The Role of Stress and Glucocorticoids in Learning and Memory

A special issue of Brain Sciences (ISSN 2076-3425). This special issue belongs to the section "Educational Neuroscience".

Deadline for manuscript submissions: closed (25 January 2021) | Viewed by 30075

Special Issue Editors


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Guest Editor
Department of Psychobiology, School of Psychology, Universidad Nacional de Educación a Distancia (UNED), Madrid, Spain
Interests: learning & memory; stress; cortisol; perceived stress; loneliness; aging; mild cognitive impairment

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Guest Editor
Department of Psychobiology, University of Valencia, 46010 Valencia, Spain
Interests: reproductive endocrinology; memory; sleep; memory and learning; psychological resilience; neuroscience; neural plasticity; cognitive neuroscience; psychological assessment; psychophysiology; cognitive neuropsychology
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Special Issue Information

Dear Colleagues,

A growing body of literature indicates that exposure to stressful events can positively or negatively modulate the amount of information that is learned, consolidated, and retrieved. This modulation depends not only on the type of stress, but also on the time that the stressful experience occurs, its duration, and its intensity. In addition, age and sex/gender differences have been observed in the specific effects of stress on cognitive function.

Considering that more research is required to extend and advance our scientific understanding of the nexus about how stress can affect learning and memory, in this Special Issue we look forward to receiving novel and original papers and reviews related (but not limited) to the following topics:

  • learning and memory under stress;
  • stressful life events and cognitive function;
  • stress response and cognitive abilities;
  • cognitive resilience.

We want to bring together a set of cutting-edge research articles that attempt to take these topics forward. The contribution may include a mixture of theoretical, conceptual, and empirical cases, but must very clearly address one or more of the Special Issue topics.

We also solicit original, unpublished empirical studies in animals and humans. Review papers are also welcome, but as the Special Issue may include a number of invited reviews, these should be discussed with the editors at an early stage to avoid duplication. Also, please ask one of the editors if you are uncertain whether a report of your research would be suitable for inclusion.

Dr. César Venero
Prof. Dr. Alicia Salvador
Guest Editors

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Keywords

  • stress
  • cortisol
  • learning and memory
  • early life stress
  • cognitive resilience
  • mild cognitive impairment
  • Alzheimer´s disease.

Published Papers (8 papers)

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Research

21 pages, 5213 KiB  
Article
Imaging of Functional Brain Circuits during Acquisition and Memory Retrieval in an Aversive Feedback Learning Task: Single Photon Emission Computed Tomography of Regional Cerebral Blood Flow in Freely Behaving Rats
by Katharina Braun, Anja Mannewitz, Joerg Bock, Silke Kreitz, Andreas Hess, Henning Scheich and Jürgen Goldschmidt
Brain Sci. 2021, 11(5), 659; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci11050659 - 18 May 2021
Viewed by 2523
Abstract
Active avoidance learning is a complex form of aversive feedback learning that in humans and other animals is essential for actively coping with unpleasant, aversive, or dangerous situations. Since the functional circuits involved in two-way avoidance (TWA) learning have not yet been entirely [...] Read more.
Active avoidance learning is a complex form of aversive feedback learning that in humans and other animals is essential for actively coping with unpleasant, aversive, or dangerous situations. Since the functional circuits involved in two-way avoidance (TWA) learning have not yet been entirely identified, the aim of this study was to obtain an overall picture of the brain circuits that are involved in active avoidance learning. In order to obtain a longitudinal assessment of activation patterns in the brain of freely behaving rats during different stages of learning, we applied single-photon emission computed tomography (SPECT). We were able to identify distinct prefrontal cortical, sensory, and limbic circuits that were specifically recruited during the acquisition and retrieval phases of the two-way avoidance learning task. Full article
(This article belongs to the Special Issue The Role of Stress and Glucocorticoids in Learning and Memory)
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21 pages, 3500 KiB  
Article
Differential Susceptibility to the Impact of the COVID-19 Pandemic on Working Memory, Empathy, and Perceived Stress: The Role of Cortisol and Resilience
by Shishir Baliyan, José Manuel Cimadevilla, Silvia de Vidania, Matías M. Pulopulos, Carmen Sandi and César Venero
Brain Sci. 2021, 11(3), 348; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci11030348 - 09 Mar 2021
Cited by 18 | Viewed by 8939
Abstract
There are important individual differences in adaptation and reactivity to stressful challenges. Being subjected to strict social confinement is a distressful psychological experience leading to reduced emotional well-being, but it is not known how it can affect the cognitive and empathic tendencies of [...] Read more.
There are important individual differences in adaptation and reactivity to stressful challenges. Being subjected to strict social confinement is a distressful psychological experience leading to reduced emotional well-being, but it is not known how it can affect the cognitive and empathic tendencies of different individuals. Cortisol, a key glucocorticoid in humans, is a strong modulator of brain function, behavior, and cognition, and the diurnal cortisol rhythm has been postulated to interact with environmental stressors to predict stress adaptation. The present study investigates in 45 young adults (21.09 years old, SD = 6.42) whether pre-pandemic diurnal cortisol indices, overall diurnal cortisol secretion (AUCg) and cortisol awakening response (CAR) can predict individuals’ differential susceptibility to the impact of strict social confinement during the Coronavirus Disease 2019 (COVID-19) pandemic on working memory, empathy, and perceived stress. We observed that, following long-term home confinement, there was an increase in subjects’ perceived stress and cognitive empathy scores, as well as an improvement in visuospatial working memory. Moreover, during confinement, resilient coping moderated the relationship between perceived stress scores and pre-pandemic AUCg and CAR. In addition, in mediation models, we observed a direct effect of AUCg and an indirect effect of both CAR and AUCg, on change in perceived self-efficacy. These effects were parallelly mediated by the increase in working memory span and cognitive empathy. In summary, our findings reveal the role of the diurnal pattern of cortisol in predicting the emotional impact of the COVID-19 pandemic, highlighting a potential biomarker for the identification of at-risk groups following public health crises. Full article
(This article belongs to the Special Issue The Role of Stress and Glucocorticoids in Learning and Memory)
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15 pages, 7308 KiB  
Article
Post-Encoding Stress Does Not Enhance Memory Consolidation: The Role of Cortisol and Testosterone Reactivity
by Vanesa Hidalgo, Carolina Villada and Alicia Salvador
Brain Sci. 2020, 10(12), 995; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci10120995 - 16 Dec 2020
Cited by 3 | Viewed by 2151
Abstract
In contrast to the large body of research on the effects of stress-induced cortisol on memory consolidation in young people, far less attention has been devoted to understanding the effects of stress-induced testosterone on this memory phase. This study examined the psychobiological (i.e., [...] Read more.
In contrast to the large body of research on the effects of stress-induced cortisol on memory consolidation in young people, far less attention has been devoted to understanding the effects of stress-induced testosterone on this memory phase. This study examined the psychobiological (i.e., anxiety, cortisol, and testosterone) response to the Maastricht Acute Stress Test and its impact on free recall and recognition for emotional and neutral material. Thirty-seven healthy young men and women were exposed to a stress (MAST) or control task post-encoding, and 24 h later, they had to recall the material previously learned. Results indicated that the MAST increased anxiety and cortisol levels, but it did not significantly change the testosterone levels. Post-encoding MAST did not affect memory consolidation for emotional and neutral pictures. Interestingly, however, cortisol reactivity was negatively related to free recall for negative low-arousal pictures, whereas testosterone reactivity was positively related to free recall for negative-high arousal and total pictures. This study provides preliminary evidence about a different reactivity of testosterone and cortisol to the MAST as well as on their effects on consolidation. Our results suggest a different pattern of relationships between these steroid hormones and the arousal of the negative images. Full article
(This article belongs to the Special Issue The Role of Stress and Glucocorticoids in Learning and Memory)
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29 pages, 3036 KiB  
Article
Prolonged Social Isolation, Started Early in Life, Impairs Cognitive Abilities in Rats Depending on Sex
by Nataliya A. Krupina, Sophie D. Shirenova and Nadezhda N. Khlebnikova
Brain Sci. 2020, 10(11), 799; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci10110799 - 30 Oct 2020
Cited by 20 | Viewed by 2597
Abstract
Background: The chronic stress of social isolation is a valid predictor of cognitive pathology. This study aimed to compare the effects of long-term social isolation on female versus male Wistar rats’ learning and memory. We hypothesized that prolonged social isolation stress, which starts [...] Read more.
Background: The chronic stress of social isolation is a valid predictor of cognitive pathology. This study aimed to compare the effects of long-term social isolation on female versus male Wistar rats’ learning and memory. We hypothesized that prolonged social isolation stress, which starts early in life, would affect learning in a sex-dependent manner. Methods: Social isolation started at the edge of early to mid-adolescence and lasted 9 months. The rat’s cognitive abilities were assessed by habituation and reactivity to novelty in the open field (OF) test, spatial memory in the Morris water maze (MWM), and the conditioned passive avoidance (PA) reflex. Basal serum corticosterone levels were assessed using an enzyme-linked immunosorbent assay. Results: Regardless of the housing conditions, females habituated to the OF under low illumination slower than males. Under bright light, the single-housed rats showed hyporeactivity to novelty. In the MWM, all the rats learned to locate the platform; however, on the first training day, the single-housed females’ speed was lower relative to other groups. Four months later, in the post-reminder probe trial, the single-housed rats reached the area around the platform site later, and only males, regardless of housing conditions, preferred the target quadrant. Single-housed rats, irrespective of sex, showed a PA deficit. There was a more pronounced conditioned fear in the single-housed males than in females. In both male and female rats, basal corticosterone levels in rat blood serum after 9 months of social isolation did not differ from that in the group-housed rats of the corresponding sex. Meanwhile, females’ basal corticosterone level was higher than in males, regardless of the housing conditions. The relative weight of the adrenal glands was increased only in single-housed females. Conclusions: Under long-term social isolation, started early in life, single-housed females compared with males showed more pronounced cognitive impairments in the MWM and PA paradigm, findings that specify their greater vulnerability to the stress of prolonged social isolation. Full article
(This article belongs to the Special Issue The Role of Stress and Glucocorticoids in Learning and Memory)
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13 pages, 1152 KiB  
Article
Resting EEG, Hair Cortisol and Cognitive Performance in Healthy Older People with Different Perceived Socioeconomic Status
by Carolina Villada, Mauricio González-López, Herlinda Aguilar-Zavala and Thalía Fernández
Brain Sci. 2020, 10(9), 635; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci10090635 - 15 Sep 2020
Cited by 3 | Viewed by 3017
Abstract
Successful aging depends upon several internal and external factors that influence the overall aging process. Objective and subjective socioeconomic status emerge as potential psychosocial factors in the ethiopathophysiology of aging-related disorders. Presumably, low socioeconomic status can act as a psychosocial stressor that can [...] Read more.
Successful aging depends upon several internal and external factors that influence the overall aging process. Objective and subjective socioeconomic status emerge as potential psychosocial factors in the ethiopathophysiology of aging-related disorders. Presumably, low socioeconomic status can act as a psychosocial stressor that can affect humans’ physiology via psychoneuroendocrine mechanisms, that may, in turn, affect the brain physiology. In resting-state electroencephalography (EEG), excess theta and delta activity has been related to cognitive decline and dementia. The main aim of this study was to analyze the effect of objective and subjective socioeconomic status (SES) on cognition and brain electrical activity through EEG measures. The present research constitutes a cross-sectional study with thirty healthy older adults (61–82 years old) separated into two clusters: high socioeconomic (HS) and low socioeconomic (LS) status; they were evaluated and compared in cognitive terms using the Wechsler Adult Intelligence Scale (WAIS-IV). An EEG at rest was recorded to measure brain activity and, as an indicator of long-term stress exposure, hair cortisol concentrations (HCC) were measured. Our results show that lower SES is related to a worse performance in working memory tasks (p = 0.009), higher delta (p = 0.002) and theta power (p = 0.039), and lower alpha activity (p = 0.028). However, it seems that SES does not significantly affect HCC in this population of healthy older adults. The effects of SES on long-term cortisol exposure, brain electrical activity, and cognitive functions in healthy older people emphasize the role of psychosocial factors in aging from an integrative perspective that will allow us to implement better prevention programs to target cognitive decline in adults. Full article
(This article belongs to the Special Issue The Role of Stress and Glucocorticoids in Learning and Memory)
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20 pages, 1799 KiB  
Article
Associations between Attention and Implicit Associative Learning in Healthy Adults: The Role of Cortisol and Salivary Alpha-Amylase Responses to an Acute Stressor
by Linda Becker and Nicolas Rohleder
Brain Sci. 2020, 10(8), 544; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci10080544 - 12 Aug 2020
Cited by 16 | Viewed by 3362
Abstract
In this study, we investigated the associations between implicit associative learning with the cortisol and salivary alpha-amylase (sAA) stress response to an acute stressor as well as their associations with attention. Eighty one healthy adults (25 male) participated and either performed the socially [...] Read more.
In this study, we investigated the associations between implicit associative learning with the cortisol and salivary alpha-amylase (sAA) stress response to an acute stressor as well as their associations with attention. Eighty one healthy adults (25 male) participated and either performed the socially evaluated cold-pressor test (SECPT) or a warm-water control task (WWT). Either prior to or immediately after the SECPT/WWT, participants implicitly learned digit-symbol pairs. A not-previously announced recall test was conducted about 20 min after the SECPT/WWT. Attention was assessed by means of a Stroop task at nine time points over the course of the experiment. Memory recall performance was not significantly associated with the acquisition time point (pre or post stressor) and did not significantly differ between the responder groups (i.e., non-responders, sAA-and-cortisol responders, only sAA responders, and only cortisol responders). Attentional performance increased throughout the experiment (i.e., reaction times in the Stroop task decreased). No differences in the attentional time course were found between the responder groups. However, some associations were found (puncorrected < 0.05) that did not pass the multiple comparison adjusted alpha level of αadjusted = 0.002, indicating different associations between attention and implicit learning between the responder groups. We conclude that the associations of sAA and cortisol responses with implicit learning are complex and are related to each other. Further studies in which both (sAA and cortisol responses) are selectively (de-) activated are needed. Furthermore, different learning tasks and less—potentially stressful—attentional assessments should be used in future research. Moreover, field studies are needed in which the associations between acute stress and implicit associative learning are investigated in everyday life. Full article
(This article belongs to the Special Issue The Role of Stress and Glucocorticoids in Learning and Memory)
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17 pages, 1649 KiB  
Article
Sex-Specific Effects of Early Life Stress on Brain Mitochondrial Function, Monoamine Levels and Neuroinflammation
by Héctor González-Pardo, Jorge L. Arias, Eneritz Gómez-Lázaro, Isabel López Taboada and Nélida M. Conejo
Brain Sci. 2020, 10(7), 447; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci10070447 - 14 Jul 2020
Cited by 22 | Viewed by 3773
Abstract
Sex differences have been reported in the susceptibility to early life stress and its neurobiological correlates in humans and experimental animals. However, most of the current research with animal models of early stress has been performed mainly in males. In the present study, [...] Read more.
Sex differences have been reported in the susceptibility to early life stress and its neurobiological correlates in humans and experimental animals. However, most of the current research with animal models of early stress has been performed mainly in males. In the present study, prolonged maternal separation (MS) paradigm was applied as an animal model to resemble the effects of adverse early experiences in male and female rats. Regional brain mitochondrial function, monoaminergic activity, and neuroinflammation were evaluated as adults. Mitochondrial energy metabolism was greatly decreased in MS females as compared with MS males in the prefrontal cortex, dorsal hippocampus, and the nucleus accumbens shell. In addition, MS males had lower serotonin levels and increased serotonin turnover in the prefrontal cortex and the hippocampus. However, MS females showed increased dopamine turnover in the prefrontal cortex and increased norepinephrine turnover in the striatum, but decreased dopamine turnover in the hippocampus. Sex differences were also found for pro-inflammatory cytokine levels, with increased levels of TNF-α and IL-6 in the prefrontal cortex and hippocampus of MS males, and increased IL-6 levels in the striatum of MS females. These results evidence the complex sex- and brain region-specific long-term consequences of early life stress. Full article
(This article belongs to the Special Issue The Role of Stress and Glucocorticoids in Learning and Memory)
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12 pages, 1850 KiB  
Article
Stress-Induced Increase in Cortisol Negatively Affects the Consolidation of Contextual Elements of Episodic Memories
by Matthew Sabia and Almut Hupbach
Brain Sci. 2020, 10(6), 358; https://0-doi-org.brum.beds.ac.uk/10.3390/brainsci10060358 - 09 Jun 2020
Cited by 2 | Viewed by 2989
Abstract
Stress can modulate episodic memory in various ways. The present study asks how post-encoding stress affects visual context memory. Participants encoded object images centrally positioned on background scenes. After encoding, they were either exposed to cold pressure stress (CPS) or a warm water [...] Read more.
Stress can modulate episodic memory in various ways. The present study asks how post-encoding stress affects visual context memory. Participants encoded object images centrally positioned on background scenes. After encoding, they were either exposed to cold pressure stress (CPS) or a warm water control procedure. Forty-right hours later, participants were cued with object images, and for each image, they were asked to select the background scene with which it was paired during study among three highly similar options. Only male but not female participants reacted with a significant increase in salivary cortisol to CPS, and the stress and control group did not differ in recognition performance. Comparing recognition performance between stress responders and non-responders, however, revealed a significant impairment in context memory in responders. Additionally, proportional increase in cortisol was negatively correlated with the number of correctly recognized scenes in responders. Due to the small number of responders, these findings need to be interpreted with caution but provide preliminary evidence that stress-induced cortisol increase negatively affects the consolidation of contextual elements of episodic memories. Full article
(This article belongs to the Special Issue The Role of Stress and Glucocorticoids in Learning and Memory)
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