Effects of acute restraint stress on different components of memory as assessed by object-recognition and object-location tasks in mice

doi:10.1016/j.bbr.2011.10.007

Behavioural Brain Research

Volume 227, Issue 1, 1 February 2012, Pages 199-207

https://doi.org/10.1016/j.bbr.2011.10.007 Get rights and content

Abstract

Studies on how acute stress and the stress-related hormones affect learning and memory have yielded inconsistent findings, which might be due to some variables such as the properties of stressors, the nature of memory, the protocols for behavioral tasks and the characteristics of the subjects. However, the impacts of acute stress on different memory components have not been clearly demonstrated within one single experiment. The aim of present study was to evaluate the effects of 1-h restraint stress and the stress-induced plasma corticosterone elevation on memory acquisition, consolidation, and retrieval in mice, using object-recognition task (ORT) and object-location task (OLT) with a 4-h or 24-h intertrial interval (ITI). The results showed that, regardless of ITI, the recognition memory retrieval was significantly disrupted by acute restraint stress exposure, which started 75 min before the test session of both ORT and OLT. Acute restraint stress performed immediately after memory acquisition interrupted the consolidation of short-term recognition memories (4-h ITI) into long-term ones (24-h ITI). Moreover, the disrupted memory retrieval or consolidation was strongly related to the stress-induced plasma corticosterone elevation in a negative manner. These preliminary results clarified that acute restraint stress differently impacts three memory components, and the enhanced plasma corticosterone level under stressful situation plays critical roles in the information processing of memory under the stressful situation.

Highlights

► Acute stress impaired the retrieval of recognition memory, regardless the tasks’ intertrial interval. ► Acute stress interrupted the transferring of short-term recognition memory into long-term ones. ► The retrieval impairment of recognition memory might be associated with stress-induced corticosterone elevation. ► The interrupted short-term recognition memory consolidation to long-term one is related to corticosterone elevation.

Introduction

Stress is classically defined as a nonspecific response to any environmental stressors (both internal and external) upon the body [1] and is accompanied by various physiological, psychological and cognitive changes. Numerous research reports have shown that stress exposure has complex effects on learning and memory. However, the literature in this area lacks consistency, with studies reporting that stress can enhance, impair, or have no effect on learning and memory [2], [3], [4], [5], [6], [7], [8]. These conflicted research results could be attributed to many variables including the nature, duration or aversive levels of stressors, the nature of the task, and characteristics of the subject such as gender and age [9], [10], [11], [12], [13].

Another important issue is that acute stress and stress-related hormones may encompass different effects on various memory components. For example, while stress as well as stress-related hormones impairs memory retrieval [14], [15], [16], [17], [18], increased levels of stress hormones resulted in enhanced memory consolidation [19], [20]. Acute restraint stress plus tail-shocks disrupted animal's memory acquisition or consolidation in object-recognition task (ORT) [21]. Exposure of rodents to an elevated platform impaired memory retrieval in both ORT and object-location task (OLT) [22]. However, most of these results were obtained through separate experiments using hormones with different dosages, or using various stressors with different intensities or durations, which might have different impacts on various memory components. Therefore, it is difficult to draw an exact conclusion about the impact of the acute stress on different memory components based on these research reports. Studies utilizing one type of stressor should be preferred for further exploring the complicated interactions between acute stress and different memory components.

Several physical or psychological stressful animal models have been established to induce stress responses. Among them, restraint stress has been well accepted as an experimental model in rodents which evokes unconditioned and unavoidable neuroendocrine responses, characterized by significant elevation of peripheral plasma corticosterone [23]. Recently, Howland and Cazakoff have indicated that acute restraint stress disrupted the recognition memory retrieval [22]. However, till now, the influence of acute stress on acquisition and consolidation has not been clearly demonstrated yet.

In the present study, acute restraint stress model was utilized for testing our hypothesis that various phases of recognition memories have different response sensitivities to acute stress. Two unstressful recognition behavior paradigms, ORT and OLT [22], [24], [25] were performed to assess the effects of acute restraint stress on different components of recognition memory, and to specifically look at how the stress-induced corticosterone elevation correlated with the recognition memory components under stress condition.

Section snippets

Animals

Adult male Swiss albino mice (6–8 weeks old, weighing 18–22 g) were obtained from the Experimental Animal Center of Dalian Medical University. Animals were housed in groups under standard conditions (12 h light/dark cycle; lights on from 07:30 a.m.; 22 ± 2 °C ambient temperature; 55 ± 10% relative humidity) and were allowed to acclimatize 7 days. Mice were handled during these 7 days prior the experiments to diminish the stress caused for experimental manipulations and were fed with standard diet and

Effects of acute restraint stress on different memory components of ORT (4-h ITI)

During the sample session, all groups exhibited a comparable amount of time exploring the two identical objects (Fig. 2A, Student's t-test, Ps > 0.05). During the test session, the behavioral data analysis demonstrated that animals of all stressed groups and non-stressed control group spent greater time exploring the novel object than the familiar one (Fig. 2B, Student's t-test, Ps < 0.05). Moreover, animals in the retrieval stressed group exhibited an impaired preference for the novel object over

Discussion

Previous studies have shown inconsistent impacts on the impacts of acute stress on memory processing [2], with some studies reporting that stress impairs memory while others showing that stress enhances memory. Moreover, a close review of the literature reveals that the effects of stress depend on the memory phase that is activated during stressful situations [13]. Stress responses and increases in corticosterone levels differentially influence three components of memory: acquisition,

Conclusion

To our knowledge, this is the first study showing the effects of acute restraint stress on various phases of memory within a single study. The results indicated that acute stress disrupted the memory retrieval, interrupted the consolidation of short-term memory into long-term one. The impairment of memory components is closely associated with corticosterone elevation. These preliminary results indicated that different memory components might be differently vulnerable to acute restraint stress

Acknowledgement

This work was supported by the China Fundamental Research Funds for the Central Universities (DUT11SM03), the grant from National Science Foundation of China (NSFC, 60971096) and the grant from National Basic Research Program of China (973 program, 2012CB518200).

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¹: These two authors contribute equally to this work.

²: During the behavioral tests, Wei Wang was a PhD student in Dalian University of Technology, and now she is a member of Affiliated Zhongshan Hospital of Dalian University.

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Research reportEffects of acute restraint stress on different components of memory as assessed by object-recognition and object-location tasks in mice

Abstract

Highlights

Introduction

Section snippets

Animals

Effects of acute restraint stress on different memory components of ORT (4-h ITI)

Discussion

Conclusion

Acknowledgement

Prog Neuropsychopharmacol Biol Psychiatry

Life Sci

Trends Cogn Sci

Acta Psychol (Amsterdam)

Neurobiol Learn Mem

Neurobiol Learn Mem

J Neuroimmunol

Neurobiol Learn Mem

Physiol Behav

Life Sci

Psychoneuroendocrinology

Neurosci Biobehav Rev

Brain Res Bull

Curr Opin Neurobiol

Neurosci Biobehav Rev

Neurosci Biobehav Rev

Horm Behav

Brain Res Rev

Behav Brain Res

Psychoneuroendocrinology

Behav Neural Biol

Neurobiol Learn Mem

J Neurosci Methods

Behav Brain Res

Behav Brain Res

Behav Brain Res

A syndrome produced by diverse nocuous agents

Nature

The relationship between acute glucocorticoid levels and hippocampal function depends upon task aversiveness and memory processing stage

Nonlinearity Biol Toxicol Med

Competitive interactions between endogenous LTD and LTP in the hippocampus underlie the consolidation of emotional memories and stress-induced amnesia

Hippocampus

Impairment of the spatial learning and memory induced by learned helplessness and chronic mild stress

Pharmacol Biochem Behav

Hormetic influence of glucocorticoids on human memory

Nonlinearity Biol Toxicol Med

Memory—a century of consolidation

Science

Stress and memory: behavioral effects and neurobiological mechanisms

Neural Plast

Research report
Effects of acute restraint stress on different components of memory as assessed by object-recognition and object-location tasks in mice