Neural reinstatement reveals divided organization of fear and extinction memories in the human brain

Hennings, Augustin C.; McClay, Mason; Drew, Michael R.; Lewis-Peacock, Jarrod A.; Dunsmoor, Joseph E.

doi:10.1016/j.cub.2021.11.004

Cited by 19 publications

(13 citation statements)

References 116 publications

(164 reference statements)

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“…In support of the emotion-facilitated integration, our imaging results showed that emotional information increased hippocampal reactivation of related memories during both encoding and retrieval. Consistent with emerging work using MVPA to study human episodic memory (Heinen et al, 2023;Hennings et al, 2022;Staresina et al, 2012;Xue et al, 2010), our findings of emotionally-charged increases in reactivation reflect trial-specific reinstatement (i.e., pair-specific similarity) controlling for a general category-level representation (i.e., across-pair similarity). Given the benefits of hippocampal pattern completion on integrative encoding (Kuhl et al, 2010;Shohamy and Wagner, 2008;Wong et al, 2019), the increased hippocampal reactivation of first neutral memories during encoding of second emotional associations could facilitate online integration by rapidly linking neural representations of related information.…”

Section: Emotion-facilitated Memory Integrationsupporting

confidence: 88%

Emotional information facilitates or disrupts memory integration through distinct hippocampal processes of reactivation and connectivity

Zhu

Liu

Kohn

et al. 2023

Preprint

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Emotion has a significant impact on how related experiences are organized into integrated memories. However, the neurobiological mechanisms of how emotion modulates memory integration for related information with different valences remain unclear. In this between-subject functional magnetic resonance imaging (fMRI) study, we investigated different emotional modulations of memory integration by manipulating the valence of stimuli used in an associative memory paradigm. Three groups of participants were tested: one group integrated emotional (i.e., negative) information with neutral information, one group integrated two emotional pieces of information, and one control group integrated two neutral pieces of information. Behaviorally, emotional information facilitated its integration with neutral information but interfered with the other emotional information. Neurally, the emotion-induced facilitation effect, occurring on memory integration of neutral and emotional information, was associated with increased trial-specific reactivation in the hippocampus during both encoding and retrieval. This facilitated integration was also supported by strengthened hippocampal connectivity with the amygdala, as well as a set of neocortical areas related to emotion regulation and the default mode network (DMN). In contrast, the emotion-induced interference effect, occurring on memory integration of two emotional pieces of information, was associated with impaired hippocampal trial-specific reactivation during retrieval that appeared to offset the facilitating effect of increased reactivation during encoding. Similar but relatively weak hippocampal connectivity was found underlying this interfered integration. Taken together, emotional information facilitates memory integration with neutral information, while disrupting the integration with other emotional information, through distinct dynamical processes of hippocampal trial-specific reactivation and connectivity.

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Section: Emotion-facilitated Memory Integrationsupporting

confidence: 88%

Emotional information facilitates or disrupts memory integration through distinct hippocampal processes of reactivation and connectivity

Zhu

Liu

Kohn

et al. 2023

Preprint

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“…C Performances on the Visser et al dataset 45 ( n = 94). D Performances on the Hennings et al dataset 43 ( n = 48). E Performances on the Reddan et al dataset 46 ( n = 68).…”

Section: Resultsmentioning

confidence: 99%

“…We first tested the extended models on three visual threat conditioning datasets ( n = 299, n = 94, and n = 48, respectively) that differed in visual stimuli, trial structure, and experimental durations 43 – 45 . All models showed significant accuracies in classifying CS+ from CS- across all three independent datasets (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…A few studies have employed MVPA methods to examine neural representations during threat conditioning and extinction 43 , 46 – 48 . The datasets used in these studies, however, were much smaller ( n < 70) and contained one version of the conditioning paradigms, thus raising concerns regarding the sensitivity and generalizability of MVPA studies 49 , 50 .…”

Section: Discussionmentioning

confidence: 99%

“…All participants in those datasets underwent the Milad threat conditioning and extinction paradigm 25 , 26 . Data from the external validation datasets 3–9 were from other studies that used variants of threat conditioning paradigms or other affect-related paradigms 19 , 22 , 34 , 43 – 46 (see Supplementary Table 4 for the summary). As stated in all of the above-referenced studies, all procedures were approved by the Institutional Review Boards of the corresponding research sites.…”

Section: Methodsmentioning

confidence: 99%

See 2 more Smart Citations

Distributed neural representations of conditioned threat in the human brain

Wen,

Pace-Schott,

Lazar

et al. 2024

Nat Commun

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Detecting and responding to threat engages several neural nodes including the amygdala, hippocampus, insular cortex, and medial prefrontal cortices. Recent propositions call for the integration of more distributed neural nodes that process sensory and cognitive facets related to threat. Integrative, sensitive, and reproducible distributed neural decoders for the detection and response to threat and safety have yet to be established. We combine functional MRI data across varying threat conditioning and negative affect paradigms from 1465 participants with multivariate pattern analysis to investigate distributed neural representations of threat and safety. The trained decoders sensitively and specifically distinguish between threat and safety cues across multiple datasets. We further show that many neural nodes dynamically shift representations between threat and safety. Our results establish reproducible decoders that integrate neural circuits, merging the well-characterized ‘threat circuit’ with sensory and cognitive nodes, discriminating threat from safety regardless of experimental designs or data acquisition parameters.

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Neuroimaging of Fear Extinction

LaBar

2023

Fear Extinction

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Neural reinstatement reveals divided organization of fear and extinction memories in the human brain

Cited by 19 publications

References 116 publications

Emotional information facilitates or disrupts memory integration through distinct hippocampal processes of reactivation and connectivity

Emotional information facilitates or disrupts memory integration through distinct hippocampal processes of reactivation and connectivity

Distributed neural representations of conditioned threat in the human brain

Neuroimaging of Fear Extinction

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