Contextual reinstatement promotes extinction generalization in healthy adults but not PTSD

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

doi:10.1016/j.neuropsychologia.2020.107573

Cited by 31 publications

(30 citation statements)

References 67 publications

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“…As we previously reported, 42 the success of fear conditioning and extinction learning was assessed by skin conductance responses (SCRs) and trial-by-trial shock expectancy (yes or no 2-alternative forced choice [AFC]). Analyses focused on differential responding (i.e., CS+ > CSÀ differences; Figure 2A; see Figure S1 for full behavioral results).…”

Section: Explicit and Implicit Measures Of Learningmentioning

confidence: 99%

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

et al. 2022

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Section: Explicit and Implicit Measures Of Learningmentioning

confidence: 99%

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

et al. 2022

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“…Interestingly, there is evidence that distinct phases of a fear conditioning experiment can be understood as separable mental contexts that uniquely organize memory (Dunsmoor et al, 2018;Hennings et al, 2020) in a manner consistent with how shifts in mental context segment experience for distinct episodes (Clewett et al, 2019;DuBrow et al, 2017). That source memory misattributions were more strongly predictive of the retroactive enhancement in item memory compared to CS type (Fig.…”

Section: Discussionmentioning

confidence: 88%

“…During pre-conditioning, participants viewed pictures of animals and tools and made a 2-AFC category judgement (animal, tool) using a button box in The rationale for presenting scene pictures during the ITI was for multivariate pattern analysis of the extinction context, but is not related to the purposes of the episodic memory data reported here. Participants returned ~24 hours later and underwent a test of fear renewal (data reported inHennings et al, 2020), and a surprise recognition memory test inside the scanner.…”

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confidence: 99%

Emotional learning retroactively enhances item memory but distorts source attributions

Hennings¹,

Lewis-Peacock²,

Dunsmoor³

2020

Preprint

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An adaptive memory system should prioritize select information surrounding a powerful learning event that may prove useful for predicting future meaningful events. The behavioral tagging hypothesis provides a mechanistic framework to interpret how weak experiences persist as durable memories through temporal association with a strong experience. Importantly, memories are composed of multiple elements, and different mnemonic aspects of the same experience may be uniquely affected by mechanisms that retroactively modulate weakly encoded memory. Here we investigated how emotional learning affects item and source memory for related events encoded close in time. Participants encoded trial-unique category exemplars before, during, and after Pavlovian fear conditioning. Results showed selective retroactive enhancements in 24-hour item memory were accompanied by a bias to misattribute items to the temporal context of fear conditioning. The strength of this source memory bias correlated with participants’ retroactive item memory enhancement, and source misattribution to the emotional context predicted whether items were remembered overall. In the framework of behavioral tagging: memory attribution was biased to the temporal context of the stronger event (fear conditioning) that provided the putative source of memory stabilization for the weaker event (non-emotional learning). We additionally found that fear conditioning selectively and retroactively enhanced stimulus typicality ratings for related items, and that stimulus typicality also predicted overall item memory. Collectively, these results provide new evidence that items related to an emotional event are misattributed to the temporal context of the emotional event and judged to be more representative of their semantic category. Both processes may help facilitate memory retrieval for related events encoded close in time.

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“…The copyright holder for this this version posted November 11, 2021. ; https://doi.org/10.1101/2021.11.09.467993 doi: bioRxiv preprint inhibition of fear behaviors (Zhang et al, 2015), each requiring recall of safety information from memory. Affective valuation, response-inhibition, and recall processes all converge on these standard safety-processing regions (Harrison et al, 2017;Hennings et al, 2020;Hermann et al, 2020;Merz et al, 2018;Roy et al, 2012). The vmPFC has a notably multifaceted functional role, modulating both fear and safety expression, rather than unidirectional threat-inhibition (Battaglia et al, 2021;Tashjian et al, 2021).…”

Section: Discussionmentioning

confidence: 99%

Cortico-striatal activity characterizes human safety learning via Pavlovian conditioned inhibition

Laing

Steward

Davey

et al. 2021

Preprint

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Safety learning generates associative links between neutral stimuli and the absence of threat, promoting the inhibition of fear and security-seeking behaviours. Precisely how safety learning is mediated at the level of underlying brain systems, particularly in humans, remains unclear. Here, we integrated a novel Pavlovian conditioned inhibition task with ultra-high field (UHF) fMRI to examine the neural basis of inhibitory safety learning in 49 healthy participants. In our task, participants were conditioned to two safety signals: a conditioned inhibitor that predicted threat-omission when paired with a known threat signal (A+/AX-), and a standard safety signal that generally predicted threat-omission (BC-). Both safety signals evoked equivalent autonomic and subjective learning responses but diverged strongly in terms of underlying brain activation. The conditioned inhibitor was characterized by more prominent activation of the dorsal striatum, anterior insular and dorsolateral prefrontal cortex compared to the standard safety signal, whereas the latter evoked greater activation of the ventromedial prefrontal cortex, posterior cingulate and hippocampus, among other regions. Further analyses of the conditioned inhibitor indicated that its initial learning was characterized by consistent engagement of dorsal striatal, midbrain, thalamic, premotor, and prefrontal subregions. These findings suggest that safety learning via conditioned inhibition involves a distributed cortico-striatal circuitry, separable from broader cortical regions involved with processing standard safety signals (e.g., CS-). This cortico-striatal system could represent a novel neural substrate of safety learning, underlying the initial generation of ‘stimulus-safety’ associations, distinct from wider cortical correlates of safety processing, which facilitate the behavioral outcomes of learning.Significance statementIdentifying safety is critical for maintaining adaptive levels of anxiety, but the neural mechanisms of human safety learning remain unclear. Using ultra-high field fMRI, we compared learning-related brain activity for a conditioned inhibitor, which actively predicted threat-omission, and a standard safety signal (CS-), which was passively unpaired with threat. The inhibitor engaged an extended circuitry primarily featuring the dorsal striatum, along with thalamic, midbrain, and premotor/prefrontal cortex regions. The CS-exclusively involved cortical safety-related regions observed in basic safety conditioning, such as the vmPFC. These findings extend current models to include learning-specific mechanisms for encoding stimulus-safety associations, which might be distinguished from expression-related cortical mechanisms. These insights may suggest novel avenues for targeting dysfunctional safety learning in psychopathology.

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Contextual reinstatement promotes extinction generalization in healthy adults but not PTSD

Cited by 31 publications

References 67 publications

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

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

Emotional learning retroactively enhances item memory but distorts source attributions

Cortico-striatal activity characterizes human safety learning via Pavlovian conditioned inhibition

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