Stress Alters the Neural Context for Building New Memories

Stressful events affect mnemonic processing, in particular for emotionally arousing events. Previous research on the mechanisms underlying stress effects on human memory focused on stress-induced changes in the neural activity elicited by a stimulus. We tested an alternative mechanism and hypothesized that stress may already alter the neural context for successful memory formation, reflected in the neural activity preceding a stimulus. Therefore, 69 participants underwent a stress or control procedure before encoding neutral and negative pictures. During encoding, we recorded high-density EEG and analyzed—based on multivariate searchlight analyses—oscillatory activity and cross-frequency coupling patterns before stimulus onset that were predictive of memory tested 24 hr later. Prestimulus theta predicted subsequent memory in controls but not in stressed participants. Instead, prestimulus gamma predicted successful memory formation after stress, specifically for emotional material. Likewise, stress altered the patterns of prestimulus theta–beta and theta–gamma phase–amplitude coupling predictive of subsequent memory, again depending on the emotionality of the presented material. Our data suggest that stress changes the neural context for building new memories, tuning this neural context specifically to the encoding of emotionally salient events. These findings point to a yet unknown mechanism through which stressful events may change (emotional) memory formation.

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Selectively Interfering With Intrusive but Not Voluntary Memories of a Trauma Film: Accounting for the Role of Associative Memory

Clinical Psychological Science ◽

10.1177/2167702621998315 ◽

2021 ◽

pp. 216770262199831

Author(s):

Alex Lau-Zhu ◽

Richard N. Henson ◽

Emily A. Holmes

Keyword(s):

Emotional Disorders ◽

Traumatic Event ◽

Emotional Memory ◽

Control Procedure ◽

Witness Testimony ◽

Intrusive Memories ◽

Therapeutic Benefits ◽

Selective Interference ◽

Intrusive Memory

Intrusive memories of a traumatic event can be reduced by a subsequent interference procedure, seemingly sparing voluntary memory for that event. This selective-interference effect has potential therapeutic benefits (e.g., for emotional disorders) and legal importance (e.g., for witness testimony). However, the measurements of intrusive memory and voluntary memory typically differ in the role of associations between a cue and the emotional memory “hotspots.” To test this, we asked participants to watch a traumatic film followed by either an interference procedure (reminder plus Tetris) or control procedure (reminder only). Measurement of intrusions (using a laboratory task) and voluntary memory (recognition for film stills) were crossed with the presence or absence of associative cues. The reminder-plus-Tetris group exhibited fewer intrusions despite comparable recognition memory, replicating the results of prior studies. Note that this selective interference did not appear to depend on associative cues. This involuntary versus voluntary memory dissociation for emotional material further supports separate-trace memory theories and has applied advantages.

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The Rapid Extraction of Gist—Early Neural Correlates of High-level Visual Processing

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_00100 ◽

2012 ◽

Vol 24 (2) ◽

pp. 521-529 ◽

Cited By ~ 13

Author(s):

Frank Oppermann ◽

Uwe Hassler ◽

Jörg D. Jescheniak ◽

Thomas Gruber

Keyword(s):

Visual Processing ◽

Time Course ◽

Occipital Cortex ◽

Stimulus Onset ◽

Gamma Band ◽

Oscillatory Activity ◽

Rapid Extraction ◽

The Right ◽

High Level ◽

Individual Objects

The human cognitive system is highly efficient in extracting information from our visual environment. This efficiency is based on acquired knowledge that guides our attention toward relevant events and promotes the recognition of individual objects as they appear in visual scenes. The experience-based representation of such knowledge contains not only information about the individual objects but also about relations between them, such as the typical context in which individual objects co-occur. The present EEG study aimed at exploring the availability of such relational knowledge in the time course of visual scene processing, using oscillatory evoked gamma-band responses as a neural correlate for a currently activated cortical stimulus representation. Participants decided whether two simultaneously presented objects were conceptually coherent (e.g., mouse–cheese) or not (e.g., crown–mushroom). We obtained increased evoked gamma-band responses for coherent scenes compared with incoherent scenes beginning as early as 70 msec after stimulus onset within a distributed cortical network, including the right temporal, the right frontal, and the bilateral occipital cortex. This finding provides empirical evidence for the functional importance of evoked oscillatory activity in high-level vision beyond the visual cortex and, thus, gives new insights into the functional relevance of neuronal interactions. It also indicates the very early availability of experience-based knowledge that might be regarded as a fundamental mechanism for the rapid extraction of the gist of a scene.

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Transient neuronal suppression for exploitation of new sensory evidence

Nature Communications ◽

10.1038/s41467-021-27697-4 ◽

2022 ◽

Vol 13 (1) ◽

Author(s):

Maxwell Shinn ◽

Daeyeol Lee ◽

John D. Murray ◽

Hyojung Seo

Keyword(s):

Decision Making ◽

Neural Activity ◽

Temporal Integration ◽

Motor Preparation ◽

Stimulus Onset ◽

Frontal Eye Field ◽

Perceptual Decision Making ◽

Behavioral Studies ◽

The Face ◽

Sensory Evidence

AbstractIn noisy but stationary environments, decisions should be based on the temporal integration of sequentially sampled evidence. This strategy has been supported by many behavioral studies and is qualitatively consistent with neural activity in multiple brain areas. By contrast, decision-making in the face of non-stationary sensory evidence remains poorly understood. Here, we trained monkeys to identify and respond via saccade to the dominant color of a dynamically refreshed bicolor patch that becomes informative after a variable delay. Animals’ behavioral responses were briefly suppressed after evidence changes, and many neurons in the frontal eye field displayed a corresponding dip in activity at this time, similar to that frequently observed after stimulus onset but sensitive to stimulus strength. Generalized drift-diffusion models revealed consistency of behavior and neural activity with brief suppression of motor output, but not with pausing or resetting of evidence accumulation. These results suggest that momentary arrest of motor preparation is important for dynamic perceptual decision making.

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The Making of Long-Lasting Memories: A Fruit Fly Perspective

Frontiers in Behavioral Neuroscience ◽

10.3389/fnbeh.2021.662129 ◽

2021 ◽

Vol 15 ◽

Author(s):

Camilla Roselli ◽

Mani Ramaswami ◽

Tamara Boto ◽

Isaac Cervantes-Sandoval

Keyword(s):

Learning And Memory ◽

Neural Activity ◽

Molecular Mechanisms ◽

De Novo ◽

Fruit Fly ◽

Memory Formation ◽

Synaptic Activity ◽

Model Organisms ◽

Transient Wave ◽

Control Of Gene Expression

Understanding the nature of the molecular mechanisms underlying memory formation, consolidation, and forgetting are some of the fascinating questions in modern neuroscience. The encoding, stabilization and elimination of memories, rely on the structural reorganization of synapses. These changes will enable the facilitation or depression of neural activity in response to the acquisition of new information. In other words, these changes affect the weight of specific nodes within a neural network. We know that these plastic reorganizations require de novo protein synthesis in the context of Long-term memory (LTM). This process depends on neural activity triggered by the learned experience. The use of model organisms like Drosophila melanogaster has been proven essential for advancing our knowledge in the field of neuroscience. Flies offer an optimal combination of a more straightforward nervous system, composed of a limited number of cells, and while still displaying complex behaviors. Studies in Drosophila neuroscience, which expanded over several decades, have been critical for understanding the cellular and molecular mechanisms leading to the synaptic and behavioral plasticity occurring in the context of learning and memory. This is possible thanks to sophisticated technical approaches that enable precise control of gene expression in the fruit fly as well as neural manipulation, like chemogenetics, thermogenetics, or optogenetics. The search for the identity of genes expressed as a result of memory acquisition has been an active interest since the origins of behavioral genetics. From screenings of more or less specific candidates to broader studies based on transcriptome analysis, our understanding of the genetic control behind LTM has expanded exponentially in the past years. Here we review recent literature regarding how the formation of memories induces a rapid, extensive and, in many cases, transient wave of transcriptional activity. After a consolidation period, transcriptome changes seem more stable and likely represent the synthesis of new proteins. The complexity of the circuitry involved in memory formation and consolidation is such that there are localized changes in neural activity, both regarding temporal dynamics and the nature of neurons and subcellular locations affected, hence inducing specific temporal and localized changes in protein expression. Different types of neurons are recruited at different times into memory traces. In LTM, the synthesis of new proteins is required in specific subsets of cells. This de novo translation can take place in the somatic cytoplasm and/or locally in distinct zones of compartmentalized synaptic activity, depending on the nature of the proteins and the plasticity-inducing processes that occur. We will also review recent advances in understanding how localized changes are confined to the relevant synapse. These recent studies have led to exciting discoveries regarding proteins that were not previously involved in learning and memory processes. This invaluable information will lead to future functional studies on the roles that hundreds of new molecular actors play in modulating neural activity.

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Thalamic theta phase alignment predicts human memory formation and anterior thalamic cross-frequency coupling

eLife ◽

10.7554/elife.07578 ◽

2015 ◽

Vol 4 ◽

Cited By ~ 17

Author(s):

Catherine M Sweeney-Reed ◽

Tino Zaehle ◽

Jürgen Voges ◽

Friedhelm C Schmitt ◽

Lars Buentjen ◽

...

Keyword(s):

Human Memory ◽

Gamma Oscillations ◽

Memory Formation ◽

Anterior Thalamic Nucleus ◽

Memory Processing ◽

Phase Alignment ◽

Theta Frequency ◽

Frequency Coupling ◽

Theta Phase ◽

Cross Frequency Coupling

Previously we reported electrophysiological evidence for a role for the anterior thalamic nucleus (ATN) in human memory formation (<xref ref-type="bibr" rid="bib29">Sweeney-Reed et al., 2014</xref>). Theta-gamma cross-frequency coupling (CFC) predicted successful memory formation, with the involvement of gamma oscillations suggesting memory-relevant local processing in the ATN. The importance of the theta frequency range in memory processing is well-established, and phase alignment of oscillations is considered to be necessary for synaptic plasticity. We hypothesized that theta phase alignment in the ATN would be necessary for memory encoding. Further analysis of the electrophysiological data reveal that phase alignment in the theta rhythm was greater during successful compared with unsuccessful encoding, and that this alignment was correlated with the CFC. These findings support an active processing role for the ATN during memory formation.

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Prestimulus feedback connectivity biases the content of visual experiences

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1817317116 ◽

2019 ◽

Vol 116 (32) ◽

pp. 16056-16061 ◽

Cited By ~ 5

Author(s):

Elie Rassi ◽

Andreas Wutz ◽

Nadia Müller-Voggel ◽

Nathan Weisz

Keyword(s):

Neural Activity ◽

Activity Patterns ◽

Low Frequency ◽

Brain Regions ◽

Stimulus Onset ◽

Neural Excitability ◽

Gamma Frequency ◽

Face Area ◽

Oscillatory Power ◽

The Impact

Ongoing fluctuations in neural excitability and in networkwide activity patterns before stimulus onset have been proposed to underlie variability in near-threshold stimulus detection paradigms—that is, whether or not an object is perceived. Here, we investigated the impact of prestimulus neural fluctuations on the content of perception—that is, whether one or another object is perceived. We recorded neural activity with magnetoencephalography (MEG) before and while participants briefly viewed an ambiguous image, the Rubin face/vase illusion, and required them to report their perceived interpretation in each trial. Using multivariate pattern analysis, we showed robust decoding of the perceptual report during the poststimulus period. Applying source localization to the classifier weights suggested early recruitment of primary visual cortex (V1) and ∼160-ms recruitment of the category-sensitive fusiform face area (FFA). These poststimulus effects were accompanied by stronger oscillatory power in the gamma frequency band for face vs. vase reports. In prestimulus intervals, we found no differences in oscillatory power between face vs. vase reports in V1 or in FFA, indicating similar levels of neural excitability. Despite this, we found stronger connectivity between V1 and FFA before face reports for low-frequency oscillations. Specifically, the strength of prestimulus feedback connectivity (i.e., Granger causality) from FFA to V1 predicted not only the category of the upcoming percept but also the strength of poststimulus neural activity associated with the percept. Our work shows that prestimulus network states can help shape future processing in category-sensitive brain regions and in this way bias the content of visual experiences.

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When encodong yields remembering: insights from event-related neuroimaging

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.1999.0481 ◽

1999 ◽

Vol 354 (1387) ◽

pp. 1307-1324 ◽

Cited By ~ 147

Author(s):

Anthony D. Wagner ◽

Wilma Koutstaal ◽

Daniel L. Schacter

Keyword(s):

Neural Activity ◽

Functional Neuroimaging ◽

Event Related Potentials ◽

Human Memory ◽

Memory Encoding ◽

Positron Emission ◽

Related Potentials ◽

The Rich ◽

Dm Effect ◽

The Brain

To understand human memory, it is important to determine why some experiences are remembered whereas others are forgotten. Until recently, insights into the neural bases of human memory encoding, the processes by which information is transformed into an enduring memory trace, have primarily been derived from neuropsychological studies of humans with select brain lesions. The advent of functional neuroimaging methods, such as positron emission tomography (PET) and functional magnetic resonance imaging (fMRI), has provided a new opportunity to gain additional understanding of how the brain supports memory formation. Importantly, the recent development of event–related fMRI methods now allows for examination of trial–by–trial differences in neural activity during encoding and of the consequences of these differences for later remembering. In this review, we consider the contributions of PET and fMRI studies to the understanding of memory encoding, placing a particular emphasis on recent event–related fMRI studies of the Dm effect: that is, differences in neural activity during encoding that are related to differences in subsequent memory. We then turn our attention to the rich literature on the Dm effect that has emerged from studies using event–related potentials (ERPs). It is hoped that the integration of findings from ERP studies, which offer higher temporal resolution, with those from event–related fMRI studies, which offer higher spatial resolution, will shed new light on when and why encoding yields subsequent remembering.

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