Asymmetric effects of emotion on mnemonic interference

Leal, Stephanie L.; Tighe, Sarah K.; Yassa, Michael A.

doi:10.1016/j.nlm.2014.02.013

Cited by 81 publications

(140 citation statements)

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“…Thus, increasing interference in mnemonic discrimination tasks, defined as the parametric similarity along one or more domains, including visual appearance or proximity in space and/or time, poses a demand for pattern separation. Manipulation of interference along other dimensions is also possible, such as reward 50 and valence 51,52 .…”

Section: Hippocampal Pattern Separation and Episodic Memorymentioning

confidence: 99%

“…Chronic stress manipulations have been used in animal models of depression to examine many of the core features of depression such as anhedonia, despair, appetite changes and anxious behavior 106 , and these models typically result in reduced hippocampal volume, which has been attributed to CA3 dendritic retraction and suppressed DG neurogenesis 107–109 . Recent work has shown that individuals with depressive symptoms have a diminished capacity to discriminate highly similar neutral objects 110–112 and scene stimuli 52 . Furthermore, discrimination of negative scenes is enhanced in individuals with depressive symptoms in a manner that corresponds to the severity of the depressive phenotype 52 .…”

Section: Neuropsychiatric Diseasementioning

confidence: 99%

“…Recent work has shown that individuals with depressive symptoms have a diminished capacity to discriminate highly similar neutral objects 110–112 and scene stimuli 52 . Furthermore, discrimination of negative scenes is enhanced in individuals with depressive symptoms in a manner that corresponds to the severity of the depressive phenotype 52 . This behavioral difference is accompanied by increased amygdala activity and decreased DG/CA3 activity in high-resolution fMRI.…”

Section: Neuropsychiatric Diseasementioning

confidence: 99%

“…Discrimination accuracy also correlates with multiple measures of negative emotionality in those with ASD. Although it is still very early to say for certain, it is possible that the hyperdiscrimination observed in ASD is related to the negativity-related hyperdiscrimination observed in depression 52 and may stem from limbic imbalance. However, neural studies are needed to formally test these hypotheses.…”

Section: Neuropsychiatric Diseasementioning

confidence: 99%

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Integrating new findings and examining clinical applications of pattern separation

2018

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Pattern separation, the ability to independently represent and store similar experiences, is a crucial facet of episodic memory. Growing evidence suggests that the hippocampus possesses unique circuitry that is computationally capable of resolving mnemonic interference by using pattern separation. In this Review, we discuss recent advances in the understanding of this process and evaluate the caveats and limitations of linking across animal and human studies. We summarize clinical and translational studies using methods that are sensitive to pattern separation impairments, an approach that stems from the fact that the hippocampus is a major site of disruption in many brain disorders. We critically evaluate the assumptions that guide fundamental and translational studies in this area. Finally, we suggest guidelines for future research and offer ways to overcome potential interpretational challenges to increase the utility of pattern separation as a construct that can further understanding of both memory processes and brain disease.

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Section: Hippocampal Pattern Separation and Episodic Memorymentioning

confidence: 99%

Section: Neuropsychiatric Diseasementioning

confidence: 99%

Section: Neuropsychiatric Diseasementioning

confidence: 99%

Section: Neuropsychiatric Diseasementioning

confidence: 99%

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Integrating new findings and examining clinical applications of pattern separation

2018

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“…Of these BPS lure-old discrimination formulas, one of the closest to our preferred measure of d a is a type of response-bias corrected proportion correct P r ¼ p("old"|old) 2 p("old"|lure) (e.g., in Leal et al 2014). Like SDT's d a and d ′ , and unlike the aforementioned BPS formulas, P r accounts for the relative overlap between lure and old memory strengths.…”

mentioning

confidence: 99%

A signal detection theory analysis of behavioral pattern separation paradigms

Loiotile

Courtney

2015

Learn. Mem.

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Behavioral pattern separation (BPS) paradigms ask participants to discriminate previously encoded (old) stimuli from highly similar (lure) and categorically distinct (novel) stimuli. The lure-old discrimination, thought to uniquely reflect pattern separation in the hippocampal formation, is typically pitted against the traditional novel-old discrimination. However, BPS paradigms have measured lure-old discrimination neither consistently across studies nor in such a way that allows for accurate comparison to novel-old discrimination. Therefore, we advocate for signal detection theory (SDT) as a unified framework. Moreover, we compare SDT with previously used measures of lure-old discrimination, indicating how other formulas' inaccuracies can lead to erroneous conclusions.Tasks measuring behavioral pattern separation (BPS) are distinguished from standard tests of memory recognition by the inclusion of stimuli that are highly similar to those previously encoded. Because each of these "lure" stimuli differs only slightly from its corresponding previously encoded "old" stimulus, successful discrimination of old from lure stimuli is thought to denote particularly detailed memory representations of the old stimuli. In contrast, it has been suggested that successful discrimination of old from "novel" stimuli (i.e., categorically new, as commonly used in tests of recognition) need not rely on detailed representations of the old stimuli, but rather can be achieved even if the old stimuli have only gist-based representations. Consistent with this distinction, several studies imply a dissociation between novelold and lure-old discrimination. For example, using the BPS paradigm, researchers have argued that only detail-based lure-old discrimination is impaired in healthy aging (Stark et al. 2013) and enhanced by post-study caffeine (Borota et al. 2014). Claims from a more recent study (Reagh and Yassa 2014) support an even stronger, double dissociation: repeated-encoding benefits gist-based, novel-old discrimination (a finding known even to Ebbinghaus (1885)), but surprisingly impairs detail-based, lureold discrimination. One major concern-particularly with findings such as these, where there appear to be differences between novel-old and lure-old discrimination-is that the measures used for lure-old discrimination vary from each other and from those used for novel-old discrimination. A unified measurement approach is needed if one is to reliably characterize lure-old discrimination as well as properly compare it to novel-old discrimination.Here, we propose the use of signal detection theory (SDT) (Green and Swets 1966) for measuring lure-old discrimination. We reran the aforementioned BPS paradigm (Reagh and Yassa 2014), which tested effects of repeated encoding on both detail and gist-based memory representations. We demonstrate not only that SDT is an appropriate framework for measuring lure-old discrimination but that SDT formulas yield opposite results to those reported: lure-old discrimination, like novel-old discrimin...

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Pattern separation of emotional information in hippocampal dentate and CA3

et al. 2014

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Emotional arousal, mediated by the amygdala, is known to modulate episodic memories stored by the hippocampus, a region involved in pattern separation (the process by which similar representations are independently stored). While emotional modulation and pattern separation have been examined independently, the current study attempts to link the two areas of research to propose an alternative account for how emotion modulates episodic memory. We utilized an emotional discrimination task designed to tax pattern separation of emotional information by concurrently varying valence and similarity of stimuli. To examine emotional modulation of memory at the level of hippocampal subfields, we used high-resolution fMRI (1.5 mm isotropic) of the medial temporal lobe. Consistent with prior reports, we observed engagement of the hippocampal dentate gyrus (DG) and CA3 during accurate discrimination of highly similar items (i.e. pattern separation). Furthermore, we observed an emotional modulation of this signal (negative > neutral) specific to trials on which participants accurately discriminated similar emotional items. The amygdala was also modulated by emotion, regardless of the accuracy of discrimination. Additionally, we found aberrant amygdala-hippocampal network activity in a sample of adults with depressive symptoms. In this sample, amygdala activation was enhanced and DG/CA3 activation was diminished during emotional discrimination compared to those without depressive symptoms. Depressive symptom severity was also negatively correlated with DG/CA3 activity. This study suggests a novel mechanistic account for how emotional information is processed by hippocampal subfields as well as how this network may be altered in mood disorders.

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Asymmetric effects of emotion on mnemonic interference

Cited by 81 publications

References 58 publications

Integrating new findings and examining clinical applications of pattern separation

Integrating new findings and examining clinical applications of pattern separation

A signal detection theory analysis of behavioral pattern separation paradigms

Pattern separation of emotional information in hippocampal dentate and CA3

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