Differential Impact of Acute and Chronic Stress on CA1 Spatial Coding and Gamma Oscillations

Tomar, Anupratap; Polygalov, Denis; McHugh, Thomas J.

doi:10.3389/fnbeh.2021.710725

Cited by 14 publications

(9 citation statements)

References 85 publications

(133 reference statements)

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“…2g ). This finding is in line with previous work showing that chronic stress in adulthood decreases gamma oscillation power within the hippocampus 62 . Given that high-frequency oscillations in vHIP inhibit the basolateral amygdala and reduce freezing in a contextual fear conditioning paradigm 63 , the reduction of vHIP gamma oscillation power in MSEW diestrus mice might coincide with diminished emotional regulation.…”

Section: Resultssupporting

confidence: 93%

The estrous cycle modulates early-life adversity effects on mouse avoidance behavior through progesterone signaling

et al. 2022

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Early-life adversity (ELA) increases the likelihood of neuropsychiatric diagnoses, which are more prevalent in women than men. Since changes in reproductive hormone levels can also increase the probability of anxiety disorders in women, we examined the effects of ELA on adult female mice across the estrous cycle. We found that during diestrus, when progesterone levels are relatively high, ELA mice exhibit increased avoidance behavior and increased theta oscillation power in the ventral hippocampus (vHIP). We also found that diestrus ELA mice had higher levels of progesterone and lower levels of allopregnanolone, a neurosteroid metabolite of progesterone, in the vHIP compared with control-reared mice. Progesterone receptor antagonism normalized avoidance behavior in ELA mice, while treatment with a negative allosteric modulator of allopregnanolone promoted avoidance behavior in control mice. These results suggest that altered vHIP progesterone and allopregnanolone signaling during diestrus increases avoidance behavior in ELA mice.

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Section: Resultssupporting

confidence: 93%

The estrous cycle modulates early-life adversity effects on mouse avoidance behavior through progesterone signaling

et al. 2022

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“…Moreover, activity within the CA1 region has been shown to be differentially attuned to acute versus chronic stressors. In a longitudinal study where local field potentials were recorded within the CA1 region on the first and last day of chronic stress, researchers found that the initial stress experience increased firing in the CA1, while repeated exposure to stress led to decreased firing (Tomar et al 2021). Without the temporal resolution, we do not have clarity on the specific activation pattern of the CA1, however, it is clearly highly involved in the initial acute stress response of future Resilient mice.…”

Section: Discussionmentioning

confidence: 99%

Patterns of Neural Activation During an Initial Social Stress Encounter are Predictive of Future Susceptibility or Resilience: A FosTRAP2 Study

Murra

Hilde

Khalil

et al. 2023

Preprint

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Repeated social stress is a significant factor in triggering depression in vulnerable individuals, and genetic and environmental factors interact to contribute to this vulnerability. Interestingly, the role of experience in shaping vulnerability is not well studied. To what extent does an individual's initial reaction to a given stressor influence their response to similar stressors in the future? And how is this initial response encoded at the neural level to bias towards future susceptibility or resilience? The Chronic Social Defeat Stress (CSDS) mouse model offers an ideal opportunity to address these questions. Following 10 days of repeated social defeat, mice diverge into two distinct populations of social reactivity: resilient (interactive) and susceptible (avoidant). It is notable that the CSDS paradigm traditionally uses genetically inbred mice, indicating that this divergence is not genetically determined. Furthermore, the emergence of the two phenotypes only occurs following several days of exposure to stress, suggesting that the repeated experience of social defeat influences future susceptibility or resilience. In this study, we asked whether specific patterns of neural activation during the initial exposure to the social defeat stress can predict whether an individual will eventually emerge as resilient or susceptible. To address this question, we used Fos-TRAP2 mouse technology to capture brain-wide neural activation patterns elicited during the initial stress exposure, while allowing the mice to go on to experience the full course of CSDS and diverge into resilient and susceptible populations. Using a high-throughput brain-wide cell counting approach, we identified the bed nucleus of the stria terminalis and lateral septal nucleus as key hubs for encoding social defeat. We also identified the basomedial amygdala as a hub for encoding future susceptibility, and the hippocampal CA1 area and medial habenula for encoding future resilience. Our findings demonstrate that the initial experience with social stress induces a distinct brain-wide pattern of neural activation associated with defeat, as well as unique activation patterns that appear to set the stage for future resilience or susceptibility. This highly orchestrated response to defeat is seen especially in animals that emerge as resilient compared to susceptible. Overall, our work represents a critical starting place for elucidating mechanisms whereby early experiences can shape vulnerability to affective disorders.

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“…LFPs are integrative excitatory and inhibitory synaptic processes [139] that span a wide range of frequencies, including theta (4-10 Hz), beta , and gamma (30-120 Hz) oscillations, as well as sharp-wave ripples (SWRs, 110-200 Hz) [140]. Rodent studies found that restraint+tailshock and CRS enhanced hippocampal theta rhythms [114] and SWRs [141] and decreased CA1 slow/fast gamma power [142]. Chronic unpredictable stress (restraint+noise+shaking+cold air stream) also heightened theta power in ventral hippocampus (vHPC) and basolateral amygdala (BLA) and increased vHPC-BLA coherence [143], whereas chronically restrained rats (2-hr/day for 10 days) exhibited decreased beta and gamma synchrony between CA1-CA3 areas but increased lateral amygdala (LA)-hippocampus synchrony with strong LA→CA1 directional activity [144].…”

Section: Neural Activitymentioning

confidence: 99%

Neurocognitive effects of stress: a metaparadigm perspective

Kim

2023

Mol Psychiatry

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Stressful experiences, both physical and psychological, that are overwhelming (i.e., inescapable and unpredictable), can measurably affect subsequent neuronal properties and cognitive functioning of the hippocampus. At the cellular level, stress has been shown to alter hippocampal synaptic plasticity, spike and local field potential activity, dendritic morphology, neurogenesis, and neurodegeneration. At the behavioral level, stress has been found to impair learning and memory for declarative (or explicit) tasks that are based on cognition, such as verbal recall memory in humans and spatial memory in rodents, while facilitating those that are based on emotion, such as differential fear conditioning in humans and contextual fear conditioning in rodents. These vertically related alterations in the hippocampus, procedurally observed after subjects have undergone stress, are generally believed to be mediated by recurrently elevated circulating hypothalamic-pituitary-adrenal (HPA) axis effector hormones, glucocorticoids, directly acting on hippocampal neurons densely populated with corticosteroid receptors. The main purposes of this review are to (i) provide a synopsis of the neurocognitive effects of stress in a historical context that led to the contemporary HPA axis dogma of basic and translational stress research, (ii) critically reappraise the necessity and sufficiency of the glucocorticoid hypothesis of stress, and (iii) suggest an alternative metaparadigm approach to monitor and manipulate the progression of stress effects at the neural coding level. Real-time analyses can reveal neural activity markers of stress in the hippocampus that can be used to extrapolate neurocognitive effects across a range of stress paradigms (i.e., resolve scaling and dichotomous memory effects issues) and understand individual differences, thereby providing a novel neurophysiological scaffold for advancing future stress research.

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Differential Impact of Acute and Chronic Stress on CA1 Spatial Coding and Gamma Oscillations

Cited by 14 publications

References 85 publications

The estrous cycle modulates early-life adversity effects on mouse avoidance behavior through progesterone signaling

The estrous cycle modulates early-life adversity effects on mouse avoidance behavior through progesterone signaling

Patterns of Neural Activation During an Initial Social Stress Encounter are Predictive of Future Susceptibility or Resilience: A FosTRAP2 Study

Neurocognitive effects of stress: a metaparadigm perspective

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