Stress-Induced Out-of-Context Activation of Memory

Ježek, Karel; Lee, Benjamin B.; Kelemen, Eduard; McCarthy, Katharine M.; McEwen, Bruce S.; Fenton, André A.

doi:10.1371/journal.pbio.1000570

Cited by 19 publications

(16 citation statements)

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“…We argue that our Enemy Avoidance task is far more demanding in terms of motion planning and prediction of future positions of a punishment-associated moving object than pursuit of a visible reward-associated cue, which may be based on simple stimulus-response association learning. The control spatial cues exert over place cell firing may depend on the cognitive requirements of the behavioral task (35). Therefore, it is possible that under different circumstances, hippocampal neurons may signal positions of moving objects.…”

Section: Discussionmentioning

confidence: 99%

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Functional inactivation of the rat hippocampus disrupts avoidance of a moving object

Telenský

Svoboda²,

Blahna³

et al. 2011

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

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The hippocampus is well known for its critical involvement in spatial memory and information processing. In this study, we examined the effect of bilateral hippocampal inactivation with tetrodotoxin (TTX) in an "enemy avoidance" task. In this paradigm, a rat foraging on a circular platform (82 cm diameter) is trained to avoid a moving robot in 20-min sessions. Whenever the rat is located within 25 cm of the robot's center, it receives a mild electrical foot shock, which may be repeated until the subject makes an escape response to a safe distance. Seventeen young male Long-Evans rats were implanted with cannulae aimed at the dorsal hippocampus 14 d before the start of the training. After 6 d of training, each rat received a bilateral intrahippocampal infusion of TTX (5 ng in 1 μL) 40 min before the training session on day 7. The inactivation severely impaired avoidance of a moving robot (n = 8).No deficit was observed in a different group of rats (n = 9) that avoided a stable robot that was only displaced once in the middle of the session, showing that the impairment was not due to a deficit in distance estimation, object-reinforcement association, or shock sensitivity. This finding suggests a specific role of the hippocampus in dynamic cognitive processes required for flexible navigation strategies such as continuous updating of information about the position of a moving stimulus.cognitive map | declarative memory | episodic memory | dynamic environments R esearch into the hippocampal role in behavior and cognition is marked by a lasting dichotomy between two major views based on studies on laboratory rodents on one side and studies on human subjects or subhuman primates on the other. Electrophysiological recordings from hippocampus of freely moving rodents showed that many pyramidal neurons act as "place cells" signaling the position of the animal within an environment (1, 2). Based on these findings, the cognitive map theory (3) postulated that the hippocampus provides an allothetic spatial representation of the environment. Further support for this theory came from lesion studies showing detrimental effects of hippocampal lesions on spatial behavior (4-6). However, damage to the hippocampus and surrounding medial temporal lobe structures produce permanent anterograde amnesia for facts and autobiographical events in humans (7). Based on this evidence, the declarative memory theory presumes that the hippocampus is responsible for creating memory representations for these classes of information, which later become hippocampus-independent in a process called systems consolidation (8,9). This theory is supported by studies on recognition memory (10) and models of amnesia (11) in primates. However, the declarative memory theory does not predict lasting hippocampal involvement in some behavioral tasks such as the spatial water maze (12-16). However, the cognitive map theory does not explain hippocampal role in overtly nonspatial memory tasks (17). In a shadow of these two major theories, minor views claim that the ...

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Section: Discussionmentioning

confidence: 99%

“…Stress affects memory (35) and modulates functional connectivity between the hippocampus and the rest of the brain (36). Moreover, hippocampal lesions have been reported to have anxiolytic effect (37).…”

Section: Discussionmentioning

confidence: 99%

Functional inactivation of the rat hippocampus disrupts avoidance of a moving object

Telenský

Svoboda²,

Blahna³

et al. 2011

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

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“…However, the impact of stress on learning demonstrates a U-shaped dose dependence curve with very low or high stress-associated tasks eliciting lower performance (Sandi et al, 1997;Salehi et al, 2010). In addition to cognitive task-associated stressors, uncorrelated mild stress that temporally overlaps closely with learning paradigms also enhances hippocampal learning (Shors et al, 1992;Cordero et al, 2003;Ježek et al, 2010). Exposure to a single acute stressor (low intensity tail shock or 2 h restraint stress) prior to testing facilitates hippocampal associative learning as assessed by trace fear conditioning (Shors et al, 1992;Beylin and Shors, 2003) and contextual fear conditioning (Cordero et al, 2003;Rodríguez Manzanares et al, 2005).…”

Section: Behavioral Effects Of Acute Mild Stress Acute Mild Stress Anmentioning

confidence: 99%

“…Exposure to a single acute stressor (low intensity tail shock or 2 h restraint stress) prior to testing facilitates hippocampal associative learning as assessed by trace fear conditioning (Shors et al, 1992;Beylin and Shors, 2003) and contextual fear conditioning (Cordero et al, 2003;Rodríguez Manzanares et al, 2005). Further, exposure to mild stressors (immobilization for 15 min or 1 h but not 3 h, single forced swim stress, repeated 5 min restraint stress) also enhances consolidation and persistence of memory (Ježek et al, 2010;Parihar et al, 2011;Parfitt et al, 2012;Giachero et al, 2013). Stress-induced NE levels (Hu et al, 2007) and CRH (Blank et al, 2002) play an important role in mediating the beneficial effects of stress on cognitive function.…”

Section: Behavioral Effects Of Acute Mild Stress Acute Mild Stress Anmentioning

confidence: 99%

The adaptive and maladaptive continuum of stress responses – a hippocampal perspective

Suri

Vaidya

2015

Reviews in the Neurosciences

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AbstractExposure to stressors elicits a spectrum of responses that span from potentially adaptive to maladaptive consequences at the structural, cellular and physiological level. These responses are particularly pronounced in the hippocampus where they also appear to influence hippocampal-dependent cognitive function and emotionality. The factors that influence the nature of stress-evoked consequences include the chronicity, severity, predictability and controllability of the stressors. In addition to adult-onset stress, early life stress also elicits a wide range of structural and functional responses, which often exhibit life-long persistence. However, the outcome of early stress exposure is often contingent on the environment experienced in adulthood, and could either aid in stress coping or could serve to enhance susceptibility to the negative consequences of adult stress. This review comprehensively examines the consequences of adult and early life stressors on the hippocampus, with a focus on their effects on neurogenesis, neuronal survival, structural and synaptic plasticity and hippocampal-dependent behaviors. Further, we discuss potential factors that may tip stress-evoked consequences from being potentially adaptive to largely maladaptive.

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“…Positioning: Fundamentally Empirical I'll start with the intellectual merits of positioning by acknowledging that there is substantial and longstanding evidence in strong support of alternative ideas that the hippocampus-associated neural system is also crucial for processing the information upon which memories, relationships, and even anxiety depend, beyond and possibly independent of spatial information (Bannerman et al, 2014;Davachi and DuBrow, 2015;Dunsmoor et al, 2015;Eichenbaum and Fortin, 2009;Jezek et al, 2010;Shrager et al, 2008;Squire et al, 2007). But here there is a serious, fundamental problem-the concepts of memory, relationship, anxiety and the like are rather subjective, the demonstration and measurement of which strongly depend upon on argument and persuasion (Vanderwolf, 1998(Vanderwolf, , 2001.…”

Section: Introductionmentioning

confidence: 99%

Coordinating with the “Inner GPS”

Fenton

2015

Hippocampus

Self Cite

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The 2014 Nobel Prize for Physiology or Medicine was awarded for the discoveries that have elucidated the components of the internal positioning system that is centered on the hippocampus and entorhinal cortex. Here I provide a less than objective discussion of the importance of these accomplishments to systems neuroscience. By identifying positioning components like place, direction, distance, borders and the like, the field is given the opportunity to have a shot at piecing together how these components are integrated into the synthetic positioning sense. We are also given what is in my view, the most experimentally accessible and therefore potentially understandable, cognitive representation. Lest we feel too confident in the completeness of our understanding, and to inspire redoubled curiosity, I briefly describe a preliminary observation from our work with the psychosis-inducing drug phencyclidine (PCP). While PCP does not disturb where individual place cells fire, it dramatically discoordinates how these cells discharge together in time. Trying to understand how the positioning component cells are coordinated to provide useful knowledge is an exciting and tenable problem to be working on.

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Stress-Induced Out-of-Context Activation of Memory

Abstract: An intensely stressful experience can itself activate memories that are unrelated to the stressful experience. This previously unknown property of stress could help explain how traumatic memories become pathological.

Cited by 19 publications

References 61 publications

Functional inactivation of the rat hippocampus disrupts avoidance of a moving object

Functional inactivation of the rat hippocampus disrupts avoidance of a moving object

The adaptive and maladaptive continuum of stress responses – a hippocampal perspective

Coordinating with the “Inner GPS”

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