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      Acute stress differentially affects spatial configuration learning in high and low cortisol-responding healthy adults

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          Abstract

          Background

          Stress and stress hormones modulate memory formation in various ways that are relevant to our understanding of stress-related psychopathology, such as posttraumatic stress disorder (PTSD). Particular relevance is attributed to efficient memory formation sustained by the hippocampus and parahippocampus. This process is thought to reduce the occurrence of intrusions and flashbacks following trauma, but may be negatively affected by acute stress. Moreover, recent evidence suggests that the efficiency of visuo-spatial processing and learning based on the hippocampal area is related to PTSD symptoms.

          Objective

          The current study investigated the effect of acute stress on spatial configuration learning using a spatial contextual cueing task (SCCT) known to heavily rely on structures in the parahippocampus.

          Method

          Acute stress was induced by subjecting participants (N = 34) to the Maastricht Acute Stress Test (MAST). Following a counterbalanced within-subject approach, the effects of stress and the ensuing hormonal (i.e., cortisol) activity on subsequent SCCT performance were compared to SCCT performance following a no-stress control condition.

          Results

          Acute stress did not impact SCCT learning overall, but opposing effects emerged for high versus low cortisol responders to the MAST. Learning scores following stress were reduced in low cortisol responders, while high cortisol-responding participants showed improved learning.

          Conclusions

          The effects of stress on spatial configuration learning were moderated by the magnitude of endogenous cortisol secretion. These findings suggest a possible mechanism by which cortisol responses serve an adaptive function during stress and trauma, and this may prove to be a promising route for future research in this area.

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          Most cited references28

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          Contextual cueing: implicit learning and memory of visual context guides spatial attention.

          Global context plays an important, but poorly understood, role in visual tasks. This study demonstrates that a robust memory for visual context exists to guide spatial attention. Global context was operationalized as the spatial layout of objects in visual search displays. Half of the configurations were repeated across blocks throughout the entire session, and targets appeared within consistent locations in these arrays. Targets appearing in learned configurations were detected more quickly. This newly discovered form of search facilitation is termed contextual cueing. Contextual cueing is driven by incidentally learned associations between spatial configurations (context) and target locations. This benefit was obtained despite chance performance for recognizing the configurations, suggesting that the memory for context was implicit. The results show how implicit learning and memory of visual context can guide spatial attention towards task-relevant aspects of a scene.
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            Hippocampal remapping and grid realignment in entorhinal cortex.

            A fundamental property of many associative memory networks is the ability to decorrelate overlapping input patterns before information is stored. In the hippocampus, this neuronal pattern separation is expressed as the tendency of ensembles of place cells to undergo extensive 'remapping' in response to changes in the sensory or motivational inputs to the hippocampus. Remapping is expressed under some conditions as a change of firing rates in the presence of a stable place code ('rate remapping'), and under other conditions as a complete reorganization of the hippocampal place code in which both place and rate of firing take statistically independent values ('global remapping'). Here we show that the nature of hippocampal remapping can be predicted by ensemble dynamics in place-selective grid cells in the medial entorhinal cortex, one synapse upstream of the hippocampus. Whereas rate remapping is associated with stable grid fields, global remapping is always accompanied by a coordinate shift in the firing vertices of the grid cells. Grid fields of co-localized medial entorhinal cortex cells move and rotate in concert during this realignment. In contrast to the multiple environment-specific representations coded by place cells in the hippocampus, local ensembles of grid cells thus maintain a constant spatial phase structure, allowing position to be represented and updated by the same translation mechanism in all environments encountered by the animal.
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              Why do we respond so differently? Reviewing determinants of human salivary cortisol responses to challenge.

              Stress and stress-related health impairments are major problems in human life and elucidating the biological pathways linking stress and disease is of substantial importance. However, the identification of mechanisms underlying a dysregulation of major components of the stress response system is, particularly in humans, a very challenging task. Salivary cortisol responses to diverse acute challenge paradigms show large intra- and interindividual variability. In order to uncover mechanisms mediating stress-related disorders and to potentially develop new therapeutic strategies, an extensive phenotyping of HPA axis stress responses is essential. Such a research agenda depends on substantial knowledge of moderating and intervening variables that affect cortisol responses to different stressors and stimuli. The aim of this report is, therefore, to provide a comprehensive summary of important determinants of, in particular, human salivary cortisol responses to different kinds of laboratory stimuli including acute psychosocial stress as well as pharmacological provocation procedures. This overview demonstrates the role of age and gender, endogenous and exogenous sex steroid levels, pregnancy, lactation and breast-feeding, smoking, coffee and alcohol consumption as well as dietary energy supply in salivary cortisol responses to acute stress. Furthermore, it briefly summarizes current knowledge of the role of genetic factors and methodological issues in terms of habituation to repeated psychosocial stress exposures and time of testing as well as psychological factors, that have been shown to be associated with salivary cortisol responses like early life experiences, social factors, psychological interventions, personality as well as acute subjective-psychological stress responses and finally states of chronic stress and psychopathology.
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                Author and article information

                Journal
                Eur J Psychotraumatol
                Eur J Psychotraumatol
                EJPT
                European Journal of Psychotraumatology
                Co-Action Publishing
                2000-8198
                2000-8066
                02 May 2013
                2013
                : 4
                : 10.3402/ejpt.v4i0.19854
                Affiliations
                Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, The Netherlands
                Author notes
                [* ]Correspondence to: Thomas Meyer, Faculty of Psychology and Neuroscience, Maastricht University, PO Box 616, NL-6200 MD Maastricht, The Netherlands, Tel: +0031 43 3882486, Fax: +0031 43 3884196, Email: thomas.meyer@ 123456maastrichtuniversity.nl
                Article
                19854
                10.3402/ejpt.v4i0.19854
                3644058
                23671762
                482dc025-e0ff-4d79-aadb-cc965a7decc0
                © 2013 Thomas Meyer et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 09 October 2012
                : 12 December 2012
                : 15 December 2012
                Categories
                Psychotrauma Research in the Netherlands

                Clinical Psychology & Psychiatry
                maastricht acute stress test,contextual cueing paradigm,spatial memory,hippocampal area,posttraumatic stress disorder

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