Mechanisms of memory under stress

Schwabe, Lars; Hermans, Erno J.; Joëls, Marian; Roozendaal, Benno

doi:10.1016/j.neuron.2022.02.020

Cited by 105 publications

(61 citation statements)

References 197 publications

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“…These findings thus strongly suggest that the information storage process underlying emotional enhancement of object recognition memory by noradrenergic activation of the BLA might not be the same as that induced by stimulation of local consolidation processes within the aIC. A recent model proposed that emotional arousal triggers dynamically and temporally regulated shifts in large-scale brain network balance, enabling an organism to comprehensively reallocate its neural resources according to cognitive demands ( 17 , 53 ). Arousing stimulation, by activating NE, will first rapidly strengthen BLA–aIC connectivity and increase salience network activity at the cost of the executive control network ( 16 , 19 , 54 ).…”

Section: Discussionmentioning

confidence: 99%

Basolateral amygdala activation enhances object recognition memory by inhibiting anterior insular cortex activity

Chen

Colucci

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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Significance The basolateral amygdala is known to mediate emotional arousal effects on different forms of recognition memory via functional interactions with the insular cortex. Human neuroimaging studies have revealed that emotional stimulation first rapidly increases activity of the anterior division of the insular cortex, as part of the large-scale salience network, but suppresses anterior insular cortex activity in a delayed fashion. Here, we show that the effect of noradrenergic activation of the basolateral amygdala on enhancing object recognition memory is associated with a suppression of anterior insular cortex activity during the postlearning consolidation period. Such delayed emotional arousal effects on brain network dynamics might disrupt attentional reorienting toward new external stimuli and thereby protect the ongoing consolidation process from interference.

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Section: Discussionmentioning

confidence: 99%

Basolateral amygdala activation enhances object recognition memory by inhibiting anterior insular cortex activity

Chen

Colucci

et al. 2022

Proc. Natl. Acad. Sci. U.S.A.

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“…Accordingly, our z-scores results ( Table 3 ) demonstrate that the main differences in connectivity across the Footshock and Timepoint factors happen between the aRSC and ACC to the BLA, PrL and hippocampal subregions, indicating that these regions may become less functionally connected in stronger CFC or remote retrieval. Therefore, we hypothesize that strong contextual fear memory may engage some brain regions associated with the SN during the consolidation phase, especially the aIC and PrL, via increased noradrenergic and glucocorticoid activity in these regions ( Schwabe et al, 2022 ), and possibly this strong CFC engram inhibits the engagement of DMN-like regions such as the ACC and aRSC over time. This hypothesis is strengthened by evidence from a recent elegant study that verified an inhibitory pathway from the CA3 to the anterodorsal thalamic nucleus (ADn), which matures over time and is necessary for remote memory retrieval ( Vetere et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

“…Several studies have also linked increasing levels of arousal and stress hormones with strengthened contextual fear memories and to an acceleration of the rate of time-dependent fear generalization and systems consolidation ( Dos Santos Corrêa et al, 2019 ; Pedraza et al, 2016 ; Schwabe et al, 2022 ). More recently, studies showed that post-training activation of the noradrenergic and glucocorticoid systems modulates contextual fear memory specificity ( Atucha et al, 2017 ; Dos Santos Corrêa et al, 2021 ; Gazarini et al, 2021 ; Roozendaal and Mirone, 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Remote contextual fear retrieval engages activity from salience network regions in rats

Corrêa¹,

Grisanti²,

Franciscatto³

et al. 2022

Neurobiology of Stress

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“…Here one might expect a reduced attenuation or no effect, which was what we observed in our study during the VR task. If an even longer time period elapsed (beginning around one-hour after stress onset), later genomic cortisol effects may contribute to a reversal in the initial effects from stress, leading to an upregulation of executive control resources involving the PFC (see [ 58 ] for an extensive review). During this phase one might expect an improvement in spatial attention or navigation; however, to date no study has examined performance on such tasks in this longer time frame.…”

Section: Discussionmentioning

confidence: 99%

Stress-induced HPA activation in virtual navigation and spatial attention performance

Richardson

Tomasulo

2022

BMC Neurosci

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Background Previous research has shown that spatial performance (e.g. navigation, visuospatial memory, attention) can be influenced by acute stress; however, studies have produced mixed findings sometimes showing an improvement after stress, other times showing impairment or no overall effect. Some of these discrepancies may be related to: the type of stress system activated by the stressor (sympathetic adrenal medulla [SAM] or hypothalamic-pituitary-adrenocortical [HPA]); whether cortisol responders vs. nonresponders are analyzed subsequent to main effects; and sex differences in stress responses. In the present study, we examine the influence of HPA activation from an acute laboratory stressor (Socially Evaluated Cold Pressor test [SECPT]) on performance during two spatial tasks: Useful Field of View (UFOV; a measure of spatial attention) and virtual reality (VR) navigation. We assigned 31 males and 30 females to either the SECPT or a Non-Stress condition prior to the two spatial tasks. Cardiovascular measures including heart rate and blood pressure, and salivary cortisol biosamples were obtained at specific time points. Results Participants in the Stress condition showed increases in heart rate, systolic and diastolic blood pressure indicating sympathetic adrenal medulla (SAM) axis activation. Stress also led to increases in salivary cortisol, suggesting hypothalamic-pituitary-adrenocortical (HPA) activation. Stress did not influence overall performance in the spatial attention UFOV or the VR navigation task. However, a sex difference in spatial attention was detected when participants were divided into Stress-cortisol responders and non-responders in the UFOV task. Male Stress-cortisol responders (n = 9) showed better UFOV accuracy than female Stress-cortisol responders (n = 6); no sex differences were found among the Non-Stress control group. Furthermore, for females in the stress condition (n = 14), higher cortisol responses were associated with lower spatial attention performance. Conclusions Socially Evaluated Cold Pressor stress resulted in no change in speed or accuracy in a VR navigation task. For the spatial attention task, the SECPT led to a sex difference among Stress-cortisol responders with males showing improved accuracy over females. The relationship between HPA activation and prefrontal cortex activity may be necessary to understand sex differences in spatial attention performance.

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Mechanisms of memory under stress

Cited by 105 publications

References 197 publications

Basolateral amygdala activation enhances object recognition memory by inhibiting anterior insular cortex activity

Basolateral amygdala activation enhances object recognition memory by inhibiting anterior insular cortex activity

Remote contextual fear retrieval engages activity from salience network regions in rats

Stress-induced HPA activation in virtual navigation and spatial attention performance

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