Emotional memory processing is influenced by sleep quality

Highlights

• Low sleep quality and lack of sleep both negatively affect emotional valence of memories.

• The affective tone of the emotional memory is preserved after a good sleep.

• Sleep deprivation leads to a decreased accuracy of emotional memory recognition.

• The poor sleepers and the good sleepers have preserved sleep-dependent consolidation of emotional information.

Abstract

Objective

The recall of emotional memory is enhanced after sleep and is hindered by sleep deprivation. We used an emotional memory task to assess whether poor sleep quality, as well as sleep deprivation, may influence the accuracy of memory recognition, but also the affective tone associated with the memory.

Methods

Seventy-five subjects, divided into poor sleeper (PS), good sleeper (GS), and sleep deprivation (SD) groups, completed two recall (R) sessions: R1, 1 h after the encoding phase; and R2, after one night of sleep for PS and GS groups and after one night of sleep deprivation for the SD group. During the encoding phase, the participants rated valence and arousal of 90 pictures. During R1 and R2, the participants first made a yes/no memory judgment of the 45 target pictures intermingled with 30 non-target pictures, then rated valence and arousal of each picture.

Results

Recognition accuracy was higher for the PS and GS groups compared to the SD group for all pictures. Emotional valence of the remembered pictures was more negative after sleep deprivation and poor quality sleep, while it was preserved after a good sleep.

Conclusions

These results provide the first evidence that poor sleep quality negatively affects emotional valence of memories, within the context of preserved emotional memory consolidation. It is suggested that low sleep quality and lack of sleep may impose a more negative affective tone to memories. The reported effects are not to be ascribed to depressive mood, but to a specific influence of poor sleep quality.

Introduction

It is well known that emotional experiences have a privileged status in the memory for their affective resonance that contributes to boosting their long-term recall [1], [2]. The neuroanatomical explanation for this emotional memory enhancement effect is that emotional arousal activates the amygdala, which in turn influences other brain regions that are important for memory storage [3], [4]. In fact, the amygdala has reciprocal connections with the hippocampus and prefrontal cortex, and modulates the activity in the hippocampus–neocortical circuit during learning and memory consolidation [5].

In the last few years, it has been shown that sleep deprivation negatively influences the functionality of the above-mentioned brain circuits that are related to emotional memory. In particular, a reduced recall of emotional pictures in sleep-deprived subjects has been associated with a lack of reduction in amygdala reactivity when they were re-exposed to these same emotional stimuli at a recognition test administered 72 h [6] or six months after encoding [7]. Along the same line, Yoo et al., investigating the impact of 35 h of sleep deprivation on emotional reactivity, showed a greater activation of the amygdala and a reduced connectivity between the amygdala and the medial prefrontal cortex in response to negative images in sleep-deprived subjects, compared to the rested control group [8]. Therefore, lack of sleep affects the regulation of the cortico-limbic emotion circuits, negatively influences emotional memory consolidation and increases emotional reactivity.

According to the “sleep to forget and sleep to remember” hypothesis [9], those who do not benefit from sleep after learning are not able to decouple memories from their “affective blanket” during the post-learning period. Thus, the magnitude of the affective “charge” remaining within memory networks persists for a longer time, potentially resulting in a condition of chronic anxiety [10]. If this theory is correct, people with a poor sleep quality – similar to sleep-deprived subjects – should show an emotional memory consolidation impairment and an increase of the affective tone associated with the emotionally loaded stimuli or events.

To date, several studies have investigated the influence of sleep and sleep deprivation on emotional memory consolidation. The findings are generally consistent in indicating that sleep supports emotional memory consolidation [2], [11], [12], [13], [14], [15], [16], while sleep deprivation negatively affects it [2], [6], [7], [17], [18], [19], [20], [21].

However, it is believed that no study has yet examined the relationship between poor sleep quality and emotional memory in humans. The issue is of intrinsic clinical interest because there is growing evidence that sleep disturbances may constitute a risk factor in the development of post-traumatic stress disorder (PTSD) [22] and depression [23], [24] by compromising sleep-dependent affective memory processing.

The Walker and van der Helm model holds that these psychiatric disorders may be caused and maintained by a poor sleep quality, which impairs the ability to form and retain memories of positive (and neutral) affective valence but leaves the long-term formation and the affective tone of negative experiences preserved [9].

Therefore, investigating the existence of a direct relationship between poor sleep quality and deficits in emotional memory processing may be important to prevent the development of psychiatric disturbances such as PTSD.

The main aim of the present study was to test the hypothesis that poor sleep quality, like sleep deprivation, is associated with a lower recall of emotional stimuli. Furthermore, the study assessed whether poor sleep quality and sleep deprivation may influence not only the accuracy of memory recognition (hippocampal activity-dependent) but also the affective tone associated with the memory (limbic activity-dependent). To this aim, a sample of subjects with poor sleep quality was compared with a sleep-deprived group and with a normally sleeping control group. A differential (d′) was considered as an index of performance accuracy (ie, a measure of accurate remembering) that should depend directly on the activity of the hippocampus, assuming that this index is a specific measure of declarative memory. On the other hand, both the valence and the arousal ratings were used as measures of the affective tone of a stimulus because it is known that they both depend on the limbic area activity [25], [26].

In keeping with the “sleep to forget and sleep to remember” hypothesis, the sleep-deprived group and, in a more attenuated form, the poor-sleep-quality group should show a lack of sleep-dependent modulation of the emotional memory, characterized by a decreased consolidation of the perceptual memory content and a failure in the reduction of its affective tone.