Targeted Reactivation during Sleep Differentially Affects Negative Memories in Socially Anxious and Healthy Children and Adolescents

J Neurosci. 2017 Mar 1;37(9):2425-2434. doi: 10.1523/JNEUROSCI.1912-16.2017. Epub 2017 Jan 31.

Abstract

Cognitive models propose a negative memory bias as one key factor contributing to the emergence and maintenance of social anxiety disorder (SAD). The long-term consolidation of memories relies on memory reactivations during sleep. We investigated in SAD patients and healthy controls the role of memory reactivations during sleep in the long-term consolidation of positive and negative information. Socially anxious and healthy children and adolescents learnt associations between pictures showing ambiguous situations and positive or negative words defining the situations' outcome. Half of the words were re-presented during postlearning sleep (i.e., they were cued). Recall of picture-word associations and subjective ratings of pleasantness and arousal in response to the pictures was tested for cued and uncued stimuli. In the morning after cueing, cueing facilitated retention of positive and negative memories equally well in SAD patients and healthy controls. One week later, cueing led to reduced ratings of pleasantness of negative information in SAD but not in healthy controls. Coincidental to these findings was more pronounced EEG theta activity over frontal, temporal and parietal regions in response to negative stimuli in SAD patients. Our findings suggest that the preferential abstraction of negative emotional information during sleep might represent one factor underlying the negative memory bias in SAD.SIGNIFICANCE STATEMENT We aim to uncover mechanisms underlying the characteristic negative memory bias in social anxiety disorder (SAD). The formation of long-lasting memories-a process referred to as memory consolidation-depends on the reactivation of newly acquired memories during sleep. We demonstrated that experimentally induced memory reactivation during sleep renders long-term memories of negative experiences more negative in SAD patients but not in healthy controls. We also found in SAD patients that the reactivation of negative experiences coincided with more pronounced oscillatory theta activity. These results provide first evidence that memory reactivation during sleep might contribute to the negative memory bias in SAD.

Keywords: consolidation; memory; reactivation; sleep; social anxiety.

MeSH terms

  • Adolescent
  • Affect / physiology*
  • Arousal
  • Association Learning / physiology*
  • Brain Mapping
  • Case-Control Studies
  • Child
  • Cues
  • Evoked Potentials
  • Female
  • Humans
  • Male
  • Memory Disorders / etiology*
  • Memory, Long-Term
  • Neuropsychological Tests
  • Phobia, Social / complications*
  • Photic Stimulation
  • Psychiatric Status Rating Scales
  • Retention, Psychology
  • Sleep / physiology*
  • Time Factors