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Articles, Behavioral/Cognitive

Fear Conditioning, Safety Learning, and Sleep in Humans

Anisa J. Marshall, Dean T. Acheson, Victoria B. Risbrough, Laura D. Straus and Sean P.A. Drummond
Journal of Neuroscience 27 August 2014, 34 (35) 11754-11760; DOI: https://doi.org/10.1523/JNEUROSCI.0478-14.2014
Anisa J. Marshall
1Research and
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Dean T. Acheson
1Research and
3Veterans Affairs San Diego Center for Excellence in Stress and Mental Health, San Diego, California 92161,
4Department of Psychiatry, University of California San Diego, San Diego, California 92093-0603, and
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Victoria B. Risbrough
1Research and
3Veterans Affairs San Diego Center for Excellence in Stress and Mental Health, San Diego, California 92161,
4Department of Psychiatry, University of California San Diego, San Diego, California 92093-0603, and
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Laura D. Straus
1Research and
5SDSU-UCSD Joint Doctoral Program in Clinical Psychology; San Diego, California 92120
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Sean P.A. Drummond
2Psychology Services, Veterans Affairs San Diego Healthcare System, San Diego, California 92161,
3Veterans Affairs San Diego Center for Excellence in Stress and Mental Health, San Diego, California 92161,
4Department of Psychiatry, University of California San Diego, San Diego, California 92093-0603, and
5SDSU-UCSD Joint Doctoral Program in Clinical Psychology; San Diego, California 92120
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Abstract

Fear conditioning is considered an animal model of post-traumatic stress disorder. Such models have shown fear conditioning disrupts subsequent rapid eye movement sleep (REM). Here, we provide a translation of these models into humans. Using the fear potentiated startle (FPS) procedure, we examined the effects of fear conditioning and safety signal learning on subsequent REM sleep in healthy adults. We also examined the effects of changes in REM sleep on retention of fear and safety learning. Participants (n = 42 normal controls) spent 3 consecutive nights in the laboratory. The first was an adaptation night. Following the second night, we administered a FPS procedure that included pairing a wrist shock with a threat signal and a safety signal never paired with a shock. The next day, we administered the FPS procedure again, with no wrist shocks to any stimulus, to measure retention of fear and safety. Canonical correlations assessed the relationship between FPS response and REM sleep. Results demonstrated that increased safety signal learning during the initial acquisition phase was associated with increased REM sleep consolidation that night, with 28.4% of the variance in increased REM sleep consolidation from baseline accounted for by safety signal learning. Overnight REM sleep was, in turn, related to overnight retention of fear and safety learning, with 22.5% of the variance in startle retention accounted for by REM sleep. These data suggest that sleep difficulties, specifically REM sleep fragmentation, may play a mechanistic role in post-traumatic stress disorder via an influence on safety signal learning and/or threat-safety discrimination.

  • fear conditioning
  • REM sleep
  • safety learning
  • translational
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The Journal of Neuroscience: 34 (35)
Journal of Neuroscience
Vol. 34, Issue 35
27 Aug 2014
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Fear Conditioning, Safety Learning, and Sleep in Humans
Anisa J. Marshall, Dean T. Acheson, Victoria B. Risbrough, Laura D. Straus, Sean P.A. Drummond
Journal of Neuroscience 27 August 2014, 34 (35) 11754-11760; DOI: 10.1523/JNEUROSCI.0478-14.2014

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Fear Conditioning, Safety Learning, and Sleep in Humans
Anisa J. Marshall, Dean T. Acheson, Victoria B. Risbrough, Laura D. Straus, Sean P.A. Drummond
Journal of Neuroscience 27 August 2014, 34 (35) 11754-11760; DOI: 10.1523/JNEUROSCI.0478-14.2014
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Keywords

  • fear conditioning
  • REM sleep
  • safety learning
  • translational

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