Rapid stress‐induced corticosterone rise in the hippocampus reverses serial memory retrieval pattern

Chauveau, Frédéric; Tronche, Christophe; Piérard, Christophe; Liscia, Pierrette; Drouet, Isabelle; Coutan, M.; Béracochéa, Daniel

doi:10.1002/hipo.20605

Cited by 50 publications

(63 citation statements)

References 74 publications

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“…Administration of corticosterone 30 min before a memory retrieval task impaired retrieval of information in a non-genomic, hippocampaldependent and MR-mediated manner (Khaksari et al 2007, Sajadi et al 2007. Finally, acute stress or cort-BSA infusion into the hippocampus induced a shift in memory retrieval tested 5 or 15 min later; however, this study did not investigate the receptor involved (Chauveau et al 2010). Rapid, in addition to delayed, corticosteroid effects thus seem to be involved in all phases of the memory process, i.e.…”

Section: Adaptation Of Behaviour and Cognitionmentioning

confidence: 75%

Rapid non-genomic effects of corticosteroids and their role in the central stress response

Groeneweg¹,

Karst²,

Kloet³

et al. 2011

Journal of Endocrinology

361

269

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In response to a stressful encounter, the brain activates a comprehensive stress system that engages the organism in an adaptive response to the threatening situation. This stress system acts on multiple peripheral tissues and feeds back to the brain; one of its key players is the family of corticosteroid hormones. Corticosteroids affect brain functioning through both delayed, genomic and rapid, non-genomic mechanisms. The latter mode of action has long been known, but it is only in recent years that the physiological basis in the brain is beginning to be unravelled. We now know that corticosteroids exert rapid, non-genomic effects on the excitability and activation of neurons in (amongst others) the hypothalamus, hippocampus, amygdala and prefrontal cortex. In addition, corticosteroids affect cognition, adaptive behaviour and neuroendocrine output within minutes. Knowledge on the identity of the receptors and secondary pathways mediating the non-genomic effects of corticosteroids on a cellular level is accumulating. Interestingly, in many cases, an essential role for the 'classical' mineralocorticoid and glucocorticoid receptors in a novel membrane-associated mechanism is found. Here, we systematically review the recent literature on non-genomic actions of corticosteroids on neuronal activity and functioning in selected limbic brain targets. Further, we discuss the relevance of these permissive effects for cognition and neuroendocrine control, and the integration of this novel mode of action into the complex balanced pattern of stress effects in the brain.

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Section: Adaptation Of Behaviour and Cognitionmentioning

confidence: 75%

Rapid non-genomic effects of corticosteroids and their role in the central stress response

Groeneweg¹,

Karst²,

Kloet³

et al. 2011

Journal of Endocrinology

361

269

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“…Running mice were then subjected to a final running session the next day, 30 minutes after being administered intraperitoneally (i.p.) with saline (Running-Saline group, n = 9) or with the inhibitor of corticosterone synthesis metyrapone (35mg/kg as in [31], Running-Metyrapone group, n = 11). Two mice were excluded as they did not access the wheel following the injection.…”

Section: Methodsmentioning

confidence: 99%

Corticosterone and dopamine D2/D3 receptors mediate the motivation for voluntary wheel running in C57BL/6J mice

Ebada

Kendall

Pardon

2016

Behavioural Brain Research

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Number of tables: 1Number of words in the abstract: 248Number of words in the manuscript (including tables and figure legends): 6,639Number of words in the introduction: 1,290Number of words in the discussion: 1,243 ABSTRACT Physical exercise can improve cognition but whether this is related to motivation levels is unknown. Voluntary wheel running is a rewarding activity proposed as a model of motivation to exercise. To question the potential effects of exercise motivation on subsequent behaviour, we used a pharmacological approach targeting some reward mechanisms. The stress hormone corticosterone has rewarding effects mediated by activation of low affinity glucocorticoid receptors (GR). To investigate whether corticosterone synthesis motivates exercise via activation of GRs and subsequently, impacts on behaviour, we treated C57BL/6J mice acutely with the inhibitor of corticosterone synthesis metyrapone (35 mg/kg) or repeatedly with the GR antagonist mifepristone (30 mg/kg) prior to 1-hour running wheel sessions. To investigate whether reducing motivation to exercise impacts on behaviour, we antagonised running-induced dopamine D2/D3 receptors activation with sulpiride (25 or 50 mg/kg) and assessed locomotor, anxiety-related and memory performance after 20 running sessions over 4 weeks. We found that corticosterone synthesis contributes to running levels, but the maintenance of running behaviour was not mediated by activation of GRs. Intermittent exercise was not associated with changes in behavioural or cognitive performance. The persistent reduction in exercise levels triggered by sulpiride also had limited impact on behavioural performance, although the level of performance for some behaviours was related to the level of exercise. Altogether, these findings indicate that corticosterone and dopamine D2/D3 receptor activation contribute to the motivation for wheel running, but suggest that motivation for exercise is not a sufficient factor to alter behaviour in healthy mice.

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“…More pointedly, whereas non-stressed animals remembered accurately the first learned discrimination and not the second one within a series, stressed mice remembered more accurately the second discrimination but not the first one. Moreover, the MRP under non-stress conditions was critically dependent on the dHPC but not on mPFC, whereas the opposite was observed under stress conditions (Chauveau et al, 2008, 2009, 2010; Tronche et al, 2010). …”

Section: Introductionmentioning

confidence: 94%

“…The impact of GCs on cognitive functions is however not uniform. GCs effects on memory processes tend either to occur gradually over time via transcriptional regulation initiated by intracellular receptor activation (McEwen and Sapolsky, 1995; McGaugh and Roozendaal, 2002; Joels et al, 2006) or may develop rapidly along a non-genomic pathway through membrane receptor activation (Borski, 2000; Falkenstein et al, 2000; Caudal et al, 2010; Chauveau et al, 2010; Conboy and Sandi, 2010; Chaouloff and Groc, 2011; Dorey et al, 2011). Recent findings have underscored striking shifts in the levels of both MRs and GRs that varied by brain regions (Segal et al, 2010) but also time after stress.…”

Section: Introductionmentioning

confidence: 99%

Stress induced a shift from dorsal hippocampus to prefrontal cortex dependent memory retrieval: role of regional corticosterone

Dominguez

Faucher

Henkous

et al. 2014

Front. Behav. Neurosci.

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Most of the deleterious effects of stress on memory retrieval are due to a dysfunction of the hippocampo-prefrontal cortex interplay. The role of the stress-induced regional corticosterone increase in such dysfunction remains however unclear, since there is no published study as yet dedicated to measuring corticosterone concentrations simultaneously in both the prefrontal cortex (mPFC) and the hippocampus (dHPC) in relation with memory impairments. To that aim, we first showed in Experiment 1 that an acute stress (3 electric footschocks; 0.9 mA each) delivered before memory testing reversed the memory retrieval pattern (MRP) in a serial discrimination task in which mice learned two successive discriminations. More precisely, whereas non-stressed animals remembered accurately the first learned discrimination and not the second one, stressed mice remembered more accurately the second discrimination but not the first one. We demonstrated that local inactivation of dHPC or mPFC with the anesthetic lidocaine recruited the dHPC activity in non-stress conditions whereas the stress-induced MRP inversion recruited the mPFC activity. In a second experiment, we showed that acute stress induced a very similar time-course evolution of corticosterone rises within both the mPFC and dHPC. In a 3rd experiment, we found however that in situ injections of corticosterone either within the mPFC or the dHPC before memory testing favored the emergence of the mPFC-dependent MRP but blocked the emergence of the dHPC-dependent one. Overall, our study evidences that the simultaneous increase of corticosterone after stress in both areas induces a shift from dHPC (non-stress condition) to mPFC-dependent MRP and that corticosterone is critically involved in mediating the deleterious effects of stress on cognitive functions involving the mPFC-HPC interplay.

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Rapid stress‐induced corticosterone rise in the hippocampus reverses serial memory retrieval pattern

Cited by 50 publications

References 74 publications

Rapid non-genomic effects of corticosteroids and their role in the central stress response

Rapid non-genomic effects of corticosteroids and their role in the central stress response

Corticosterone and dopamine D2/D3 receptors mediate the motivation for voluntary wheel running in C57BL/6J mice

Stress induced a shift from dorsal hippocampus to prefrontal cortex dependent memory retrieval: role of regional corticosterone

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