Post-encoding Stress Research Articles

When stress enhances memory encoding: The beneficial effects of changing context

The effects of acute stress on memory encoding are complex, and we do not yet know all of the conditions that can determine whether stress at encoding improves or impairs memory. Recent work has found that changing contexts between encoding and stress can abolish the effects of post-encoding stress on memory, suggesting that context may play an important role in the effects of stress on memory. However, the role of context in the effects of stress on memory encoding is not yet known. We addressed this gap by examining the effects of context on the influence of acute stress on memory encoding. In a 2 × 2 experimental design, participants (N = 103) completed either a stressor (i.e., Socially Evaluated Cold Presser Test) or control task (i.e., warm water control) before completing a memory encoding task, which occurred in either in the same room as or a different room from the stressor or control task. Memory retrieval was tested for each participant within the context that they completed the encoding task. We found that, relative to nonstressed (i.e., control) participants, stressed participants who switched contexts prior to encoding showed better memory for both negative and neutral images. In contrast, when the stressor or control task occurred in the same room as memory encoding, stress had no beneficial effect on memory. These results highlight the importance of the ongoing context as a determinant of the effects of stress on memory encoding and present a challenge to current theoretical accounts of stress and memory.

A single brief stressful event time-dependently affects object recognition memory and promotes familiarity preference in marmoset monkeys

A stressful experience can enhance information storage and impair memory retrieval in the rodent novel object recognition (NOR) task. However, recent conflicting results underscore the need for further investigation. Nonhuman primates may provide a unique, underexplored and more translational means to investigate stress-mediated changes in memory. Therefore, we assessed whether a single brief extrinsic stress event affects information encoding, storage and/or retrieval in adult marmoset monkeys submitted to the NOR task. This consisted of an initial 10 min familiarization period with two identical neutral objects. After a 6 h delay, a 10 min test trial was held where a new and familiar object could be explored. Stress was induced by a 15 min restraint event held before or after the encoding phase, or prior to retrieval. Pre-encoding stress had no effect on task performance, as this group displayed above-chance novelty preference similar to non-stressed controls. Post-encoding stress induced memory deficits, with both objects being explored equally. Interestingly, pre-retrieval stress induced an above-chance familiarity preference. A single brief stressful event thus affects recognition memory in a time-dependent manner. Also, negative discrimination ratios can be used as a measure of memory in the NOR task and a change in strategy may not mean memory failure in spontaneous learning paradigms.

The effects of psychosocial stress on item, cued-pair and emotional memory.

Physical stress, such as from the cold-pressor test, has been robustly associated with altered memory retrieval, but it is less clear whether the same happens following psychosocial stress. Studies using psychosocial stressors report mixed effects on memory, leading to uncertainty about the common cognitive impact of both forms of stress. The current study uses a series of four carefully designed experiments, each differing by only a single critical factor to determine the effects of psychosocial stress on specific aspects of episodic memory. In three experiments, we induced psychosocial stress after participants encoded words, then assessed retrieval of those words after a prolonged delay. These experiments found no effect of post-encoding stress on recognition of neutral words or cued recall of word-pairs, but a small effect on recollection of semantically related words. There were, however, positive relationships within the stress group between measures of stress (cortisol in experiment 1 and self-reported-anxiety in experiment 3) and recollection of single word stimuli. In the fourth experiment, we found that psychosocial stress immediately before retrieval did not influence word recognition. Recollection, particularly for semantically related stimuli, may therefore be more susceptible to the effects of psychosocial stress, and future studies can assess how this relates to other forms of stress. Overall, our findings suggest that the effects of psychosocial stress on episodic memory may be more subtle than expected, warranting further exploration in larger studies.

Post-Encoding Stress Does Not Enhance Memory Consolidation: The Role of Cortisol and Testosterone Reactivity.

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.

Stress-Induced Increase in Cortisol Negatively Affects the Consolidation of Contextual Elements of Episodic Memories.

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.

Determining the biological associates of acute cold pressor post-encoding stress effects on human memory: The role of salivary interleukin-1β

Stress generally hurts many aspects of memory, but an interesting finding to emerge from the stress and memory literature is that stress that occurs shortly after learning (i.e., post-encoding stress) usually benefits memory. Although this effect is well established, the biological mechanisms underpinning this effect are not—especially in humans. We addressed this gap in the present study by collecting saliva samples from 80 participants who were randomized to a post-encoding stress (i.e., cold pressor for 3 min) or control task (i.e., warm water for 3 min) and 48 h later completed a recognition memory task. Saliva was collected both prior to and 15 min after the offset of (18 min after the onset of) the stress/control manipulation. Drawing on animal and human work, we examined how five stress-responsive biomarkers—cortisol, salivary α-amylase, progesterone, estradiol, and the proinflammatory cytokine interleukin (IL)-1β, all assessed in saliva—related to the effects of stress on memory. We found that stress enhanced recollection of negative images and that these effects were selectively related to salivary IL-1β. Moreover, we found that the beneficial effects of stress on memory were statistically mediated by salivary IL-1β. We found no robust associations—either linear or quadratic—between memory and any other biomarker, nor did we find significant interactions between biomarkers in predicting memory. These results suggest that immune system activity indexed by salivary IL-1β may play an important role in contributing to post-encoding stress effects on human memory.

Stress and the medial temporal lobe at rest: Functional connectivity is associated with both memory and cortisol

When acute stress is experienced immediately after memory encoding (i.e., post-encoding stress) it can significantly impact subsequent memory for that event. For example, recent work has suggested that post-encoding stress occurring in a different context from encoding impairs memory. However, the neural processes underlying these effects are poorly understood. We aimed to expand this understanding by conducting an analysis of resting functional connectivity in the period following post-encoding stress that occurred in a different context than encoding, using seed regions in the medial temporal lobes known for their roles in memory. In the current study of 44 males randomized to stress (n = 23) or control (n = 21) groups, we found that stress increased cortisol, impaired recollection of neutral materials, and altered functional connectivity with medial temporal lobe regions. Although stress did not significantly alter hippocampus-amygdala functional connectivity, relative to participants in the control group, participants in the post-encoding stress group showed lower functional connectivity between the hippocampus and a region with a peak in the superior temporal gyrus. Across participants in both groups, functional connectivity between these regions was related to greater increases in cortisol, and it was also inversely related to recollection of neutral materials. In contrast, the stress group showed greater parahippocampal cortex functional connectivity with a region in the left middle temporal gyrus than the control group. Moreover, greater functional connectivity between the parahippocampal cortex and the observed cluster in the middle temporal gyrus was associated with greater cortisol changes from pre- to post-manipulation, but was not related to differences in memory. The results show that post-encoding stress can alter the resting-state functional connectivity between the medial temporal lobe and neocortex, which may help explain how stress impacts memory.

ISPNE Award Plenary: Lifetime Achievement Award Address: Time: Thursday, 06/Sep/2018: 4:30pm–5:15pm

When acute stress is experienced immediately after memory encoding (i.e., post-encoding stress) it can significantly impact subsequent memory for that event. For example, recent work has suggested that post-encoding stress occurring in a different context from encoding impairs memory. However, the neural processes underlying these effects are poorly understood. We aimed to expand this understanding by conducting an analysis of resting functional connectivity in the period following post-encoding stress that occurred in a different context than encoding, using seed regions in the medial temporal lobes known for their roles in memory. In the current study of 44 males randomized to stress (n = 23) or control (n = 21) groups, we found that stress increased cortisol, impaired recollection of neutral materials, and altered functional connectivity with medial temporal lobe regions. Although stress did not significantly alter hippocampus-amygdala functional connectivity, relative to participants in the control group, participants in the post-encoding stress group showed lower functional connectivity between the hippocampus and a region with a peak in the superior temporal gyrus. Across participants in both groups, functional connectivity between these regions was related to greater increases in cortisol, and it was also inversely related to recollection of neutral materials. In contrast, the stress group showed greater parahippocampal cortex functional connectivity with a region in the left middle temporal gyrus than the control group. Moreover, greater functional connectivity between the parahippocampal cortex and the observed cluster in the middle temporal gyrus was associated with greater cortisol changes from pre- to post-manipulation, but was not related to differences in memory. The results show that post-encoding stress can alter the resting-state functional connectivity between the medial temporal lobe and neocortex, which may help explain how stress impacts memory.

Post-encoding stress produces memory- and cortisol-related changes in functional connectivity with the hippocampus and parahippocampal cortex

Post-encoding stress produces memory- and cortisol-related changes in functional connectivity with the hippocampus and parahippocampal cortex

Using acute stress to improve episodic memory: The critical role of contextual binding.

Previous research has shown that encountering a brief stressor shortly after learning can be beneficial for memory. Recent studies, however, have shown that post-encoding stress does not benefit all recently encoded memories, and an adequate theoretical account of these effects remains elusive. The current study tested a contextual binding account of post encoding stress by examining the effect of varying the context in which the stressor was experienced. Participants encoded a mixture of negative and neutral images, immediately followed by a stressor (i.e., socially evaluated cold pressor) or a non-stress control task. Half of the participants received the stress/control manipulation in the same context as the study materials and half were moved to another context (i.e., a different room with a different experimenter). Two days later all participants returned to the original study room and received a recognition memory test. The results indicated that stress increased recognition memory only when the stressor occurred in the same context as the study materials, whereas stress did not benefit memory if the stressor occurred in a different context. Moreover, stress related increases in salivary cortisol were related to increases in memory when the stressor occurred in the same context as the study materials but not when the context changed. Similar effects were observed for negative and neutral materials and for males and females. These results are consistent with a contextual binding account and suggest that stress acts on memory by enhancing the encoding of the ongoing context of the stressor which benefits memory for the immediately preceding events that share the same context.

Acute stress throughout the memory cycle: Diverging effects on associative and item memory.

Acute stress can modulate memory for individual parts of an event (items), but whether it similarly influences memory for associations between items remains unclear. We used a within-subjects design to explore the influence of acute stress on item and associative memory in humans. Participants associated negative words with neutral objects, rated their subjective arousal for each pair, and completed delayed item and paired associative recognition tasks. We found strikingly different patterns of acute stress effects on item and associative memory: for high-arousal pairs, preencoding stress enhanced associative memory, whereas postencoding stress enhanced item memory. Preretrieval stress consistently impaired both forms of memory. We found that the influence of stress-induced cortisol also varied, with a linear relationship between cortisol and item memory but a quadratic relationship between cortisol and associative memory. These findings reveal key differences in how stress, throughout the memory cycle, shapes our memories for items and associations. (PsycINFO Database Record (c) 2018 APA, all rights reserved).

Post-encoding stress enhances mnemonic discrimination of negative stimuli.

Stress influences how we remember emotional events and how these events shape future behaviors. However, the impact of stress on memory specificity for emotional events has yet to be examined. To this end, the present study utilized a mnemonic discrimination task that taxes hippocampal pattern separation, the process of distinguishing between overlapping experiences, thereby allowing us to better understand the mechanisms by which stress affects gist versus detail memory of emotional events. Participants encoded scenes composed of negative or neutral objects placed on neutral backgrounds and then underwent a psychosocial stressor or matched control task. Twenty-four hours later during testing, objects were presented separately, with some identical old objects (targets), some new objects (foils), and some similar but not identical objects (lures). Target recognition was enhanced for negative compared to neutral objects in both the stress and control groups. Interestingly, post-encoding stress selectively enhanced mnemonic discrimination of negative versus neutral objects, which was not the case in the control group. Measures of salivary cortisol revealed a quadratic inverted U relationship between negative mnemonic discrimination and cortisol increase. These findings suggest that moderate cortisol release following stress is associated with enhanced memory precision for negative information.

The effects of post-encoding stress and glucocorticoids on episodic memory in humans and rodents

It is now well established that acute stress shortly after encoding (i.e., post-encoding stress) can benefit episodic memory. In the current paper, we briefly review the human literature examining the effects of post-encoding stress on episodic memory, and we relate that literature to studies of post-encoding manipulations of cortisol in humans, as well as studies of post-encoding stress and administration of corticosterone on analogous memory tasks in rodents. An examination of the literature reveals several important gaps in our understanding of stress and memory. For example, although the human literature shows that post-encoding stress generally improves memory, these effects are not observed if stress occurs in a different context from learning. Moreover, the rodent literature shows that post-encoding stress generally impairs memory instead of improving it, and these effects depend on whether the animal is habituated to the learning context prior to encoding. Although many aspects of the results support a cellular consolidation account of post-encoding stress, we present possible modifications, such as a network reset, to better account for the data. We also suggest that it is important to incorporate ideas of contextual binding in order to understanding the effects of post-encoding stress and glucocorticoids on memory.

The effects of acute stress on episodic memory: A meta-analysis and integrative review.

A growing body of research has indicated that acute stress can critically impact memory. However, there are a number of inconsistencies in the literature, and important questions remain regarding the conditions under which stress effects emerge as well as basic questions about how stress impacts different phases of memory. In this meta-analysis, we examined 113 independent studies in humans with 6,216 participants that explored effects of stress on encoding, postencoding, retrieval, or postreactivation phases of episodic memory. The results indicated that when stress occurred prior to or during encoding it impaired memory, unless both the delay between the stressor and encoding was very short and the study materials were directly related to the stressor, in which case stress improved encoding. In contrast, postencoding stress improved memory unless the stressor occurred in a different physical context than the study materials. When stress occurred just prior to or during retrieval, memory was impaired, and these effects were larger for emotionally valenced materials than neutral materials. Although stress consistently increased cortisol, the magnitude of the cortisol response was not related to the effects of stress on memory. Nonetheless, the effects of stress on memory were generally reduced in magnitude for women taking hormonal contraceptives. These analyses indicate that stress disrupts some episodic memory processes while enhancing others, and that the effects of stress are modulated by a number of critical factors. These results provide important constraints on current theories of stress and memory, and point to new questions for future research. (PsycINFO Database Record

Stress as a mnemonic filter: Interactions between medial temporal lobe encoding processes and post-encoding stress.

Acute stress has been shown to modulate memory for recently learned information, an effect attributed to the influence of stress hormones on medial temporal lobe (MTL) consolidation processes. However, little is known about which memories will be affected when stress follows encoding. One possibility is that stress interacts with encoding processes to selectively protect memories that had elicited responses in the hippocampus and amygdala, two MTL structures important for memory formation. There is limited evidence for interactions between encoding processes and consolidation effects in humans, but recent studies of consolidation in rodents have emphasized the importance of encoding "tags" for determining the impact of consolidation manipulations on memory. Here, we used functional magnetic resonance imaging in humans to test the hypothesis that the effects of post-encoding stress depend on MTL processes observed during encoding. We found that changes in stress hormone levels were associated with an increase in the contingency of memory outcomes on hippocampal and amygdala encoding responses. That is, for participants showing high cortisol reactivity, memories became more dependent on MTL activity observed during encoding, thereby shifting the distribution of recollected events toward those that had elicited relatively high activation. Surprisingly, this effect was generally larger for neutral, compared to emotionally negative, memories. The results suggest that stress does not uniformly enhance memory, but instead selectively preserves memories tagged during encoding, effectively acting as mnemonic filter. © 2016 Wiley Periodicals, Inc.

Effects of post-encoding stress on performance in the DRM false memory paradigm.

Numerous studies have investigated how stress impacts veridical memory, but how stress influences false memory formation remains poorly understood. In order to target memory consolidation specifically, a psychosocial stress (TSST) or control manipulation was administered following encoding of 15 neutral, semantically related word lists (DRM false memory task) and memory was tested 24 h later. Stress decreased recognition of studied words, while increasing false recognition of semantically related lure words. Moreover, while control subjects remembered true and false words equivalently, stressed subjects remembered more false than true words. These results suggest that stress supports gist memory formation in the DRM task, perhaps by hindering detail-specific processing in the hippocampus.

Differential effects of stress-induced cortisol responses on recollection and familiarity-based recognition memory

Stress-induced changes in cortisol can impact memory in various ways. However, the precise relationship between cortisol and recognition memory is still poorly understood. For instance, there is reason to believe that stress could differentially affect recollection-based memory, which depends on the hippocampus, and familiarity-based recognition, which can be supported by neocortical areas alone. Accordingly, in the current study we examined the effects of stress-related changes in cortisol on the processes underlying recognition memory. Stress was induced with a cold-pressor test after incidental encoding of emotional and neutral pictures, and recollection and familiarity-based recognition memory were measured one day later. The relationship between stress-induced cortisol responses and recollection was non-monotonic, such that subjects with moderate stress-related increases in cortisol had the highest levels of recollection. In contrast, stress-related cortisol responses were linearly related to increases in familiarity. In addition, measures of cortisol taken at the onset of the experiment showed that individuals with higher levels of pre-learning cortisol had lower levels of both recollection and familiarity. The results are consistent with the proposition that hippocampal-dependent memory processes such as recollection function optimally under moderate levels of stress, whereas more cortically-based processes such as familiarity are enhanced even with higher levels of stress. These results indicate that whether post-encoding stress improves or disrupts recognition memory depends on the specific memory process examined as well as the magnitude of the stress-induced cortisol response.

Cold-pressor stress after learning enhances familiarity-based recognition memory in men

Stress that is experienced after items have been encoded into memory can protect memories from the effects of forgetting. However, very little is known about how stress impacts recognition memory. The current study investigated how an aversive laboratory stressor (i.e., the cold-pressor test) that occurs after information has been encoded into memory affects subsequent recognition memory in an immediate and a delayed test (i.e., 2-h and 3-month retention interval). Recognition was assessed for negative and neutral photographs using a hybrid remember/know confidence procedure in order to characterize overall performance and to separate recollection- and familiarity-based responses. The results indicated that relative to a non-stress control condition, post-encoding stress significantly improved familiarity but not recollection-based recognition memory or free recall. The beneficial effects of stress were observed in males for negative and neutral materials at both immediate and long-term delays, but were not significant in females. The results indicate that aversive stress can have long-lasting beneficial effects on the memory strength of information encountered prior to the stressful event.

The effects of post-encoding stress on recognition memory: Examining the impact of skydiving in young men and women

Prior studies have indicated that post-encoding stress can protect memories from the effects of forgetting, and this has been taken as evidence that stress facilitates memory consolidation. However, it is not known whether stress acts by directly influencing the strength of the underlying memories or whether it influences the generation process that plays a critical role in tests such as free recall. To address this issue, we examined the effects of stress produced by skydiving on recognition memory for negative and neutral pictures. Relative to a non-stress control condition, post-encoding stress in males was found to increase recognition memory for neutral pictures. However, stress was not found to improve recognition for emotional pictures, nor was it found to influence recognition memory in female participants. Additional analysis of recognition performance suggested that stress increased familiarity-based recognition rather than recollection. This study indicates that stress can improve familiarity-based recognition, thus showing that stress directly increases the strength of the underlying memories.