Chronic unpredictable stress during adolescence protects against adult traumatic brain injury-induced affective and cognitive deficits

Tremblaye, Patricia B. de la; Wellcome, Jody L; Wiley, Kaitlyn; Lomahan, Carolyn A.; Moschonas, Eleni H.; Cheng, Jeffrey P.; Bondi, Corina O.; Kline, Anthony E.

doi:10.1016/j.brainres.2021.147544

Cited by 12 publications

(6 citation statements)

References 66 publications

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“…Notably, the effect of stress on TBI is not always negative. In contrast to the above findings [ 161 ], unpredictable stress during adolescence may protect against adult TBI-induced affective and cognitive deficits [ 162 ]. Why does stress have seemingly contradictory results in TBI?…”

Section: Neurobiological Links Between Stress and Brain Injuries/dise...mentioning

confidence: 82%

Neurobiological Links between Stress, Brain Injury, and Disease

Guo

Zheng

et al. 2022

Oxidative Medicine and Cellular Longevity

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Stress, which refers to a combination of physiological, neuroendocrine, behavioral, and emotional responses to novel or threatening stimuli, is essentially a defensive adaptation under physiological conditions. However, strong and long-lasting stress can lead to psychological and pathological damage. Growing evidence suggests that patients suffering from mild and moderate brain injuries and diseases often show severe neurological dysfunction and experience severe and persistent stressful events or environmental stimuli, whether in the acute, subacute, or recovery stage. Previous studies have shown that stress has a remarkable influence on key brain regions and brain diseases. The mechanisms through which stress affects the brain are diverse, including activation of endoplasmic reticulum stress (ERS), apoptosis, oxidative stress, and excitatory/inhibitory neuron imbalance, and may lead to behavioral and cognitive deficits. The impact of stress on brain diseases is complex and involves impediment of recovery, aggravation of cognitive impairment, and neurodegeneration. This review summarizes various stress models and their applications and then discusses the effects and mechanisms of stress on key brain regions—including the hippocampus, hypothalamus, amygdala, and prefrontal cortex—and in brain injuries and diseases—including Alzheimer’s disease, stroke, traumatic brain injury, and epilepsy. Lastly, this review highlights psychological interventions and potential therapeutic targets for patients with brain injuries and diseases who experience severe and persistent stressful events.

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Section: Neurobiological Links Between Stress and Brain Injuries/dise...mentioning

confidence: 82%

Neurobiological Links between Stress, Brain Injury, and Disease

Guo

Zheng

et al. 2022

Oxidative Medicine and Cellular Longevity

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“…Interestingly, recent experimental evidence suggests that prior exposure to stress before TBI can also be neuroprotective. When adolescent rodents exposed to early-life CUS are given several weeks to recover from stress before receiving TBI in adulthood, they exhibit decreased behavioral deficits compared to rodents receiving TBI with no stress (de la Tremblaye et al, 2021 ). In general, ELS seems to exacerbate the damage and cognitive consequences sustained by TBI but may provide some protection if followed by adequate recovery time (de la Tremblaye et al, 2021 ; Lajud et al, 2021 ; Sanchez et al, 2021 ).…”

Section: Tbi Induces Neuroendocrine Dysfunctionmentioning

confidence: 99%

“…When adolescent rodents exposed to early-life CUS are given several weeks to recover from stress before receiving TBI in adulthood, they exhibit decreased behavioral deficits compared to rodents receiving TBI with no stress (de la Tremblaye et al, 2021 ). In general, ELS seems to exacerbate the damage and cognitive consequences sustained by TBI but may provide some protection if followed by adequate recovery time (de la Tremblaye et al, 2021 ; Lajud et al, 2021 ; Sanchez et al, 2021 ). The relationship between TBI and stress is complex, and it is important to point out that chronic stress during development could have a unique impact on the response to TBI compared to pre-injury stress during adulthood.…”

Section: Tbi Induces Neuroendocrine Dysfunctionmentioning

confidence: 99%

Context is key: glucocorticoid receptor and corticosteroid therapeutics in outcomes after traumatic brain injury

Taylor,

Kokiko-Cochran

2024

Front. Cell. Neurosci.

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Traumatic brain injury (TBI) is a global health burden, and survivors suffer functional and psychiatric consequences that can persist long after injury. TBI induces a physiological stress response by activating the hypothalamic-pituitary-adrenal (HPA) axis, but the effects of injury on the stress response become more complex in the long term. Clinical and experimental evidence suggests long lasting dysfunction of the stress response after TBI. Additionally, pre- and post-injury stress both have negative impacts on outcome following TBI. This bidirectional relationship between stress and injury impedes recovery and exacerbates TBI-induced psychiatric and cognitive dysfunction. Previous clinical and experimental studies have explored the use of synthetic glucocorticoids as a therapeutic for stress-related TBI outcomes, but these have yielded mixed results. Furthermore, long-term steroid treatment is associated with multiple negative side effects. There is a pressing need for alternative approaches that improve stress functionality after TBI. Glucocorticoid receptor (GR) has been identified as a fundamental link between stress and immune responses, and preclinical evidence suggests GR plays an important role in microglia-mediated outcomes after TBI and other neuroinflammatory conditions. In this review, we will summarize GR-mediated stress dysfunction after TBI, highlighting the role of microglia. We will discuss recent studies which target microglial GR in the context of stress and injury, and we suggest that cell-specific GR interventions may be a promising strategy for long-term TBI pathophysiology.

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“…In rodent models, unpredictable chronic stress during adolescence may have a protective impact on TBI-induced cognitive deficits. 10 Currently, the molecular interaction between psychological stress and TBI is poorly understood. However, one mechanism by which these different stressors might be connected is through activation of the hypothalamicpituitary-adrenal (HPA) axis, including cortisol release (corticosterone in mice) from the adrenal cortex.…”

Section: Introductionmentioning

confidence: 99%

“…Notably, the effects of stress on TBI are not always negative. In rodent models, unpredictable chronic stress during adolescence may have a protective impact on TBI‐induced cognitive deficits 10 …”

Section: Introductionmentioning

confidence: 99%

Acute stress modulates the outcome of traumatic brain injury‐associated gene expression and behavioral responses

Reiners,

Leopold,

Hallebach

et al. 2023

The FASEB Journal

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Psychological stress and traumatic brain injury (TBI) result in long‐lasting emotional and behavioral impairments in patients. So far, the interaction of psychological stress with TBI not only in the brain but also in peripheral organs is poorly understood. Herein, the impact of acute stress (AS) occurring immediately before TBI is investigated. For this, a mouse model of restraint stress and TBI was employed, and their influence on behavior and gene expression in brain regions, the hypothalamic–pituitary–adrenal (HPA) axis, and peripheral organs was analyzed. Results demonstrate that, compared to single AS or TBI exposure, mice treated with AS prior to TBI showed sex‐specific alterations in body weight, memory function, and locomotion. The induction of immediate early genes (IEGs, e.g., c‐Fos) by TBI was modulated by previous AS in several brain regions. Furthermore, IEG upregulation along the HPA axis (e.g., pituitary, adrenal glands) and other peripheral organs (e.g., heart) was modulated by AS–TBI interaction. Proteomics of plasma samples revealed proteins potentially mediating this interaction. Finally, the deletion of Atf3 diminished the TBI‐induced induction of IEGs in peripheral organs but left them largely unaltered in the brain. In summary, AS immediately before brain injury affects the brain and, to a strong degree, also responses in peripheral organs.

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Chronic unpredictable stress during adolescence protects against adult traumatic brain injury-induced affective and cognitive deficits

Cited by 12 publications

References 66 publications

Neurobiological Links between Stress, Brain Injury, and Disease

Neurobiological Links between Stress, Brain Injury, and Disease

Context is key: glucocorticoid receptor and corticosteroid therapeutics in outcomes after traumatic brain injury

Acute stress modulates the outcome of traumatic brain injury‐associated gene expression and behavioral responses

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