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Repeated exposure to conditioned fear stress increases anxiety and delays sleep recovery following exposure to an acute traumatic stressor.

Greenwood BN, Thompson RS, Opp MR, Fleshner M - Front Psychiatry (2014)

Bottom Line: The potentiation of anxiety produced by prior repeated fear was temporary; exaggerated fear was present 1 day but not 4 days following acute stress.This initial reduction in sleep was followed by robust REM rebound and diurnal rhythm flattening of sleep/wake behavior.These data suggest that impaired recovery of sleep/wake behavior following acute stress could contribute to the mechanisms by which a history of prior repeated stress increases vulnerability to subsequent novel stressors and stress-related disorders.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Colorado Denver , Denver, CO , USA.

ABSTRACT
Repeated stressor exposure can sensitize physiological responses to novel stressors and facilitate the development of stress-related psychiatric disorders including anxiety. Disruptions in diurnal rhythms of sleep-wake behavior accompany stress-related psychiatric disorders and could contribute to their development. Complex stressors that include fear-eliciting stimuli can be a component of repeated stress experienced by human beings, but whether exposure to repeated fear can prime the development of anxiety and sleep disturbances is unknown. In the current study, adult male F344 rats were exposed to either control conditions or repeated contextual fear conditioning for 22 days followed by exposure to no, mild (10), or severe (100) acute uncontrollable tail shock stress. Exposure to acute stress produced anxiety-like behavior as measured by a reduction in juvenile social exploration and exaggerated shock-elicited freezing in a novel context. Prior exposure to repeated fear enhanced anxiety-like behavior as measured by shock-elicited freezing, but did not alter social exploratory behavior. The potentiation of anxiety produced by prior repeated fear was temporary; exaggerated fear was present 1 day but not 4 days following acute stress. Interestingly, exposure to acute stress reduced rapid eye movement (REM) and non-REM (NREM) sleep during the hours immediately following acute stress. This initial reduction in sleep was followed by robust REM rebound and diurnal rhythm flattening of sleep/wake behavior. Prior repeated fear extended the acute stress-induced REM and NREM sleep loss, impaired REM rebound, and prolonged the flattening of the diurnal rhythm of NREM sleep following acute stressor exposure. These data suggest that impaired recovery of sleep/wake behavior following acute stress could contribute to the mechanisms by which a history of prior repeated stress increases vulnerability to subsequent novel stressors and stress-related disorders.

No MeSH data available.


Related in: MedlinePlus

Effects of repeated fear and acute stress on diurnal difference of sleep/wake behavior. Following 22 days of no repeated fear (home cage) or repeated fear stress (repeated fear), rats were exposed to no acute stress (0), mild (10 uncontrollable tail shocks; 10), or severe (100 uncontrollable tails shocks; 100) acute stress. Diurnal difference of % rapid eye movement [REM; (A,B)] sleep, non-rapid eye movement [NREM; (C,D)] sleep, and wake (E,F) were calculated by subtracting light cycle values from dark cycle values of sleep parameters measured in the home cage for 48 h starting the dark (active) cycle immediately following acute stressor exposure. The diurnal differences calculated from the first 24 h period starting the first active (dark) cycle immediately following acute stress are shown in the left panel (A,C,E). The diurnal differences calculated from the second 24 h period following acute stress are shown in the right panel (B,D,F). *p < 0.05 relative to respective 0 groups (lines represent main effects of acute stress); ϕp < 0.05 relative to all other groups.
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Figure 7: Effects of repeated fear and acute stress on diurnal difference of sleep/wake behavior. Following 22 days of no repeated fear (home cage) or repeated fear stress (repeated fear), rats were exposed to no acute stress (0), mild (10 uncontrollable tail shocks; 10), or severe (100 uncontrollable tails shocks; 100) acute stress. Diurnal difference of % rapid eye movement [REM; (A,B)] sleep, non-rapid eye movement [NREM; (C,D)] sleep, and wake (E,F) were calculated by subtracting light cycle values from dark cycle values of sleep parameters measured in the home cage for 48 h starting the dark (active) cycle immediately following acute stressor exposure. The diurnal differences calculated from the first 24 h period starting the first active (dark) cycle immediately following acute stress are shown in the left panel (A,C,E). The diurnal differences calculated from the second 24 h period following acute stress are shown in the right panel (B,D,F). *p < 0.05 relative to respective 0 groups (lines represent main effects of acute stress); ϕp < 0.05 relative to all other groups.

Mentions: To determine the impact of repeated fear and acute uncontrollable stress on the diurnal rhythms of sleep/wake behavior, the diurnal difference (dark–light) of % REM, % NREM, and % wake were compared between groups following acute stressor exposure. Consistent with greater REM rebound in the light cycle observed in the home cage rats following acute stress (Figure 6A), both repeated fear [F(1, 30) = 5.67; p = 0.02] and acute stress [F(2, 30) = 10.37; p = 0.0004] reduced the diurnal difference of % REM (Figure 7A). The flattening of the diurnal rhythm of % REM sleep was present during the first, but was gone by the second (Figure 7B), 24 h period following acute stress. Acute stress reduced the diurnal difference of % NREM sleep [F(2, 30) = 14.3; p < 0.0001; Figure 7C] and % wake [F(2, 30) = 18.77; p < 0.0001; Figure 7E] during the first 24 h period following acute stress in both home cage and repeated fear-exposed rats. During the second 24 h period following acute stress, significant interactions between repeated fear and acute stress revealed that the flattening of the diurnal rhythm of both % NREM sleep [F(2, 30) = 4.88; p = 0.01; Figure 7D] and % wake [F(2,30) = 5.44; p = 0.009; Figure 7F] persisted longer following acute stress in rats previously exposed to repeated fear. See Figure 7 for results of post hoc tests.


Repeated exposure to conditioned fear stress increases anxiety and delays sleep recovery following exposure to an acute traumatic stressor.

Greenwood BN, Thompson RS, Opp MR, Fleshner M - Front Psychiatry (2014)

Effects of repeated fear and acute stress on diurnal difference of sleep/wake behavior. Following 22 days of no repeated fear (home cage) or repeated fear stress (repeated fear), rats were exposed to no acute stress (0), mild (10 uncontrollable tail shocks; 10), or severe (100 uncontrollable tails shocks; 100) acute stress. Diurnal difference of % rapid eye movement [REM; (A,B)] sleep, non-rapid eye movement [NREM; (C,D)] sleep, and wake (E,F) were calculated by subtracting light cycle values from dark cycle values of sleep parameters measured in the home cage for 48 h starting the dark (active) cycle immediately following acute stressor exposure. The diurnal differences calculated from the first 24 h period starting the first active (dark) cycle immediately following acute stress are shown in the left panel (A,C,E). The diurnal differences calculated from the second 24 h period following acute stress are shown in the right panel (B,D,F). *p < 0.05 relative to respective 0 groups (lines represent main effects of acute stress); ϕp < 0.05 relative to all other groups.
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Figure 7: Effects of repeated fear and acute stress on diurnal difference of sleep/wake behavior. Following 22 days of no repeated fear (home cage) or repeated fear stress (repeated fear), rats were exposed to no acute stress (0), mild (10 uncontrollable tail shocks; 10), or severe (100 uncontrollable tails shocks; 100) acute stress. Diurnal difference of % rapid eye movement [REM; (A,B)] sleep, non-rapid eye movement [NREM; (C,D)] sleep, and wake (E,F) were calculated by subtracting light cycle values from dark cycle values of sleep parameters measured in the home cage for 48 h starting the dark (active) cycle immediately following acute stressor exposure. The diurnal differences calculated from the first 24 h period starting the first active (dark) cycle immediately following acute stress are shown in the left panel (A,C,E). The diurnal differences calculated from the second 24 h period following acute stress are shown in the right panel (B,D,F). *p < 0.05 relative to respective 0 groups (lines represent main effects of acute stress); ϕp < 0.05 relative to all other groups.
Mentions: To determine the impact of repeated fear and acute uncontrollable stress on the diurnal rhythms of sleep/wake behavior, the diurnal difference (dark–light) of % REM, % NREM, and % wake were compared between groups following acute stressor exposure. Consistent with greater REM rebound in the light cycle observed in the home cage rats following acute stress (Figure 6A), both repeated fear [F(1, 30) = 5.67; p = 0.02] and acute stress [F(2, 30) = 10.37; p = 0.0004] reduced the diurnal difference of % REM (Figure 7A). The flattening of the diurnal rhythm of % REM sleep was present during the first, but was gone by the second (Figure 7B), 24 h period following acute stress. Acute stress reduced the diurnal difference of % NREM sleep [F(2, 30) = 14.3; p < 0.0001; Figure 7C] and % wake [F(2, 30) = 18.77; p < 0.0001; Figure 7E] during the first 24 h period following acute stress in both home cage and repeated fear-exposed rats. During the second 24 h period following acute stress, significant interactions between repeated fear and acute stress revealed that the flattening of the diurnal rhythm of both % NREM sleep [F(2, 30) = 4.88; p = 0.01; Figure 7D] and % wake [F(2,30) = 5.44; p = 0.009; Figure 7F] persisted longer following acute stress in rats previously exposed to repeated fear. See Figure 7 for results of post hoc tests.

Bottom Line: The potentiation of anxiety produced by prior repeated fear was temporary; exaggerated fear was present 1 day but not 4 days following acute stress.This initial reduction in sleep was followed by robust REM rebound and diurnal rhythm flattening of sleep/wake behavior.These data suggest that impaired recovery of sleep/wake behavior following acute stress could contribute to the mechanisms by which a history of prior repeated stress increases vulnerability to subsequent novel stressors and stress-related disorders.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, University of Colorado Denver , Denver, CO , USA.

ABSTRACT
Repeated stressor exposure can sensitize physiological responses to novel stressors and facilitate the development of stress-related psychiatric disorders including anxiety. Disruptions in diurnal rhythms of sleep-wake behavior accompany stress-related psychiatric disorders and could contribute to their development. Complex stressors that include fear-eliciting stimuli can be a component of repeated stress experienced by human beings, but whether exposure to repeated fear can prime the development of anxiety and sleep disturbances is unknown. In the current study, adult male F344 rats were exposed to either control conditions or repeated contextual fear conditioning for 22 days followed by exposure to no, mild (10), or severe (100) acute uncontrollable tail shock stress. Exposure to acute stress produced anxiety-like behavior as measured by a reduction in juvenile social exploration and exaggerated shock-elicited freezing in a novel context. Prior exposure to repeated fear enhanced anxiety-like behavior as measured by shock-elicited freezing, but did not alter social exploratory behavior. The potentiation of anxiety produced by prior repeated fear was temporary; exaggerated fear was present 1 day but not 4 days following acute stress. Interestingly, exposure to acute stress reduced rapid eye movement (REM) and non-REM (NREM) sleep during the hours immediately following acute stress. This initial reduction in sleep was followed by robust REM rebound and diurnal rhythm flattening of sleep/wake behavior. Prior repeated fear extended the acute stress-induced REM and NREM sleep loss, impaired REM rebound, and prolonged the flattening of the diurnal rhythm of NREM sleep following acute stressor exposure. These data suggest that impaired recovery of sleep/wake behavior following acute stress could contribute to the mechanisms by which a history of prior repeated stress increases vulnerability to subsequent novel stressors and stress-related disorders.

No MeSH data available.


Related in: MedlinePlus