Sleep Promotes Consolidation of Emotional Memory in Healthy Children but Not in Children with Attention-Deficit Hyperactivity Disorder

Alexander Prehn-Kristensen,Manuel Munz,Ina Molzow,Lioba Baving,Ines Wilhelm,Christian D Wiesner,Hengyi Rao

doi:10.1371/journal.pone.0065098

Alexander Prehn-Kristensen, Manuel Munz + Show 5 more

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https://doi.org/10.1371/journal.pone.0065098

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Abstract

Fronto-limbic brain activity during sleep is believed to support the consolidation of emotional memories in healthy adults. Attention deficit-hyperactivity disorder (ADHD) is accompanied by emotional deficits coincidently caused by dysfunctional interplay of fronto-limbic circuits. This study aimed to examine the role of sleep in the consolidation of emotional memory in ADHD in the context of healthy development. 16 children with ADHD, 16 healthy children, and 20 healthy adults participated in this study. Participants completed an emotional picture recognition paradigm in sleep and wake control conditions. Each condition had an immediate (baseline) and delayed (target) retrieval session. The emotional memory bias was baseline–corrected, and groups were compared in terms of sleep-dependent memory consolidation (sleep vs. wake). We observed an increased sleep-dependent emotional memory bias in healthy children compared to children with ADHD and healthy adults. Frontal oscillatory EEG activity (slow oscillations, theta) during sleep correlated negatively with emotional memory performance in children with ADHD. When combining data of healthy children and adults, correlation coefficients were positive and differed from those in children with ADHD. Since children displayed a higher frontal EEG activity than adults these data indicate a decline in sleep-related consolidation of emotional memory in healthy development. In addition, it is suggested that deficits in sleep-related selection between emotional and non-emotional memories in ADHD exacerbate emotional problems during daytime as they are often reported in ADHD.

Highlights

Attention deficit hyperactivity disorder (ADHD) is one of the most frequently diagnosed psychiatric disorders in children and adolescents
While several studies reported a benefit from sleep with respect to emotional memory in healthy individuals [17,18,19,25,57,58,59], our results showed for the first time that healthy children outperform healthy adults
As memory performance was baseline-corrected, the results revealed that the healthy children displayed a diminished emotional memory bias only in the wake but not in the sleep condition

Summary

Introduction

Attention deficit hyperactivity disorder (ADHD) is one of the most frequently diagnosed psychiatric disorders in children and adolescents. ADHD is characterized by symptoms of inattention, hyperactivity, and/or impulsiveness [1] and it is often accompanied by emotional problems [2,3,4]. Imaging studies in ADHD revealed alterations in the structure and function of the prefrontal cortex, and in the amygdala and the hippocampus [5,6,7,8] which are both critically involved in emotional processes [9,10,11]. The affected interplay between these regions is assumed to cause emotional problems in ADHD during daytime [12]. Better performance in emotional memory is coincided by an integration of PFC, amygdala, and the hippocampus during sleep [20]. Sleep electro-encephalogram (EEG) studies revealed that hippocampus-related memory consolidation is supported by slow frontal oscillation activity (,1Hz) during slow wave sleep (SWS) [21,22], while amygdala-associated memory consolidation is supported by frontal theta oscillations during REM sleep [23,24,25]

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