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Sex differences in the delayed impact of acute stress on the amygdala.

ABSTRACT: There is accumulating evidence that stress triggers specific temporal patterns of morphological plasticity in the amygdala, a brain area that plays a pivotal role in the debilitating emotional symptoms of stress-related psychiatric disorders. Acute immobilization stress is known to cause a delayed increase in the density of dendritic spines on principal neurons in the basolateral amygdala (BLA) of rats. These neuronal changes are also accompanied by a delayed enhancement in anxiety-like behavior. However, these earlier studies used male rats, and the delayed behavioral and synaptic effects of acute stress on the BLA of female rats remain unexplored. Here, using whole-cell recordings in rat brain slices, we find that a single exposure to 2-h immobilization stress leads to an increase, 10 days later, in the frequency of miniature excitatory postsynaptic currents (mEPSCs) recorded from lateral amygdala (LA) principal neurons in male rats. Further, acute stress also causes a reduction in the frequency of miniature inhibitory postsynaptic currents (mIPSCs) in LA neurons 10 days after acute stress. In striking contrast, excitatory and inhibitory synaptic transmission in the LA of female rats does not exhibit any delayed change despite exposure to the same acute stress. Finally, we examined the functional impact of these contrasting synaptic changes at the behavioral level. Male rats exhibit a delayed increase in anxiety-like behavior on the elevated plus-maze 10 days after acute stress. However, the same stress does not lead to a delayed anxiogenic effect in female rats. Together, these results demonstrate that the delayed modulation of the balance of synaptic excitation and inhibition in the amygdala, as well as anxiety-like behavior, differ between males and females. These findings provide a framework, across biological scales, for analyzing how affective symptoms of stress disorders vary between the sexes.

SUBMITTER: Gupta K

PROVIDER: S-EPMC7807162 | biostudies-literature | 2021 May

REPOSITORIES: biostudies-literature

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Sex differences in the delayed impact of acute stress on the amygdala.

Gupta Kanika K Chattarji Sumantra S

Neurobiology of stress 20210107

There is accumulating evidence that stress triggers specific temporal patterns of morphological plasticity in the amygdala, a brain area that plays a pivotal role in the debilitating emotional symptoms of stress-related psychiatric disorders. Acute immobilization stress is known to cause a delayed increase in the density of dendritic spines on principal neurons in the basolateral amygdala (BLA) of rats. These neuronal changes are also accompanied by a delayed enhancement in anxiety-like behavior ...[more]

PMID: 33490316

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Project description:Stressors experienced during adolescence have been demonstrated to have a long-lasting influence on affective behavior in adulthood. Notably, most studies to date have found these outcomes after chronic stress during adolescence. In the present study we tested how exposure to a single episode of acute footshock during early adolescence would modify subsequent adult anxiety- and depressive-like behaviors in male and female Sprague-Dawley rats. Adolescent rats were exposed to inescapable footshock (80 shocks, 5 s, 1.0 mA, 90 sec variable inter-trial interval (ITI)) at Post-natal day (PND) 29-30 and remained undisturbed until adulthood where they were evaluated with several behavioral assays for anxiety as well as depressive-like behavior via forced swim. In addition, gene expression changes were assessed immediately after a 30 min forced swim challenge in adulthood among several stress-related brain regions including the Central Amygdala (CeA), Medial Amygdala (MeA), ventral Hippocampus (vHPC), and Paraventricular Nucleus (PVN). Studies used real-time RT-PCR to examine the cytokines Interleukin-1β (IL-1β) and Interleukin-6 (IL-6), corticotropin-releasing hormone (CRH), the immediate early genes c-Fos, c-Jun, Egr1 and Arc, and several genes relating to corticosteroid receptor function (glucocorticoid and mineralocorticoid receptor (GR and MR, respectively), Gilz (glucocorticoid-induced leucine zipper), Sgk1 (Serum and Glucocorticoid regulated Kinase 1)). Behaviorally, males displayed signs of increased anxiety, most notably in the light-dark box, whereas females did not. No notable depressive-like behavior was observed in forced swim as a result of adolescent stress history, but adolescent footshock exacerbated the c-Fos response in the MeA produced by swim in both sexes. Forced swim led to increased IL-1β expression in the PVN regardless of adolescent stress history, whereas most HPA (hypothalamic-pituitaryadrenal) axis-related genes were largely unaffected in the vHPC. To determine the potential for β-adrenergic receptors to contribute to the male-specific anxiety-like behavior, two further studies applied a β-adrenergic agonist (isoproterenol) or antagonist (propranolol) in male rats. These studies found that propranolol administered 2 h after footshock led to a reduction in some anxiety-like behaviors as compared to controls. Overall, these findings suggest that exposure to a single, intense stress challenge imposed during adolescence may have sex-specific consequences across the lifespan and may implicate the MeA in developmental plasticity.

Dataset Information

Sex differences in the delayed impact of acute stress on the amygdala.

Publications

Sex differences in the delayed impact of acute stress on the amygdala.

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