title: Fear conditioning, safety learning, and sleep in humans.
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.
authors.affiliation: Research and.
authors.forename: Anisa J
authors.initials: AJ
authors.lastname: Marshall
authors.affiliation: Research and Veterans Affairs San Diego Center for Excellence in Stress and Mental Health, San Diego, California 92161, Department of Psychiatry, University of California San Diego, San Diego, California 92093-0603, and.
authors.forename: Dean T
authors.initials: DT
authors.lastname: Acheson
authors.affiliation: Research and Veterans Affairs San Diego Center for Excellence in Stress and Mental Health, San Diego, California 92161, Department of Psychiatry, University of California San Diego, San Diego, California 92093-0603, and.
authors.forename: Victoria B
authors.initials: VB
authors.lastname: Risbrough
authors.affiliation: Research and SDSU-UCSD Joint Doctoral Program in Clinical Psychology; San Diego, California 92120.
authors.forename: Laura D
authors.initials: LD
authors.lastname: Straus
authors.affiliation: Psychology Services, Veterans Affairs San Diego Healthcare System, San Diego, California 92161, Veterans Affairs San Diego Center for Excellence in Stress and Mental Health, San Diego, California 92161, Department of Psychiatry, University of California San Diego, San Diego, California 92093-0603, and SDSU-UCSD Joint Doctoral Program in Clinical Psychology; San Diego, California 92120 drummond@ucsd.edu.
authors.forename: Sean P A
authors.initials: SP
authors.lastname: Drummond
mesh_terms: D000328:Adult; D003214:Conditioning, Classical / Q000502:physiology*; D005239:Fear / Q000502:physiology*; D005260:Female; D006801:Humans; D007858:Learning / Q000502:physiology*; D008297:Male; D012895:Sleep, REM / Q000502:physiology*; D013313:Stress Disorders, Post-Traumatic / Q000150:complications / Q000503:physiopathology*; D055815:Young Adult
keywords: REM sleep; fear conditioning; safety learning; translational