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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

Freezing behavior and body weights for rats used in Experiments 1 and 2. (A) Freezing was scored before (pre) and after (post) administration of 3 foot shocks during contextual fear conditioning on day 0. Rats were re-exposed to the conditioned context twice a day, early (a.m.), or late (p.m.) during the light cycle, for 22 days. Re-instatement shocks (denoted by arrows) were administered at the end of the p.m. session when average freezing fell below 50%. The number of shocks administered is noted next to each arrow. Rats in both Experiment 1 (B) and Experiment 2 (C) exposed to repeated fear stress gained less weight over time relative to home cage control rats. *p < 0.05 relative to home cage control.
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Figure 2: Freezing behavior and body weights for rats used in Experiments 1 and 2. (A) Freezing was scored before (pre) and after (post) administration of 3 foot shocks during contextual fear conditioning on day 0. Rats were re-exposed to the conditioned context twice a day, early (a.m.), or late (p.m.) during the light cycle, for 22 days. Re-instatement shocks (denoted by arrows) were administered at the end of the p.m. session when average freezing fell below 50%. The number of shocks administered is noted next to each arrow. Rats in both Experiment 1 (B) and Experiment 2 (C) exposed to repeated fear stress gained less weight over time relative to home cage control rats. *p < 0.05 relative to home cage control.

Mentions: Rats exposed to repeated conditioned fear stress for 22 days displayed freezing behavior upon each re-exposure to the conditioned context (Figure 2A). Rats in both Experiments 1 and 2 required 6 foot shocks to maintain levels of freezing above 50%. Body weights of rats used in Experiments 1 and 2 are shown in Figures 2B,C, respectively. Both groups gained weight over time [Experiment 1, F(8, 352) = 467.1; p < 0.0001; Experiment 2, F(8, 360) = 704.5; p < 0.0001], but rats exposed to repeated fear stress gained less weight over time compared to rats exposed to home cage treatment [Experiment 1, F(8, 352) = 57.56; p < 0.0001; Experiment 2, F(8, 360) = 37.97; p < 0.0001]. Freezing and body weight data from rats used in Experiment 3 have been published previously (18) and thus are not shown.


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)

Freezing behavior and body weights for rats used in Experiments 1 and 2. (A) Freezing was scored before (pre) and after (post) administration of 3 foot shocks during contextual fear conditioning on day 0. Rats were re-exposed to the conditioned context twice a day, early (a.m.), or late (p.m.) during the light cycle, for 22 days. Re-instatement shocks (denoted by arrows) were administered at the end of the p.m. session when average freezing fell below 50%. The number of shocks administered is noted next to each arrow. Rats in both Experiment 1 (B) and Experiment 2 (C) exposed to repeated fear stress gained less weight over time relative to home cage control rats. *p < 0.05 relative to home cage control.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4202708&req=5

Figure 2: Freezing behavior and body weights for rats used in Experiments 1 and 2. (A) Freezing was scored before (pre) and after (post) administration of 3 foot shocks during contextual fear conditioning on day 0. Rats were re-exposed to the conditioned context twice a day, early (a.m.), or late (p.m.) during the light cycle, for 22 days. Re-instatement shocks (denoted by arrows) were administered at the end of the p.m. session when average freezing fell below 50%. The number of shocks administered is noted next to each arrow. Rats in both Experiment 1 (B) and Experiment 2 (C) exposed to repeated fear stress gained less weight over time relative to home cage control rats. *p < 0.05 relative to home cage control.
Mentions: Rats exposed to repeated conditioned fear stress for 22 days displayed freezing behavior upon each re-exposure to the conditioned context (Figure 2A). Rats in both Experiments 1 and 2 required 6 foot shocks to maintain levels of freezing above 50%. Body weights of rats used in Experiments 1 and 2 are shown in Figures 2B,C, respectively. Both groups gained weight over time [Experiment 1, F(8, 352) = 467.1; p < 0.0001; Experiment 2, F(8, 360) = 704.5; p < 0.0001], but rats exposed to repeated fear stress gained less weight over time compared to rats exposed to home cage treatment [Experiment 1, F(8, 352) = 57.56; p < 0.0001; Experiment 2, F(8, 360) = 37.97; p < 0.0001]. Freezing and body weight data from rats used in Experiment 3 have been published previously (18) and thus are not shown.

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