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      Influence of Pre-Training Predator Stress on the Expression of c-fos mRNA in the Hippocampus, Amygdala, and Striatum Following Long-Term Spatial Memory Retrieval

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          Abstract

          We have studied the influence of pre-training psychological stress on the expression of c-fos mRNA following long-term spatial memory retrieval. Rats were trained to learn the location of a hidden escape platform in the radial-arm water maze, and then their memory for the platform location was assessed 24 h later. Rat brains were extracted 30 min after the 24-h memory test trial for analysis of c-fos mRNA. Four groups were tested: (1) Rats given standard training (Standard); (2) Rats given cat exposure (Predator Stress) 30 min prior to training (Pre-Training Stress); (3) Rats given water exposure only (Water Yoked); and (4) Rats given no water exposure (Home Cage). The Standard trained group exhibited excellent 24 h memory which was accompanied by increased c-fos mRNA in the dorsal hippocampus and basolateral amygdala (BLA). The Water Yoked group exhibited no increase in c-fos mRNA in any brain region. Rats in the Pre-Training Stress group were classified into two subgroups: good and bad memory performers. Neither of the two Pre-Training Stress subgroups exhibited a significant change in c-fos mRNA expression in the dorsal hippocampus or BLA. Instead, stressed rats with good memory exhibited significantly greater c-fos mRNA expression in the dorsolateral striatum (DLS) compared to stressed rats with bad memory. This finding suggests that stressed rats with good memory used their DLS to generate a non-spatial (cue-based) strategy to learn and subsequently retrieve the memory of the platform location. Collectively, these findings provide evidence at a molecular level for the involvement of the hippocampus and BLA in the retrieval of spatial memory and contribute novel observations on the influence of pre-training stress in activating the DLS in response to long-term memory retrieval.

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          Most cited references102

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          Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5.

          Recent work has shown that the hippocampus contains a class of receptors for the excitatory amino acid glutamate that are activated by N-methyl-D-aspartate (NMDA) and that exhibit a peculiar dependency on membrane voltage in becoming active only on depolarization. Blockade of these sites with the drug aminophosphonovaleric acid (AP5) does not detectably affect synaptic transmission in the hippocampus, but prevents the induction of hippocampal long-term potentiation (LTP) following brief high-frequency stimulation. We now report that chronic intraventricular infusion of D,L-AP5 causes a selective impairment of place learning, which is highly sensitive to hippocampal damage, without affecting visual discrimination learning, which is not. The L-isomer of AP5 did not produce behavioural effects. AP5 treatment also suppressed LTP in vivo. These results suggest that NMDA receptors are involved in spatial learning, and add support to the hypothesis that LTP is involved in some, but not all, forms of learning.
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            Place navigation impaired in rats with hippocampal lesions.

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              Regional dissociations within the hippocampus--memory and anxiety.

              The amnestic effects of hippocampal lesions are well documented, leading to numerous memory-based theories of hippocampal function. It is debatable, however, whether any one of these theories can satisfactorily account for all the consequences of hippocampal damage: Hippocampal lesions also result in behavioural disinhibition and reduced anxiety. A growing number of studies now suggest that these diverse behavioural effects may be associated with different hippocampal subregions. There is evidence for at least two distinct functional domains, although recent neuroanatomical studies suggest this may be an underestimate. Selective lesion studies show that the hippocampus is functionally subdivided along the septotemporal axis into dorsal and ventral regions, each associated with a distinct set of behaviours. Dorsal hippocampus has a preferential role in certain forms of learning and memory, notably spatial learning, but ventral hippocampus may have a preferential role in brain processes associated with anxiety-related behaviours. The latter's role in emotional processing is also distinct from that of the amygdala, which is associated specifically with fear. Gray and McNaughton's theory can in principle incorporate these apparently distinct hippocampal functions, and provides a plausible unitary account for the multiple facets of hippocampal function.
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                Author and article information

                Journal
                Front Behav Neurosci
                Front. Behav. Neurosci.
                Frontiers in Behavioral Neuroscience
                Frontiers Research Foundation
                1662-5153
                12 March 2011
                24 June 2011
                2011
                : 5
                : 30
                Affiliations
                [1] 1simpleDepartment of Psychology and Neuroscience, University of Colorado Boulder, CO, USA
                [2] 2simpleDepartment of Psychology and Sociology, Ohio Northern University Ada, OH, USA
                [3] 3simpleResearch and Development Service, James A. Haley Veterans’ Hospital Tampa, FL, USA
                [4] 4simpleDepartment of Psychology, University of South Florida Tampa, FL, USA
                [5] 5simpleDepartment of Molecular Pharmacology and Physiology, University of South Florida Tampa, FL, USA
                [6] 6simpleCenter for Preclinical and Clinical Research on Post-traumatic Stress Disorder, University of South Florida Tampa, FL, USA
                Author notes

                Edited by: Shigeyoshi Itohara, RIKEN Brain Science Institute, Japan

                Reviewed by: Sumantra “Shona” Chattarji, National Centre for Biological Sciences, India; Thomas Mchugh, RIKEN Brain Science Institute, Japan

                *Correspondence: David M. Diamond, Department of Psychology, PCD 4118G, University of South Florida, 4202 E. Fowler Avenue, Tampa, FL 33620, USA. e-mail: ddiamond@ 123456usf.edu

                Current address: Michael B. VanElzakker, Department of Psychology, Tufts University, Medford, MA, USA.

                Article
                10.3389/fnbeh.2011.00030
                3125520
                21738501
                8092bdab-7504-46d8-ba54-c35ddc155073
                Copyright © 2011 VanElzakker, Zoladz, Thompson, Park, Halonen, Spencer and Diamond.

                This is an open-access article subject to a non-exclusive license between the authors and Frontiers Media SA, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and other Frontiers conditions are complied with.

                History
                : 14 February 2011
                : 31 May 2011
                Page count
                Figures: 6, Tables: 0, Equations: 0, References: 112, Pages: 13, Words: 11782
                Categories
                Neuroscience
                Original Research

                Neurosciences
                striatum,c-fos,amygdala,rat,hippocampus,spatial memory
                Neurosciences
                striatum, c-fos, amygdala, rat, hippocampus, spatial memory

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