Processing of Emotional Reactivity and Emotional Memory over Sleep

Baran, Bengi; Pace‐Schott, Edward F.; Ericson, Callie; Spencer, Rebecca M. C.

doi:10.1523/jneurosci.2532-11.2012

Cited by 218 publications

(225 citation statements)

References 46 publications

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“…Increased amygdala recruitment due to the consolidation of fear learning during sleep, as reported here, may favor the processing of the CS+ during the face discrimination task. These results add support to the notion that sleep may promote the consolidation of emotional memories (Baran et al, 2012;Hu et al, 2006;Menz et al, 2013;Payne and Kensinger, 2011;Sterpenich et al, 2007Sterpenich et al, , 2009Wagner et al, 2001). This hypothesis is also consistent with our finding of increased amygdala-FFA functional connectivity after sleep, selectively when CS+ face information is present.…”

Section: Discussionsupporting

confidence: 82%

“…For example, long-lasting improvement in perceptual learning tasks requires (rapid eye movement (REM) and non-rapid eye movement (NREM)) sleep and involves plasticity in early sensory cortices (Aeschbach et al, 2008;Gais et al, 2000;Schwartz et al, 2002;Stickgold et al, 2000;Yotsumoto et al, 2009). Similarly, emotional memories, fear conditioning, and extinction of a conditioned response are consolidated by a period of sleep following initial exposure (Baran et al, 2012;Payne and Kensinger, 2011;Sterpenich et al, 2007Sterpenich et al, , 2009, particularly REM sleep (Menz et al, 2013;Nishida et al, 2009;Pace-Schott et al, 2009;Wagner et al, 2001). However, it is unknown whether sleep contributes to the remodeling of sensory representations of emotionally-relevant stimuli in sensory cortices, enhancing their perceptual discriminability subsequent to emotional learning.…”

Section: Introductionmentioning

confidence: 99%

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Sleep sharpens sensory stimulus coding in human visual cortex after fear conditioning

et al. 2014

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Efficient perceptual identification of emotionally-relevant stimuli requires optimized neural coding. Because sleep contributes to neural plasticity mechanisms, we asked whether the perceptual representation of emotionally-relevant stimuli within sensory cortices is modified after a period of sleep. We show combined effects of sleep and aversive conditioning on subsequent discrimination of face identity information, with parallel plasticity in the amygdala and visual cortex. After one night of sleep (but neither immediately nor after an equal waking interval), a fear-conditioned face was better detected when morphed with another identity. This behavioral change was accompanied by increased selectivity of the amygdala and face-responsive fusiform regions. Overnight neural changes can thus sharpen the representation of threat-related stimuli in cortical sensory areas, in order to improve detection in impoverished or ambiguous situations. These findings reveal an important role of sleep in shaping cortical selectivity to emotionally-relevant cues and thus promoting adaptive responses to new dangers.

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Section: Discussionsupporting

confidence: 82%

Section: Introductionmentioning

confidence: 99%

Sleep sharpens sensory stimulus coding in human visual cortex after fear conditioning

et al. 2014

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“…[20][21][22] In a separate study, we found sleep-dependent memory consolidation may causally impact subsequent (ie, next-day) mood. Specifically, we found sleep staging predicts post-sleep affect/mood but only when sleep-dependent emotional memory consolidation occurred.…”

Section: Statement Of Significancementioning

confidence: 77%

Mild Traumatic Brain Injury Chronically Impairs Sleep- and Wake-Dependent Emotional Processing

Mantua¹,

Henry

Garskovas

et al. 2017

Sleep

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Study Objectives: A single traumatic brain injury (TBI), even when mild (ie, concussion), can cause lasting consequences. Individuals with a history of chronic (>1-year prior) mild TBI have an increased risk of mood disturbances (eg, depression, suicide). This population also has lingering sleep alterations, including poor sleep quality and changes in sleep stage proportions. Given these sleep deficits, we aimed to test whether sleep-dependent emotional memory consolidation is reduced in this population. We utilized a mild TBI group (3.7 ± 2.9 years post injury) and an uninjured (non-TBI) population. Methods: Participants viewed negative and neutral images both before and after a 12-hour period containing sleep ("Sleep" group) or an equivalent period of time spent awake ("Wake" group). Participants rated images for valence/arousal at both sessions, and memory recognition was tested at session two. Results: The TBI group had less rapid eye movement (REM), longer REM latency, and more sleep complaints. Sleep-dependent memory consolidation of nonemotional images was present in all participants. However, consolidation of negative images was only present in the non-TBI group. A lack of differentiation between the TBI Sleep and Wake groups was due to poor performance in the sleep group and, unexpectedly, enhanced performance in the wake group. Additionally, although the non-TBI participants habituated to negative images over a waking period, the TBI participants did not. Conclusions: We propose disrupted sleep-and wake-dependent emotional processing contributes to poor emotional outcomes following chronic, mild TBI. This work has broad implications, as roughly one-third of the US population will sustain a mild TBI during their lifetime.

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“…Sleep has been repeatedly shown to preferentially benefit emotional memories over neutral ones (Hu, Stylos-Allan, & Walker, 2006;Nishida, Pearsall, Buckner, & Walker, 2009;Payne & Kensinger, 2010;Wagner, Gais, & Born, 2001), although evidence of this effect is not conclusive (Baran, Pace-Schott, Ericson, & Spencer, 2012), as well as to selectively benefit the emotional components of a memory over the neutral contextual details (Cunningham et al, 2014;Payne, Chambers, & Kensinger, 2012;Payne et al, 2015;Payne et al, 2008). REM sleep, specifically oscillations in the theta frequency range, has been most often linked to emotional memory consolidation (Nishida et al, 2009).…”

Section: Sleep Tends To Preferentially Benefit Emotional Memoriesmentioning

confidence: 99%

The differential effects of emotional salience on direct associative and relational memory during a nap

Alger

Payne

2016

Cogn Affect Behav Neurosci

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Relational memories are formed from shared components between directly learned memory associations, flexibly linking learned information to better inform future judgments. Sleep has been found to facilitate both direct associative and relational memories. However, the impact of incorporating emotionally salient information into learned material and the interaction of emotional salience and sleep in facilitating both types of memory is unknown. Participants encoded two sets of picture pairs, with either emotionally negative or neutral objects paired with neutral faces. The same objects were present in both sets, paired with two different faces across the sets. Baseline memory for these directly paired associates was tested immediately after encoding, followed by either a 90-min nap opportunity or wakefulness. Five hours after learning, a surprise test assessed relational memory, the indirect association between two faces paired with the same object during encoding, followed by a retest of direct associative memory. Overall, negative information was remembered better than neutral for directly learned pairs. A nap facilitated both preservation of direct associative memories and formation of relational memories, compared to remaining awake. Interestingly, however, this sleep benefit was observed specifically for neutral directly paired associates, while both neutral and negative relational associations benefitted from a nap. Finally, REM sleep played opposing roles in neutral direct and relational associative memory formation, with more REM sleep leading to forgetting of direct associations but promoting relational associations, suggesting that, while not benefitting memory consolidation for directly learned details, REM sleep may foster the memory reorganization needed for relational memory.Keywords Emotion . Associative memory . Naps . Sleep . Inference . Relational memory In our encounters with the everyday stream of information, we do not encode and store all individual experiences in a veridical fashion. Rather, new information is integrated with old, and overlapping details are consolidated into schemata, or networks linked by common features of related memories, to flexibly form novel relationships (Eichenbaum, 2004;Eichenbaum & Cohen, 2001). We use these new representations derived from related memories to adaptively make inferential judgments about future experiences. However, our everyday experiences are not devoid of emotion. Emotional salience, defined by the valence (negative to positive) and arousal (calming to arousing) of an experience, is a biologically adaptive cue that can influence how an event is remembered and possibly how it is integrated in memory. In addition to the influence of emotion, sleep during the consolidation and integration period of a new memory may impact its fate. This experiment investigates the separate and interacting contributions of emotional salience and sleep to the consolidation of direct associative and relational memories, the indirect associations between two...

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Processing of Emotional Reactivity and Emotional Memory over Sleep

Cited by 218 publications

References 46 publications

Sleep sharpens sensory stimulus coding in human visual cortex after fear conditioning

Sleep sharpens sensory stimulus coding in human visual cortex after fear conditioning

Mild Traumatic Brain Injury Chronically Impairs Sleep- and Wake-Dependent Emotional Processing

The differential effects of emotional salience on direct associative and relational memory during a nap

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