Unexpected Role of Physiological Estrogen in Acute Stress-Induced Memory Deficits

Hokenson, Rachael E.; Short, Annabel K.; Chen, Yuncai; Pham, Aidan L; Adams, Emily T.; Bolton, Jessica L.; Swarup, Vivek; Gall, Christine M.; Baram, Tallie Z.

doi:10.1523/jneurosci.2146-20.2020

Cited by 32 publications

(26 citation statements)

References 124 publications

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“…Further, estrogen has been shown to have effects on brain structures involved in cognitive‐based behaviors (Ghazvini et al., 2016; Sheppard et al., 2019). Although there are many investigations of the beneficial roles of estrogen on stress‐induced complications (Dumas et al., 2012; Hokenson et al., 2021), there are few studies regarding its behavioral effects on physical or psychological stress in laboratory animals. Due to the prevalence of stress among women, especially postmenopausal women, and its destructive effects on cognition, it is necessary to find a way to reduce stress' negative effects.…”

Section: Introductionmentioning

confidence: 99%

Estrogen attenuates physical and psychological stress‐induced cognitive impairments in ovariectomized rats

Khaleghi

Rajizadeh

Bashiri³

et al. 2021

Brain and Behavior

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Introduction Women are more vulnerable to stress‐related disorders than men, which is counterintuitive as female sex hormones, especially estrogen, have been shown to be protective against stress disorders. Methods In this study, we investigated whether two different models of stress act differently on ovariectomized (OVX) rats and the impact of estrogen on physical or psychological stress‐induced impairments in cognitive‐behaviors. Adult female Wistar rats at 21–22 weeks of age were utilized for this investigation. Sham and OVX rats were subjected to physical and psychological stress for 1 hr/day for 7 days, and cognitive performance was assessed using morris water maze (MWM) and passive avoidance (PA) tests. The open field and elevated plus maze tests (EPM) evaluated exploratory and anxiety‐like behaviors. Results In sham and OVX rats, both physical and psychological stressors were associated with an increase in EPM‐determined anxiety‐like behavior. OVX rats exhibited decreased explorative behavior in comparison with nonstressed sham rats (p < .05). Both physical stress and psychological stress resulted in disrupted spatial cognition as assayed in the MWM (p < .05) and impaired learning and memory as determined by the PA test when the OVX and sham groups were compared with the nonstressed sham group. Estrogen increased explorative behavior, learning and memory (p < .05), and decreased anxiety‐like behavior compared with vehicle in OVX rats exposed to either type of stressor. Conclusions When taken together, estrogen and both stressors had opposite effects on memory, anxiety, and PA performance in a rat model of menopause, which has important implications for potential protective effects of estrogen in postmenopausal women exposed to chronic stress.

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Section: Introductionmentioning

confidence: 99%

Estrogen attenuates physical and psychological stress‐induced cognitive impairments in ovariectomized rats

Khaleghi

Rajizadeh

Bashiri³

et al. 2021

Brain and Behavior

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“…Estrogen signaling influences memory, social learning, and aggressive/defensive behavior associated with the hippocampal and medial PFC functioning (e.g., Milner et al, 2008;Luine and Frankfurt, 2012;Laredo et al, 2014;Almey et al, 2015) and thus contributes to sex differences in stress coping. In females, circulating estradiol levels mediate stress resilience (e.g., Wei et al, 2014b;Luine, 2016;Yuen et al, 2016) and facilitate cerebro-and cardio-protection (e.g., Guo et al, 2005;Murphy, 2011;Adlanmerini et al, 2014) in linear and inverted U-shaped dose-effect (e.g., Bayer et al, 2018), where high estrogen levels increase cognitive sensitivity to stress (e.g., Graham and Scott, 2018;Hokenson et al, 2021). On the one hand, this may help explain why the prevalence of PTSD-surrender-in-defeat stage in our model-is two times higher in women than in men (e.g., Breslau, 2002;Zlotnick et al, 2006;Pooley et al, 2018).…”

Section: Surrender-in-defeat (Checkmate) Stagementioning

confidence: 99%

Mental Resilience and Coping With Stress: A Comprehensive, Multi-level Model of Cognitive Processing, Decision Making, and Behavior

Palamarchuk

Vaillancourt

2021

Front. Behav. Neurosci.

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Aversive events can evoke strong emotions that trigger cerebral neuroactivity to facilitate behavioral and cognitive shifts to secure physiological stability. However, upon intense and/or chronic exposure to such events, the neural coping processes can be maladaptive and disrupt mental well-being. This maladaptation denotes a pivotal point when psychological stress occurs, which can trigger subconscious, “automatic” neuroreactivity as a defence mechanism to protect the individual from potential danger including overwhelming unpleasant feelings and disturbing or threatening thoughts.The outcomes of maladaptive neural activity are cognitive dysfunctions such as altered memory, decision making, and behavior that impose a risk for mental disorders. Although the neurocognitive phenomena associated with psychological stress are well documented, the complex neural activity and pathways related to stressor detection and stress coping have not been outlined in detail. Accordingly, we define acute and chronic stress-induced pathways, phases, and stages in relation to novel/unpredicted, uncontrollable, and ambiguous stressors. We offer a comprehensive model of the stress-induced alterations associated with multifaceted pathophysiology related to cognitive appraisal and executive functioning in stress.

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“…Sex differences in stress responses are well established [76][77][78][79]. The majority of resilience substrates identified to date have been studied and identified in male rodents.…”

Section: Developing a Cohesive Picture Of How Resilience Can Be Promotedmentioning

confidence: 99%

Rethinking stress resilience

Bhatnagar

2021

Trends in Neurosciences

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Unexpected Role of Physiological Estrogen in Acute Stress-Induced Memory Deficits

Abstract: for offering methods insight for the Y-maze and Dr. Anton Palma for helpful insight on statistical analyses. This work was funded by NIH R01 MH073136 (TZB), P50 MH096889 (TZB), and T32 MH119049-02 (REH).

Cited by 32 publications

References 124 publications

Estrogen attenuates physical and psychological stress‐induced cognitive impairments in ovariectomized rats

Estrogen attenuates physical and psychological stress‐induced cognitive impairments in ovariectomized rats

Mental Resilience and Coping With Stress: A Comprehensive, Multi-level Model of Cognitive Processing, Decision Making, and Behavior

Rethinking stress resilience

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