Psychophysiological arousal at encoding leads to reduced reactivity but enhanced emotional memory following sleep

Cunningham, Tony J.; Crowell, Charles R.; Alger, Sara E.; Kensinger, Elizabeth A.; Villano, Michael; Mattingly, Stephen M.; Payne, Jessica D.

doi:10.1016/j.nlm.2014.06.002

Cited by 77 publications

(78 citation statements)

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“…In these experiments, emotional objects are better remembered than neutral objects, but at the expense of memory for neutral information in the background, and sleep magnifies this trade-off effect, boosting memory specifically for the emotional images. Furthermore, there is evidence that shows that emotionally salient information that is attended to and results in an arousal response is marked for preferential consolidation during sleep, also resulting in stronger activation in the hippocampus and amygdala (Bennion et al, 2015;Cunningham et al, 2014). Thus, in this study we considered that the emotional item of a pair might draw focus away from the neutral item, thereby impeding the ability to pair them together.…”

Section: Discussionmentioning

confidence: 99%

“…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%

“…In our study, we anticipated that sleep would facilitate the consolidation of the negative paired associates and the formation of negative relational memories over neutral pairs. We hypothesized that the emotional response to the negative pairs may Btag^those integrated associations for preferential processing during sleep (see Bennion, Mickley Steinmetz, Kensinger, & Payne, 2015;Cunningham et al, 2014).…”

Section: Sleep Tends To Preferentially Benefit Emotional Memoriesmentioning

confidence: 99%

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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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Section: Discussionmentioning

confidence: 99%

Section: Sleep Tends To Preferentially Benefit Emotional Memoriesmentioning

confidence: 99%

Section: Sleep Tends To Preferentially Benefit Emotional Memoriesmentioning

confidence: 99%

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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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“…In elucidating the conditions under which these tagging benefits may occur, it should be noted that previous studies have included adult participants who either had an adequate amount of overnight sleep (Bennion et al ., 2014, 2015a; Cunningham et al ., 2014) or a daytime nap (Bennion et al ., 2016; Oudiette et al ., 2013) during the consolidation interval. Partial or total sleep deprivation may attenuate these tagging benefits.…”

Section: Introductionmentioning

confidence: 99%

Sleep restriction can attenuate prioritization benefits on declarative memory consolidation

Bennion

Chee

2016

Journal of Sleep Research

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SummaryAs chronic sleep restriction is a widespread problem among adolescents, the present study investigated the effects of a 1‐week sleep restriction (SR) versus control period on the consolidation of long‐term memory for prose passages. We also determined whether the benefit of prioritization on memory is modulated by adequate sleep occurring during consolidation. Fifty‐six healthy adolescents (25 male, aged 15–19 years) were instructed to remember a prose passage in which half of the content was highlighted (prioritized), and were told that they would receive an additional bonus for remembering highlighted content. Following an initial free recall test, participants underwent a 7‐night period in which they received either a 5‐h (SR) or 9‐h (control) nightly sleep opportunity, monitored by polysomnography on selected nights. Free recall of the passage was tested at the end of the sleep manipulation period (1 week after encoding), and again 6 weeks after encoding. Recall of highlighted content was superior to that of non‐highlighted content at all three time‐points (initial, 1 week, 6 weeks). This beneficial effect of prioritization on memory was stronger 1 week relative to a few minutes after encoding for the control, but not the SR group. N3 duration was similar in the control and SR groups. Overall, the present study shows that the benefits of prioritization on memory are enhanced over time, requiring time and sleep to unfold fully. Partial sleep deprivation (i.e. 5‐h nocturnal sleep opportunity) may attenuate such benefits, but this may be offset by preservation of N3 sleep duration.

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“…Sleep is known to specifically promote consolidation of emotionally salient memories (for reviews, see Goldstein & Walker, 2014;Payne & Kensinger, 2010 Kensinger (2008), sleep modifies emotional memories by enhancing the negative aspects of the scene (e.g., a damaged car) at the expense of its neutral aspects (e.g., pedestrians on the pavement; see also Cunningham et al, 2014;Payne, Chambers, & Kensinger, 2012;Payne et al, 2015). In view of this overnight memory trade-off, a straightforward prediction is that negative memories should be even more negative once sleep has occurred.…”

Section: Introductionmentioning

confidence: 99%

Setting the alarm: Word emotional attributes require consolidation to be operational.

Dumay¹,

Sharma²,

Kellen³

et al. 2018

Emotion

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Demonstrations of emotional Stroop in conditioned made-up words are flawed due to the lack of task ensuring similar word encoding across conditions. Here, participants were trained on associations between made-up words (e.g., 'drott') and pictures with an alarming or neutral content (e.g., 'a dead sheep' versus 'a munching cow') in a situation that required attention to both ends of each association.To test whether word emotional attributes need to consolidate before they can hijack attention, one set of associations was learnt seven days before the test, whereas the other set was learnt either six hours or immediately before the test. The novel words' ability to evoke their emotional attributes was assessed using both Stroop and an auditory analogue called pause detection. Matching words and pictures was harder for alarming associations. However, similar learning rate and forgetting at seven days were observed for both types of associations. Pause detection revealed no emotion effect for same-day (i.e., unconsolidated) associations, but robust interference for seven-day-old (i.e., consolidated) alarming associations. Attention capture was found in the emotional Stroop as well, though only when trial n-1 referred to a same-day association. This task also showed stronger response repetition priming (independently of emotion) when trials n and n-1 both tapped into sevenday-old associations. Word emotional attributes hence take between six hours and seven days to be operational. Moreover, age interactions between consecutive trials can be used to gauge implicitly the indirect (relational) episodic associations that develop in the meantime between the memories of individual items.

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Psychophysiological arousal at encoding leads to reduced reactivity but enhanced emotional memory following sleep

Cited by 77 publications

References 46 publications

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

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

Sleep restriction can attenuate prioritization benefits on declarative memory consolidation

Setting the alarm: Word emotional attributes require consolidation to be operational.

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