cox et al., 2018). Comparisons among restricted versions of the model show that its account of associative feature formation, coupled with limits on the rate at which features accumulate from multiple items, explains how and why the dynamics of associative recognition differ from those of item recognition even while both tasks rely on the same underlying representations. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

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.

Validation of a rodent model of episodic memory replay.

Vivid episodic memories in humans have been described as the replay of the flow of past events in sequential order. Recently, Panoz-Brown et al. Current Biology, 28, 1628-1634, (2018) developed an olfactory memory task in which rats were presented with a list of trial-unique odors in an encoding context; next, in a distinctive memory assessment context, the rats were rewarded for choosing the second to last item from the list while avoiding other items from the list. In a different memory assessment context, the fourth to last item was rewarded. According to the episodic memory replay hypothesis, the rat remembers the list items and searches these items to find the item at the targeted locations in the list. However, events presented sequentially differ in memory trace strength, allowing a rat to use the relative familiarity of the memory traces, instead of episodic memory replay, to solve the task. Here, we directly manipulated memory trace strength by manipulating the odor intensity of target odors in both the list presentation and memory assessment. The rats relied on episodic memory replay to solve the memory assessment in conditions in which reliance on memory trace strength is ruled out. We conclude that rats are able to replay episodic memories.

Repetition-Dependent Adaptation and Prediction Error Signalling in Schizophrenia Patients With Auditory Hallucinations: A Roving Mismatch Negativity Study

BackgroundDysregulated prediction error-signalling may explain auditory hallucinations in schizophrenia (SZ-AH). Roving mismatch negativity (rMMN) is an event-related potential (ERP) index where the deviant tone becomes the new standard with repetitions. Longer repetitions of standard stimuli yield a more positive sensory-adaptation response (Repetition Positivity–RP), elicit a stronger deviance-detection when interrupted (deviant negativity–DN), and the difference waveform between them reflects the strength of prediction-error signalling (mismatch negativity–MMN). MethodsTwenty-three SZ-AH patients and twenty-three healthy controls (HC) underwent rMMN assessment. Various standard stimuli were repeated in sets of 3, 8 and 33 yielding three components for RP (RP3, RP8, RP33), DN (DN3, DN8, DN33), and MMN (MMN3, MMN8, MMN33). Amplitudes and latencies were compared across groups. Correlation between (a) rMMN amplitudes and latencies, and clinical variables in SZ-AH, and (b) the RP-DN amplitude pair for all three repetition sets (3, 8, 33) were also examined. ResultsAll DN and MMN33 amplitudes were significantly suppressed in SZ-AH, while RP amplitudes were not. MMN33 latency was significantly longer in SZ-AH than HC. A few amplitudes and latencies significantly correlated with the frequency of AH. HC showed a significant positive correlation between RP-DN amplitude pairs for sets of 3 and 8 but not for 33; SZ-AH group’s correlation profile was opposite to this. DiscussionThe link between repetition-dependent sensory-adaptation and deviance-detection is perturbed in SZ-AH. The unimpaired RP profile in SZ-AH is due to potential interference of AH with auditory information processing, and does not indicate a preserved short-term plasticity of the echoic memory trace.

Affective music during episodic memory recollection modulates subsequent false emotional memory traces: an fMRI study.

Music is a powerful medium that influences our emotions and memories. Neuroscience research has demonstrated music's ability to engage brain regions associated with emotion, reward, motivation, and autobiographical memory. While music's role in modulating emotions has been explored extensively, our study investigates whether music can alter the emotional content of memories. Building on the theory that memories can be updated upon retrieval, we tested whether introducing emotional music during memory recollection might introduce false emotional elements into the original memory trace. We developed a 3-day episodic memory task with separate encoding, recollection, and retrieval phases. Our primary hypothesis was that emotional music played during memory recollection would increase the likelihood of introducing novel emotional components into the original memory. Behavioral findings revealed two key outcomes: 1) participants exposed to music during memory recollection were more likely to incorporate novel emotional components congruent with the paired music valence, and 2) memories retrieved 1day later exhibited a stronger emotional tone than the original memory, congruent with the valence of the music paired during the previous day's recollection. Furthermore, fMRI results revealed altered neural engagement during story recollection with music, including the amygdala, anterior hippocampus, and inferior parietal lobule. Enhanced connectivity between the amygdala and other brain regions, including the frontal and visual cortex, was observed during recollection with music, potentially contributing to more emotionally charged story reconstructions. These findings illuminate the interplay between music, emotion, and memory, offering insights into the consequences of infusing emotional music into memory recollection processes.

A reduction in self-reported confidence accompanies the recall of memories distorted by prototypes

When we recall a past event, we reconstruct the event based on a combination of episodic details and semantic knowledge (e.g., prototypes). Though prototypes can impair the veracity of recall, it remains unclear whether we are metacognitively aware of the distortions they introduce. To address this, we conducted six experiments in which participants learned object-colour/object-location pairs and subsequently recalled the colour/location when cued with the object. Leveraging unsupervised machine learning algorithms, we extracted participant-specific prototypes and embedded responses in two-dimensional space to quantify prototype-based distortions in individual memory traces. Our findings reveal robust and conceptually replicable evidence to suggest that prototype-based distortion is accompanied by a reduction in self-reported confidence - an implicit measure of metacognitive awareness. Critically, we find evidence to suggest that it is prototype-based distortion of a memory trace that undermines confidence, rather than a lack of confidence biasing reconstruction towards the use of prototypes. Collectively, these findings suggest that we possess metacognitive awareness of distortions embedded in our memories.

Retrieval of contextual memory can be predicted by CA3 remapping and is differentially influenced by NMDAR activity in rat hippocampus subregions.

Episodic memory is essential to navigate in a changing environment by recalling past events, creating new memories, and updating stored information from experience. Although the mechanisms for acquisition and consolidation have been profoundly studied, much less is known about memory retrieval. Hippocampal spatial representations are key for retrieval of contextually guided episodic memories. Indeed, hippocampal place cells exhibit stable location-specific activity which is thought to support contextual memory, but can also undergo remapping in response to environmental changes. It is unclear if remapping is directly related to the expression of different episodic memories. Here, using an incidental memory recognition task in rats, we showed that retrieval of a contextually guided memory is reflected by the levels of CA3 remapping, demonstrating a clear link between external cues, hippocampal remapping, and episodic memory retrieval that guides behavior. Furthermore, we describe NMDARs as key players in regulating the balance between retrieval and memory differentiation processes by controlling the reactivation of specific memory traces. While an increase in CA3 NMDAR activity boosts memory retrieval, dentate gyrus NMDAR activity enhances memory differentiation. Our results contribute to understanding how the hippocampal circuit sustains a flexible balance between memory formation and retrieval depending on the environmental cues and the internal representations of the individual. They also provide new insights into the molecular mechanisms underlying the contributions of hippocampal subregions to generate this balance.

Endel Tulving (1927-2023).

This article presents an obituary for Endel Tulving. Tulving's educational and professional careers are summarized. His work in the field of human memory is detailed. It is noted that Tulving's look at the field of verbal learning in the late 1950s persuaded him that the dominant associative tradition missed many important aspects of human memory. His research found that at the time of retrieval, memory for the original event may be successfully reinstated only by contextual cues that interact in a complementary fashion with the specifically encoded memory trace, a process that Tulving referred to as "synergistic ecphory". He is also known for his work on memory systems. In his book, Elements of Episodic Memory published in 1983, Tulving proposed that memory for experienced events, episodic memory, should be distinguished from general knowledge of the world, semantic memory, and from procedural memory, the learned ability to perform such skilled procedures as riding a bicycle or playing a musical instrument. He also proposed an evolutionary framework for these different but related systems, suggesting that simple animals show only procedural memory, more complex animals are consciously aware of their knowledge of the world, but only humans possess episodic memory-the ability to use "mental time travel" to consciously recreate past experiences and to imagine possible future events. Although known initially for his purely cognitive behavioral research, during the 1980s and 1990s, Tulving increasingly incorporated neuropsychological and neuroimaging approaches into his work. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

Brain oscillations: Hippocampal–prefrontal ripples unfolded

Memory consolidation is the process of translating memory traces from the hippocampus to the cortex. Hippocampal ripples are key in driving this transfer. A new study now shows that independent cortical ripples can suppress this communication. What could be the underlying mechanisms?

Saving Kurapaty: The Memorialisation of Victims of Political Repressions in Belarus as a Transitional Justice Mechanism

Abstract This article examines the memorialisation of victims of political repressions as part of a transitional justice policy. By drawing on insights from memory studies, it reveals how such memorialisation practices can become a dynamic transitional justice mechanism developed by grassroots movements. The case study in focus is the arrangement of memorials to the victims of Stalinist repressions in Kurapaty near Minsk, Belarus, identifying societal actors participating in memorialisation practices and exploring their values. This study provides a more complex understanding of questions concerning transitional justice, memorialisation, and material traces of traumatic memory embodied in the memorials.

Memory traces of duration and location in the right intraparietal sulcus

Time and space form an integral part of every human experience, and for the neuronal representation of these perceptual dimensions, previous studies point to the involvement of the right-hemispheric intraparietal sulcus and structures in the medial temporal lobe. Here we used multi-voxel pattern analysis (MVPA) to investigate long-term memory traces for temporal and spatial stimulus features in those areas. Participants were trained on four images associated with short versus long durations and with left versus right locations. Our results demonstrate stable representations of both temporal and spatial information in the right posterior intraparietal sulcus. Building upon previous findings of stable neuronal codes for directly perceived durations and locations, these results show that the reactivation of long-term memory traces for temporal and spatial features can be decoded from neuronal activation patterns in the right parietal cortex.

Persistent Interruption in Parvalbumin-Positive Inhibitory Interneurons: Biophysical and Mathematical Mechanisms.

Persistent activity in excitatory pyramidal cells (PYRs) is a putative mechanism for maintaining memory traces during working memory. We have recently demonstrated persistent interruption of firing in fast-spiking parvalbumin-expressing interneurons (PV-INs), a phenomenon that could serve as a substrate for persistent activity in PYRs through disinhibition lasting hundreds of milliseconds. Here, we find that hippocampal CA1 PV-INs exhibit type 2 excitability, like striatal and neocortical PV-INs. Modeling and mathematical analysis showed that the slowly inactivating potassium current KV1 contributes to type 2 excitability, enables the multiple firing regimes observed experimentally in PV-INs, and provides a mechanism for robust persistent interruption of firing. Using a fast/slow separation of times scales approach with the KV1 inactivation variable as a bifurcation parameter shows that the initial inhibitory stimulus stops repetitive firing by moving the membrane potential trajectory onto a coexisting stable fixed point corresponding to a nonspiking quiescent state. As KV1 inactivation decays, the trajectory follows the branch of stable fixed points until it crosses a subcritical Hopf bifurcation (HB) and then spirals out into repetitive firing. In a model describing entorhinal cortical PV-INs without KV1, interruption of firing could be achieved by taking advantage of the bistability inherent in type 2 excitability based on a subcritical HB, but the interruption was not robust to noise. Persistent interruption of firing is therefore broadly applicable to PV-INs in different brain regions but is only made robust to noise in the presence of a slow variable, KV1 inactivation.

Accelerating Graph Analytics Using Attention-Based Data Prefetcher

Graph analytics shows promise for solving challenging problems on relational data. However, memory constraints arise from the large size of graphs and the high complexity of algorithms. Data prefetching is a crucial technique to hide memory access latency by predicting and fetching data into the memory cache beforehand. Traditional prefetchers struggle with fixed rules in adapting to complex memory access patterns in graph analytics. Machine learning (ML) algorithms, particularly long short-term memory (LSTM) models, excel in memory access prediction. However, they encounter challenges such as difficulty in learning interleaved access patterns and high storage costs when predicting in large memory address space. In addition, there remains a gap between designing a high-performance ML-based memory access predictor and developing an effective ML-based prefetcher for an existing memory system. In this work, we propose a novel Attention-based prefetching framework to accelerate graph analytics applications. To achieve high-performance memory access prediction, we propose A2P, a novel Attention-based memory Access Predictor for graph analytics. We use the multi-head self-attention mechanism to extract features from memory traces. We design a novel bitmap labeling method to collect future deltas within a spatial range, making interleaved patterns easier to learn. We introduce a novel super page concept, allowing the model to surpass physical page constraints. To integrate A2P into a memory system, we design a three-module prefetching framework composed of an existing memory hierarchy, a prefetch controller, and the predictor A2P. In addition, we propose a hybrid design to combine A2P and existing hardware prefetchers for higher prefetching performance. We evaluate A2P and the prefetching framework using the widely used GAP benchmark. Prediction experiments show that for the top three predictions, A2P outperforms the widely used state-of-the-art LSTM-based model by 23.1% w.r.t. Precision, 21.2% w.r.t. Recall, and 10.4% w.r.t. Coverage. Prefetching experiments show that A2P provides 18.4% IPC Improvement on average, outperforming state-of-the-art prefetchers BO by 17.2%, ISB by 15.0%, and Delta-LSTM by 10.9%. The hybrid prefetcher combining A2P and ISB achieves 21.7% IPC Improvement, outperforming the hybrid of BO and ISB by 16.3%.

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'.