Elsevier

Biological Psychiatry

Volume 60, Issue 12, 15 December 2006, Pages 1324-1330
Biological Psychiatry

Original article
Impaired Declarative Memory Consolidation During Sleep in Patients With Primary Insomnia: Influence of Sleep Architecture and Nocturnal Cortisol Release

https://doi.org/10.1016/j.biopsych.2006.03.051Get rights and content

Background

A central cognitive function of sleep is to consolidate newly acquired memories for long-term storage. Here, we investigated whether the overnight consolidation of declarative memory in patients with chronic sleep disturbances is impaired, owing to less slow wave sleep (SWS) and an increased cortisol release.

Methods

Polysomnographic recordings, serum cortisol concentrations, and overnight memory consolidation in 16 patients with primary insomnia were compared with those of 13 healthy control subjects.

Results

Patients displayed distinctly less overnight consolidation of declarative memory (p < .05), which was significantly correlated with SWS in the control subjects (r = .69) but with rapid eye movement (REM) sleep in the patients (r = .56), who had a diminished amount of SWS (p < .05). Increased cortisol levels in the middle of the night were associated with impaired retrieval of declarative memory after sleep for both control subjects (r = −.52) and patients (r = −.46).

Conclusions

Primary insomnia is associated with a diminished sleep-related consolidation of declarative memory. Efficient overnight consolidation of declarative memory is associated with high amounts of SWS and low serum cortisol levels during the early part of the night. Where SWS is decreased, REM sleep might play a partly compensatory role in the consolidation of declarative memory.

Section snippets

Subjects

Sixteen patients with primary insomnia (8 men) and 13 age-matched healthy control subjects (5 men) participated in the study. Patients were consecutively recruited from the Outpatient Sleep Disorders Clinic of the University of Luebeck, and control subjects were recruited by advertisement. All patients who met the criteria for primary insomnia according to the DSM-IV were asked to participate in the study. The DSM-IV criteria for primary insomnia are sleep disturbances that cause patients to

Subjects

There were no statistical differences between patients and control subjects in age (patients: 41.6 ± 1.2 years; control subjects: 40.1 ± 11.3 years; [t(27) = −.36, p = .73]), body mass index (patients: 23.1 ± 2.4; control subjects: 23.6 ± 3.5, [t(27) = .49, p = .63]), and years of education (patients: 14.4 ± 2.7; control subjects: 14.9 ± 3.6; [t(27) = .59, p = .69]). Mean duration of insomnia among patients was 9.2 ± 8.1 years.

Memory Tasks

Groups did not perform differently on the word-pair associates task

Discussion

This study investigated the overnight sleep-dependent consolidation of both declarative and non-declarative memory in patients with primary insomnia. The results indicate a deficit of hippocampus-dependent declarative memory consolidation in these patients as opposed to healthy sleepers. Whereas in the healthy subjects declarative memory consolidation was positively correlated with SWS, the insomnia patients with a significantly lower amount of SWS showed no such association. By contrast, there

References (50)

  • A. Rodenbeck et al.

    Interactions between evening and nocturnal cortisol secretion and sleep parameters in patients with severe chronic primary insomnia

    Neurosci Lett

    (2002)
  • C. Smith

    Sleep states and memory processes in humans: Procedural versus declarative memory systems

    Sleep Med Rev

    (2001)
  • M.P. Walker et al.

    Practice with sleep makes perfect: Sleep-dependent motor skill learning

    Neuron

    (2002)
  • M.P. Walker et al.

    Sleep-dependent learning and memory consolidation

    Neuron

    (2004)
  • M.P. Walker et al.

    Sleep-dependent motor memory plasticity in the human brain

    Neuroscience

    (2005)
  • Diagnostic and Statistical Manual of Mental Disorders (DSM-IV)

    (1994)
  • J. Backhaus et al.

    Long-term effectiveness of a short-term cognitive-behavioral group treatment for primary insomnia

    Eur Arch Psychiatry Clin Neurosci

    (2001)
  • J. Backhaus et al.

    Short-term training increases diagnostic and treatment rate for insomnia in general practice

    Eur Arch Psychiatry Clin Neurosci

    (2002)
  • R.M. Benca et al.

    Sleep and psychiatric disordersA meta-analysis

    Arch Gen Psychiatry

    (1992)
  • D.J. de Quervain et al.

    Acute cortisone administration impairs retrieval of long-term declarative memory in humans

    Nat Neurosci

    (2000)
  • S. Fischer et al.

    Sleep forms memory for finger skills

    Proc Natl Acad Sci U S A

    (2002)
  • S. Gais et al.

    Declarative memory consolidation: mechanisms acting during human sleep

    Learn Mem

    (2004)
  • S. Gais et al.

    Low acetylcholine during slow-wave sleep is critical for declarative memory consolidation

    Proc Natl Acad Sci USA

    (2004)
  • S. Gais et al.

    Learning-dependent increases in sleep spindle density

    J Neurosci

    (2002)
  • R. Huber et al.

    Local sleep and learning

    Nature

    (2004)
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