Constitutive differences in glucocorticoid responsiveness are related to divergent spatial information processing abilities

Huzard, Damien; Vouros, Avgoustinos; Monari, Silvia; Astori, Simone; Vasilaki, Eleni; Sandi, Carmen

doi:10.1080/10253890.2019.1625885

Cited by 12 publications

(8 citation statements)

References 75 publications

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“…Specifically, animals that showed poorer retention levels on the first trial following training day 1 were the ones that showed blunted corticosterone reactivity when exposed as adults to a novelty challenge. These observations align well with the well-known contribution of training-triggered corticosterone levels for memory function in general (de Kloet et al, 2018; de Quervain et al, 2017; Sandi, 2011)) and, specifically, for the consolidation of spatial information (Akirav et al, 2004; Conboy et al, 2010; Huzard et al, 2020; Quirarte et al, 1997; Sandi et al, 1997).…”

Section: Discussionsupporting

confidence: 87%

“…Strikingly, individual differences in the adaptation of the glucocorticoid response to repeated stress exposure during the peripubertal period in rats were found to predict subsequent changes in emotional and social phenotypes observed during adolescence (Papilloud et al, 2019) and adulthood (Walker et al, 2018; 2017). In addition, genetic selection in rats for the degree of corticosterone adaptation during peripubertal stress (Walker and Sandi, 2018) underscored genetic line-related differences in spatial learning and memory performance (Huzard et al, 2020). Accordingly, given the strong modulatory capacity of glucocorticoids on brain function and cognition (de Quervain et al, 2017; Sandi, 2011), including spatial learning (Akirav et al, 2004; Conboy et al, 2010; Sandi et al, 1997), we hypothesize that long-term programming of peripubertal stress on spatial learning would depend on the individual degree of glucocorticoid adaptation to repeated stress.…”

Section: Introductionmentioning

confidence: 99%

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Programming effects of peripubertal stress on spatial learning

Tzanoulinou

Gantelet

Sandi

et al. 2020

Preprint

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Exposure to adversity during early life can have profound influences on brain function and behavior later in life. The peripubertal period is emerging as an important time-window of susceptibility to stress, with substantial evidence documenting long-term consequences in the emotional and social domains. However, little is known about how stress during this period impacts subsequent cognitive functioning. Here, we assessed potential long-term effects of peripubertal stress on spatial learning and memory using the water maze task. In addition, we interrogated whether individual differences in stress-induced behavioral and endocrine changes are related to the degree of adaptation of the corticosterone response to repeated stressor exposure during the peripubertal period. We found that, when tested at adulthood, peripubertally stressed animals displayed a slower learning rate. Strikingly, the level of spatial orientation in the water maze completed on the last training day was predicted by the degree of adaptation of the recovery -and not the peak- of the corticosterone response to stressor exposure (i.e., plasma levels at 60 min post-stressor) across the peripubertal stress period. In addition, peripubertal stress led to changes in emotional and glucocorticoid reactivity to novelty exposure, as well as in the expression levels of the plasticity molecule PSA-NCAM in the hippocampus. Importantly, by assessing the same endpoints in another peripubertally stressed cohort tested during adolescence, we show that the observed effects at adulthood are the result of a delayed programming manifested at adulthood and not protracted effects of stress. Altogether, our results support the view that the degree of stress-induced adaptation of the hypothalamus-pituitary-adrenal axis responsiveness at the important transitional period of puberty relates to the long-term programming of cognition, behavior and endocrine reactivity.

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Section: Discussionsupporting

confidence: 87%

Section: Introductionmentioning

confidence: 99%

Programming effects of peripubertal stress on spatial learning

Tzanoulinou

Gantelet

Sandi

et al. 2020

Preprint

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“…While the exact nature and mechanisms for aging continue to be debated, important markers of biological age might include blood measures of genomic instability, epigenetics, and cellular senescence (Lidzbarsky et al, 2018;Niedernhofer et al, 2018;Aristizabal et al, 2020), telomere length (Vera et al, 2013;Stauffer et al, 2018), inflammation and the proinflammatory secr, etory profile designated the senescence-associated secretory phenotype (SASP;Boersma et al, 1985;Heller et al, 1998;Guayerbas et al, 2002;Moeller et al, 2014;Martinez de Toda et al, 2016), hormone levels (Gee et al, 1983;Matt et al, 1986;Smith et al, 1992;Fentie et al, 2004), mitochondrial function, redox state, and antioxidant defense (Heller et al, 1998;Stauffer et al, 2018;Jain et al, 2019). For example, levels of corticosterone in the blood have been associated with memory function during aging (McQuail et al, 2018;Huzard et al, 2020).…”

Section: Blood Biomarkersmentioning

confidence: 99%

Cognitive Reserve in Model Systems for Mechanistic Discovery: The Importance of Longitudinal Studies

McQuail

Dunn

Stern

et al. 2021

Front. Aging Neurosci.

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The goal of this review article is to provide a resource for longitudinal studies, using animal models, directed at understanding and modifying the relationship between cognition and brain structure and function throughout life. We propose that forthcoming longitudinal studies will build upon a wealth of knowledge gleaned from prior cross-sectional designs to identify early predictors of variability in cognitive function during aging, and characterize fundamental neurobiological mechanisms that underlie the vulnerability to, and the trajectory of, cognitive decline. Finally, we present examples of biological measures that may differentiate mechanisms of the cognitive reserve at the molecular, cellular, and network level.

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“…Will we observe the same trajectory classes in other AAPA experiments, depending on the treatments and with other strains? Our earlier work on MWM and the strategies identified therein were in fact used to analyse data from different experiments and labs 24 , 29 , 30 , suggesting that it might be possible that the same generality holds for the AAPAT. However, we need to highlight a fundamental difference.…”

Section: Discussionmentioning

confidence: 99%

Strategies discovery in the active allothetic place avoidance task

Vouros

Gehring

Jura

et al. 2022

Sci Rep

Self Cite

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The Active Allothetic Place Avoidance task is an alternative setup to Morris Water Maze that allows studying spatial memory in a dynamic world in the presence of conflicting information. In this task, a rat, freely moving on a rotating circular arena, has to avoid a sector defined within the room frame where shocks are presented. While for Morris Water Maze several studies have identified animal strategies which specifically affect performance, there were no such studies for the Active Allothetic Place Avoidance task. Using standard machine learning methods, we were able to reveal for the first time, to the best of our knowledge, explainable strategies that the animals employ in this task and demonstrate that they can provide a high-level interpretation for performance differences between an animal group treated with silver nanoparticles (AgNPs) and the control group.

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Constitutive differences in glucocorticoid responsiveness are related to divergent spatial information processing abilities

Cited by 12 publications

References 75 publications

Programming effects of peripubertal stress on spatial learning

Programming effects of peripubertal stress on spatial learning

Cognitive Reserve in Model Systems for Mechanistic Discovery: The Importance of Longitudinal Studies

Strategies discovery in the active allothetic place avoidance task

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