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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 prior repeated fear stress on persistence of anxiety behavior following severe acute stress. Following 22 days of no repeated fear (home cage) or repeated fear stress (repeated fear), rats were either exposed to no acute stress or to 100 uncontrollable tail shocks (acute severe stress). Juvenile social exploration (A) and shock-elicited freezing (B) were measured either 1 or 4 days later in a novel environment. *p < 0.05 relative to 0 groups; #main effect of repeated fear stress (p < 0.05).
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Figure 4: Effects of prior repeated fear stress on persistence of anxiety behavior following severe acute stress. Following 22 days of no repeated fear (home cage) or repeated fear stress (repeated fear), rats were either exposed to no acute stress or to 100 uncontrollable tail shocks (acute severe stress). Juvenile social exploration (A) and shock-elicited freezing (B) were measured either 1 or 4 days later in a novel environment. *p < 0.05 relative to 0 groups; #main effect of repeated fear stress (p < 0.05).

Mentions: In Experiment 2, rats exposed to repeated fear or home cage treatments were tested for anxiety-like behavior either 1 or 4 days following 0 or 100 tail shocks. Results similar to those observed in Experiment 1 were seen here. Exposure to acute stress reduced social exploration [F(2, 41) = 9.38; p = 0.0004; Figure 4A] and increased shock-elicited freezing [F(2, 41) = 4.75; p = 0.01; Figure 4B]. Regardless of history of prior repeated fear exposure, a reduction in social exploratory behavior was observed both 1 (p = 0.003) and 4 (p = 0.0002) days following tail shock stress, whereas the increase in shock-elicited freezing was only present when rats were tested 1 day following tail shock (p = 0.01). Although a history of repeated fear had no impact on social exploration [F(1, 41) = 0.007; p > 0.05], exaggerated shock-elicited freezing was again observed in rats exposed to repeated fear stress [F(1, 41) = 9.52; p = 0.004]. This exaggerated fear produced by repeated fear stress relative to home cage treatment was temporary. Exaggerated fear produced by repeated fear stress was present in rats not exposed to acute tail shock stress (p = 0.01) and 1 day (p = 0.02), but not 4 days (p > 0.05), following acute tail shock stress. Again, neither acute tail shock stress [F(2, 41) = 3.07; p > 0.05] nor repeated fear [F(1, 41) = 0.16; p > 0.05] altered the number of cage crosses during social exploration testing (data 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)

Effects of prior repeated fear stress on persistence of anxiety behavior following severe acute stress. Following 22 days of no repeated fear (home cage) or repeated fear stress (repeated fear), rats were either exposed to no acute stress or to 100 uncontrollable tail shocks (acute severe stress). Juvenile social exploration (A) and shock-elicited freezing (B) were measured either 1 or 4 days later in a novel environment. *p < 0.05 relative to 0 groups; #main effect of repeated fear stress (p < 0.05).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Effects of prior repeated fear stress on persistence of anxiety behavior following severe acute stress. Following 22 days of no repeated fear (home cage) or repeated fear stress (repeated fear), rats were either exposed to no acute stress or to 100 uncontrollable tail shocks (acute severe stress). Juvenile social exploration (A) and shock-elicited freezing (B) were measured either 1 or 4 days later in a novel environment. *p < 0.05 relative to 0 groups; #main effect of repeated fear stress (p < 0.05).
Mentions: In Experiment 2, rats exposed to repeated fear or home cage treatments were tested for anxiety-like behavior either 1 or 4 days following 0 or 100 tail shocks. Results similar to those observed in Experiment 1 were seen here. Exposure to acute stress reduced social exploration [F(2, 41) = 9.38; p = 0.0004; Figure 4A] and increased shock-elicited freezing [F(2, 41) = 4.75; p = 0.01; Figure 4B]. Regardless of history of prior repeated fear exposure, a reduction in social exploratory behavior was observed both 1 (p = 0.003) and 4 (p = 0.0002) days following tail shock stress, whereas the increase in shock-elicited freezing was only present when rats were tested 1 day following tail shock (p = 0.01). Although a history of repeated fear had no impact on social exploration [F(1, 41) = 0.007; p > 0.05], exaggerated shock-elicited freezing was again observed in rats exposed to repeated fear stress [F(1, 41) = 9.52; p = 0.004]. This exaggerated fear produced by repeated fear stress relative to home cage treatment was temporary. Exaggerated fear produced by repeated fear stress was present in rats not exposed to acute tail shock stress (p = 0.01) and 1 day (p = 0.02), but not 4 days (p > 0.05), following acute tail shock stress. Again, neither acute tail shock stress [F(2, 41) = 3.07; p > 0.05] nor repeated fear [F(1, 41) = 0.16; p > 0.05] altered the number of cage crosses during social exploration testing (data 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