The present experiment combined three experimental procedures — a retrieval-practice learning manipulation, a list-discrimination task, and a stress-induction technique — to examine the influences of different learning strategies and acute stress on multiple measures of episodic memory.
Prior research demonstrated that learning information via retrieval practice, which entails studying and taking practice tests, resulted in less memory impairment under stress than learning information via repeated studying. The present experiment combined three experimental procedures to further examine the memory mechanisms underlying the efficacy of retrieval practice in the context of stress. A list-discrimination task was implemented, in which participants learned two distinct wordlists. This was combined with a retrieval-practice manipulation, as half of the participants engaged in practice testing and half engaged in conventional studying during learning. A week later, participants underwent stress induction, using the Trier Social Stress Test. Before and after stress induction, participants completed tests of item and source memory (i.e., list discrimination). The combination of these three procedures yielded informative results: retrieval practice, in the context of stress, improved item memory but not source memory relative to conventional studying. Limitations and future directions for the use of this methodology are discussed.
Instances of acute psychological stress generally impair memory retrieval1. For instance, performing a high-pressure public-speaking task reduces the amount of information that individuals can subsequently remember2,3,4,5,6. This common finding is largely attributed to the neural influence of the human stress hormone cortisol. When cortisol levels are heightened after stress, cortisol binds to glucocorticoid receptors in the hippocampus7,8, impairing recollection of previously-learned information9.
In recent research, the detrimental effects of stress on memory retrieval were eliminated when participants studied stimuli using the highly-effective learning strategy retrieval practice10. Participants either learned a wordlist via repeated studying, or via studying followed by several attempts at freely recalling the words (i.e., retrieval practice). A day later, when memory was tested after stress induction, those who learned via repeated studying remembered fewer words than their non-stressed counterparts, whereas those who learned via repeated testing showed no memory impairment.
To better understand why retrieval practice so effectively buffered memory against the deleterious effects of acute stress, it is helpful to take a closer look at the memory processes being affected. The prior study simply examined item memory by having participants recall the words that they had learned10. In the present study, source memory was more carefully examined to determine whether retrieval practice was also supporting memory for the context in which each item was learned. This approach was informed by research showing that retrieval practice increases memory for contextual information associated with a given learning episode (e.g., when each item was learned, where each item was learned)11.
To determine how retrieval practice interacts with acute stress to influence both item and source memory, it was necessary to combine three experimental procedures. First, a standard retrieval-practice manipulation was implemented in which participants either studied stimuli several times or engaged in studying followed by free recall. Second, a list-discrimination task was used to separately examine item and source memory. This involved having participants learn stimuli from two temporally-segregated and color-coded lists that could be differentiated on a later memory test. Third, a commonly-used method of psychological stress induction was used, in which participants must give a short speech and solve math problems while being judged12.
This research was conducted in accordance with current American Psychological Association (APA) professional ethical standards and was approved by the Tufts University Social, Behavioral & Educational Research Institutional Review Board.Â
NOTE: The experiment reported in the present manuscript was previously published elsewhere13.
1. Participant Recruitment, Screening, and Scheduling
2. Construction of Stimuli and Memory Tests
3. Stress-induction Protocol
4. Saliva Sample Collection and Supplies
NOTE: Saliva collection is only necessary during experimental session 2, in which stress is induced
5. Subjective Stress Measure
6. Encoding Procedure (Experimental Session 1)
7. Retrieval Procedure (Experimental Session 2)
8. Computing Dependent Measures
Efficacy of the retrieval-practice manipulation
Note that the following analyses were previously published by Smith et al.13. During encoding in experimental session 1, free recall of the words from each wordlist was relatively low for individuals in the retrieval-practice group. These individuals recalled, on average, 14 of 60 items and 13 of 60 items during their recall attempts for the first list. They recalled, on average, 16 of 60 items and 15 of 60 items during their recall attempts for the second list.
Of note is the fact that retrieval practice is only beneficial as a learning technique if the retrieval-practice attempts that one makes are successful. That is, an individual must successfully retrieve the studied information during their retrieval-practice attempts to experience any subsequent memory benefits. For example, an individual who recalls only 5 of 60 items during their retrieval-practice attempts would not show exceptional memory performance on a later test, while an individual who recalls 55 of the items likely would. Therefore, hit proportions on the final recognition tests for individuals in the retrieval-practice group were restricted to items that they accurately recalled at least once during session 1, in order to meaningfully examine the benefits of retrieval practice.
Using this restriction, the retrieval-practice group demonstrated higher hit proportions on the session 2 recognition tests than those in the study-practice group, as expected [F(1, 60) = 80.34, p < 0.001, ηp2 = 0.57]. Individuals in the retrieval-practice group demonstrated average hit rates of 0.91 (standard error of the mean [SEM] = 0.02) and 0.91 (SEM = 0.01) on the pre- and post-stress tests (respectively), whereas those in the SP group had average hit proportions of 0.66 (SEM = 0.02) and 0.66 (SEM = 0.03).
Efficacy of the list-discrimination task
To determine whether performance on the list-discrimination task was due to participants’ ability to discriminate between items learned on the two lists or was simply due to guessing, source memory scores were compared to chance levels of performance (i.e., 50% accuracy). Participants in the study-practice group exhibited above-chance levels of discrimination on both the pre- and post-stress recognition tests [pre-stress test: t(29) = 3.14, p = 0.004; post-stress test: t(29) = 2.78, p = 0.009]13. However, those in the retrieval-practice group demonstrated chance levels of performance on both tests [pre-stress test: t(31) = 0.76, p = 0.452; post-stress test: t(31) = 1.50, p = 0.144]13. Note that participants had accurately recalled these items at least once during their session-1 free-recall attempts, but still demonstrated chance levels of performance.
Efficacy of the stress-induction procedure
As shown in Figure 3, the modified version of the TSST-G used in the present protocol effectively induced both psychological stress and physiological stress. Participants demonstrated post-stress increases in STICSA scores [F(1, 60) = 25.93, p < 0.001, ηp2 = 0.30] and cortisol levels [F(2, 116) = 3.75, p = 0.026, ηp2 = 0.06]. Across the three measures of cortisol, participants demonstrated marked increases from baseline to 25 min post-stress [t(59) = 1.97, p = 0.027, Cohen’s d = 0.25] and from 12 min post-stress to 25 min post-stress [t(59) = 2.16, p = 0.018, Cohen’s d = 0.28]. Cortisol levels did not significantly increase from baseline to 12 min post-stress [t(59) = 1.24, p = 0.110].
Putting it all together: the influence of stress and retrieval practice on item and source memory
Across the measures of item memory, the combination of stress and retrieval practice generally produced the best performance on the session-2 recognition tests. The retrieval-practice group demonstrated a positive relationship between delta cortisol and hit proportions [r(31) = 0.41, p = 0.023], whereas the study-practice group did not [r(27) = -0.17, p = 0.384]. As depicted in Figure 4, the retrieval-practice group also demonstrated the lowest false-alarm proportions, but only on the post-stress test [F(1, 60) = 4.10, p = 0.047, ηp2 = 0.06]. Last, whereas gamma correlations were generally at chance levels for list-discrimination, the post-stress gamma value for the retrieval-practice group was the only value to exceed chance-level performance [t(31) = 3.03, p = 0.005, d = 0.54]. This reflects participants' awareness of which items they correctly and incorrectly assigned to red and blue lists.
In contrast, source memory was unaffected by stress and, as noted above, individuals in the retrieval-practice group demonstrated chance-level performance (Figure 4). Despite correctly remembering 91% of the items that they correctly recalled during free-recall in session 1, individuals in the retrieval-practice group could not accurately remember whether these items came from the red or the blue list.
Figure 1: Graphic simulation of the encoding procedure during session 1. The stimuli depicted are representative of the two 60-item lists of stimuli. Please click here to view a larger version of this figure.
Figure 2: Graphic simulation of the recognition test and accompanying list-discrimination questions and confidence judgments. Each recognition question is presented individually, followed by a prompt to indicate which list the item came from and how confident the participant is in that judgment. Ninety items are presented in this manner on each recognition test (see section 2.3). Please click here to view a larger version of this figure.
Figure 3: Evidence of the efficacy of the TSST stress-induction procedure. Stress increased subjective anxiety, as measured by the STICSA (A), and also increased salivary cortisol levels relative to baseline (B). Error bars represent SEM. *p < 0.05, ***p < 0.001. This figure has been modified from Smith et al.13. Please click here to view a larger version of this figure.
Figure 4: Evidence that the combination of stress and retrieval practice improved item memory (A) but not source memory (B). Error bars represent SEM. *p < 0.05. This figure has been modified from Smith et al.13. Please click here to view a larger version of this figure.
Episodic memories are associated with contextual information. To gain a deeper understanding of how psychological stress and different learning strategies influence episodic memory, it is important to consider how these variables influence the contextual elements of memory. The context associated with a memory (e.g., where the memory was acquired, when it was acquired) could be examined in infinitely-many ways. The present protocol took a step forward in examining memory for context with the use of a list-discrimination task, which assesses the source of a given memory. The novel combination of a list-discrimination task with stress induction and a retrieval-practice encoding manipulation allowed for a test of the memory mechanisms underlying the efficacy of retrieval practice for buffering memory against acute stress10.
Future researchers may consider modifying the retrieval-practice manipulation employed in the present protocol. As stated in the Results, participants in the retrieval-practice group only recalled about 25% of wordlist items during their free-recall attempts in session 1. This low level of performance is not optimal either experimentally or practically, although the hit-proportion restriction used in the present protocol did allow for meaningful examination of the efficacy of retrieval practice. For consistency with previous literature10, the present protocol required that the retrieval-practice group simply study each wordlist once and then make free-recall attempts without subsequent feedback or re-exposure to the stimuli. However, research suggests that retrieval practice results in more robust learning when participants are given feedback about their performance during the retrieval-practice attempts24 and when participants are re-exposed to the stimuli between each retrieval-practice attempt25. Thus, a more effective retrieval-practice manipulation may involve multiple cycles of studying, free-recall testing, and feedback regarding correctness.
The list-discrimination procedure employed in the present experiment was only somewhat effective, given that some participants demonstrated chance-level performance. This task was borrowed from previous research, in which source memory was tested within minutes of the wordlist encoding procedure26,27. The one-week delay between encoding and memory testing that was implemented in the present protocol may have contributed to the observed chance-level list-discrimination performance. Thus, to improve list-discrimination performance so that any effects of stress and retrieval practice may become more apparent, future researchers may consider shortening the retention interval between encoding and testing. However, the one-week interval used in the present protocol may be desirable because it mimics more realistic circumstances (e.g., learning information today and recalling it a week from now). To maintain this delay but improve participants'Â ability to discriminate between items learned from the two wordlists, researchers may consider making the two encoding episodes (i.e., learning the two wordlists) more distinct. As examples, encoding of the two wordlists could be separated by a longer interval of time or the wordlists could be encoded in different physical locations.
In addition to the limitations of the retrieval-practice and list-discrimination protocols, the stress-induction procedure used in the present experiment demonstrated limited efficacy. Participants showed only a moderate increase in cortisol across the three measurements. Because this exact method of stress-induction has successfully induced stronger stress responses in previous experiments28,29, the present results are likely due to sample differences rather than an ineffective paradigm. Women, particularly those taking oral contraceptives, often demonstrate a blunted cortisol response to acute stressors15. The present study recruited a largely-female sample (73% female), which may have contributed to lower post-stress cortisol at the group level. There are several options for controlling for this issue. Future researchers may choose to recruit a male-only sample30, include sex as an independent variable in statistical analyses4, or include contraceptive use and menstrual-cycle phase as variables in analyses on cortisol1. However, these options require additional considerations. The first limits the generalizability of findings, and the second and third require larger sample sizes to account for the addition of variables to the statistical model.
Some additional methodological changes should be considered. First, to better map the post-stress increase in cortisol and subsequent recovery period, researchers should collect more saliva samples. For example, some researchers opt to collect samples every 5-10 min after the onset of stress for up to one hour after stress induction31. Second, researchers may consider manipulating stress between-subjects. In the present repeated-measures design, issues such as participant fatigue could confound the effects of stress that were observed. A between-subjects design with a non-stressed control group would eradicate these potential issues. Additionally, the act of retrieving items on the pre-stress test may have imparted retrieval-practice benefits on the post-stress test, effectively reducing the benefits of the retrieval-practice encoding manipulation. A between-subjects manipulation of stress, featuring only one memory test (post-stress), would eliminate this potential issue. Third, researchers should consider the emotional impact of the distractor task implemented between stress induction and memory testing during session 2. Having participants watch a sitcom (i.e., The Office) may induce a positive mood. Including a post-sitcom measure of participants'Â mood states would provide a more precise understanding of how mood and physiological stress influence subsequent memory performance. As a final note, an additional baseline measure of state anxiety should be added to the beginning of session 1 in the present protocol. To examine if study practice and retrieval practice differentially impact anxiety levels during session-1 encoding, this initial measure is necessary for comparison to the measure that is taken at the end of session 1.
The present protocol employed a novel combination of three experimental procedures — a retrieval-practice manipulation, a list-discrimination task, and the TSST stress-induction technique — to examine one potential memory mechanism underlying the effectiveness of retrieval practice at creating stress-resistant memories. The results of this methodology showed that, in the context of stress, retrieval practice improved memory for the items that were learned but did not improve memory for the source of the items. These findings speak to the efficacy of combining these procedures to investigate questions related to retrieval practice, the contextual elements of episodic memory, and/or acute psychological stress. Future research examining questions related to one or more of these topics should consider using these techniques, but with attention given to the modifications outlined above.
This work was funded by the U.S. Army Combat Capabilities Development Command (CCDC) Soldier Center. The views expressed in this article are solely those of the authors and do not reflect the official policies or positions of the U.S. Army, the Department of Defense, or any other department or agency of the U.S. government. The authors thank Abbie Gantner for her assistance with data collection.
Name | Company | Catalog Number | Comments |
Blank paper | N/A | N/A | Paper is given to participants for speech preparation during stress induction |
Clipboard equipped with blank sheets of paper and a list of 50 math subtraction tasks with answers (e.g., 4782 - 17). | N/A | N/A | The experimenter holds the clipboard during stress induction. (S)he takes notes on the blank paper during participants' speeches, and refers to the math problems for the math-subtraction portion of stress induction. |
Computers (two) | N/A | N/A | Necessary for presenting stimuli, administering memory tests, and recording participants' responses. |
Crovial storage box (recommended) | N/A | N/A | Helpful for storing saliva samples until the time of analysis. |
Cryovials (2 mL) | N/A | N/A | Needed for collection of saliva samples for cortisol analysis. The present paradigm required three cryovials per participant. |
Cubicle desks with chairs (two of each) | N/A | N/A | Cubicles are helpful for limiting distractions during encoding and memory testing. |
Freezer | N/A | N/A | Needed for storing saliva samples until the time of analysis. Freezer must maintain a temperature of approximately 0 degrees fahrenheit. |
Smoothie-sized straws | N/A | N/A | Helpful for passing saliva from the mouth into each cryovial. |
Stimulus presentation software (recommended) | E-Prime 3.0 (recommended) | Helpful for precision in stimulus presentation (e.g., 2 s presentation rate for words during experimental session 1) and video presentation (e.g., Planet Earth during session 1). Also helpful for administration of recognition tests and recording participant responses (session 2). | |
The State Trait Inventory for Cognitive and Somatic Anxiety | N/A | N/A | Necessary for assessing subjective stress. Borrowed from Grös, Antony, Simms, and McCabe (2007). |
Video camera with tripod | N/A | N/A | Necessary for stress-induction procedure. Camera needs to appear to record participants, but does not need to be capable of recording. |
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