Enhanced human memory consolidation with post-learning stress: interaction with the degree of arousal at encoding

Abundant evidence indicates that endogenous stress hormones such as epinephrine and corticosterone modulate memory consolidation in animals. We recently provided the first demonstration that an endogenous stress hormone (epinephrine) can enhance human memory consolidation. However, these findings also suggested that post-learning stress hormone activation does not uniformly enhance memory for all recently acquired information; rather, that it interacts with the degree of arousal at initial encoding of material in modulating memory for the material. Here we tested this hypothesis by administering cold pressor stress (CPS) or a control procedure to subjects after they viewed slides of varying emotional content, and assessing memory for the slides 1 wk later. CPS, which significantly elevated salivary cortisol levels, enhanced memory for emotionally arousing slides compared with the controls, but did not affect memory for relatively neutral slides. These findings further support the view that post-learning stress hormone-related activity interacts with arousal at initial encoding to modulate memory consolidation.     

Serial position phenomena: Training and retrieval effects

With successive free recall lists primacy items are usually among the first to be reported on the initial list. Recency items will then take over and be first reported on later lists. This retrieval shift was studied under varied list conditions designed to counteract ordinary position effects, and proved to be a stable and resistent effect. One experiment had subjects practice on five different free recall lists over three trials, and the results agreed with the hypothesis that primacy reduction is caused by proactive interference rather than by the primacy to recency report shift. Experiments of the usual one-session laboratory type have consistently failed to show practice effects on serial lists with incompatible spatial and temporal order cues. In a case study of five subjects examined over a period of three months only slight improvement on single-trial lists was observed. However, when naive subjects were given four successive trials with the same type of cue-conflict list, prominent practice effects were easily demonstrated. Observations confirmed the assumption that repeated presentations of items located in middle list positions may counteract the privilege of primacy and recency positions. When repetitions were made within contracting and expanding lists, the results proved that active anchoring, making itself visible as primacy effects, is feasible with contracting lists but difficult with expanding lists. Active performance of list learning strategies generally results in primacy effects; whereas passive shortcut procedures, in learning and retrieval of information, produce recency effects. Predominant recency effects are symptoms of difficult task situations only partially mastered by the learner; primacy effects point to more successful elaboration. Overall, serial position effects do not seem to be due to structural memory stores so much as to the working of cognitive strategy factors. A problem-solving theory was presented as an alternative to information-processing models of serial learning and memory.     

Primacy and recency effects in nonhuman primates.

The reports of primacy and recency memory effects in nonhuman primates have been criticized because they have all used an initiating response. That is, the presentation of the to-be-remembered list of items was always contingent on a response being initiated by the nonhuman primate. It has been argued that this initiating response improves performance for early items in the list, resulting in the occurrence of the primacy effect, independent of any memory processing mechanism. This criticism was addressed in the present study by not using an initiating response prior to the presentation of the list. Nevertheless, both a primacy and a recency effect were observed in all 6 rhesus monkeys evaluated using a serial probe recognition task. Thus, the results are similar to those for humans, in that both primacy and recency effects can be obtained in nonhuman primates. A brief literature review is included, and it is proposed that the primacy and recency effects observed in humans, nonhuman primates, and infraprimates can be explained within the context of the configural-association theory.     

An experimental analysis of memory processing

Rhesus monkeys were trained and tested in visual and auditory list-memory tasks with sequences of four travel pictures or four natural/environmental sounds followed by single test items. Acquisitions of the visual list-memory task are presented. Visual recency (last item) memory diminished with retention delay, and primacy (first item) memory strengthened. Capuchin monkeys, pigeons, and humans showed similar visual-memory changes. Rhesus learned an auditory memory task and showed octave generalization for some lists of notes--tonal, but not atonal, musical passages. In contrast with visual list memory, auditory primacy memory diminished with delay and auditory recency memory strengthened. Manipulations of interitem intervals, list length, and item presentation frequency revealed proactive and retroactive inhibition among items of individual auditory lists. Repeating visual items from prior lists produced interference (on nonmatching tests) revealing how far back memory extended. The possibility of using the interference function to separate familiarity vs. recollective memory processing is discussed.     

Glucocorticoids enhance taste aversion memory via actions in the insular cortex and basolateral amygdala

It is well established that glucocorticoid hormones strengthen the consolidation of hippocampus-dependent spatial and contextual memory. The present experiments investigated glucocorticoid effects on the long-term formation of conditioned taste aversion (CTA), an associative learning task that does not depend critically on hippocampal function. Corticosterone (1.0 or 3.0 mg/kg) administered subcutaneously to male Sprague–Dawley rats immediately after the pairing of saccharin consumption with the visceral malaise-inducing agent lithium chloride (LiCl) dose-dependently increased aversion to the saccharin taste on a 96-h retention test trial. In a second experiment, rats received corticosterone either immediately after saccharin consumption or after the LiCl injection, when both stimuli were separated by a 3-h time interval, to investigate whether corticosterone enhances memory of the gustatory or visceral stimulus presentation. Consistent with the finding that the LiCl injection, but not saccharin consumption, increases endogenous corticosterone levels, corticosterone selectively enhanced CTA memory when administered after the LiCl injection. Suppression of this training-induced release of corticosterone with the synthesis-inhibitor metyrapone (35 mg/kg) impaired CTA memory, and was dose-dependently reversed by post-training supplementation of corticosterone. Moreover, direct post-training infusions of corticosterone into the insular cortex or basolateral complex of the amygdala, two brain regions that are critically involved in the acquisition and consolidation of CTA, also enhanced CTA retention, whereas post-training infusions into the dorsal hippocampus were ineffective. These findings provide evidence that glucocorticoid effects on memory consolidation are not limited to hippocampus-dependent spatial/contextual information, but that these hormones also modulate memory consolidation of discrete-cue associative learning via actions in other brain regions.     

Primacy versus recency in a quantitative model: activity is the critical distinction

Behavioral and neurobiological evidence shows that primacy and recency are subserved by memory systems for intermediate- and short-term memory, respectively. A widely accepted explanation of recency is that in short-term memory, new learning overwrites old learning. Primacy is not as well understood, but many hypotheses contend that initial items are better encoded into long-term memory because they have had more opportunity to be rehearsed. A simple, biologically motivated neural network model supports an alternative hypothesis of the distinct processing requirements for primacy and recency given single-trial learning without rehearsal. Simulations of the model exhibit either primacy or recency, but not both simultaneously. The incompatibility of primacy and recency clarifies possible reasons for two neurologically distinct systems. Inhibition, and its control of activity, determines those list items that are acquired and retained. Activity levels that are too low do not provide sufficient connections for learning to occur, while higher activity diminishes capacity. High recurrent inhibition, and progressively diminishing activity, allows acquisition and retention of early items, while later items are never acquired. Conversely, low recurrent inhibition, and the resulting high activity, allows continuous acquisition such that acquisition of later items eventually interferes with the retention of early items.     

Free recall and complexity of pictorial stimuli

In order to explore variables underlying primacy and recency effects in free recall of pictorial material, norms were developed using 120 subjects who rated the vividness and complexity of slides. Two experiments were then run in which two levels of each of these variables (extreme high and low ratings) were factorially combined. In the first experiment 24 subjects were shown three mixed lists, two short and one long (consisting of materials of all four combinations of vividness and complexity), and in the second experiment 12 subjects were shown four pure lists (consisting of materials of a single type). Analysis of variance showed list length in the mixed list experiment and complexity in both experiments to be strong determinants of recall. Greatest recall was for items of low complexity in short lists. Weak, but statistically significant, serial position effects were evident, particularly for less complex items. The effects of primacy and recency seem to decrease with increasing complexity of visual materials, perhaps because of the greater difficulty in rehearsing more complex pictures either verbally or iconically.     

Visual list memory in capuchin monkeys (Cebus apella)

Memory of 3 capuchin monkeys, Cebus apella, was tested with lists of 4 travel-slide pictures and different retention intervals. They touched different areas of a video monitor to indicate whether a test picture was in a list. At short retention intervals (0 s, 1 s, 2 s), memory was good for the last list items (recency effect). At a 10-s retention interval, memory improved for 1st list items (primacy effect). At long retention intervals (20 s and 30 s), primacy effects were strong and recency effects had dissipated. The pattern of retention-interval changes was similar to rhesus monkeys, humans, and pigeons. The time course of recency dissipation was similar to rhesus monkeys. The capuchin's superior tool-use ability was discussed in relation to whether it reflects a superior general cognitive ability, such as memory. In terms of visual memory, capuchin monkeys were not shown to be superior to rhesus monkeys.     

Three more semantic serial position functions and a SIMPLE explanation

There are innumerable demonstrations of serial position functions—with characteristic primacy and recency effects—in episodic tasks, but there are only a handful of such demonstrations in semantic memory tasks, and those demonstrations have used only two types of stimuli. Here, we provide three more examples of serial position functions when recalling from semantic memory. Participants were asked to reconstruct the order of (1) two cartoon theme song lyrics, (2) the seven Harry Potter books, and (3) two sets of movies, and all three demonstrations yielded conventional-looking serial position functions with primacy and recency effects. The data were well-fit by SIMPLE, a local distinctiveness model of memory that was originally designed to account for serial position effects in short- and long-term episodic memory. According to SIMPLE, serial position functions in both episodic and semantic memory tasks arise from the same type of processing: Items that are more separated from their close neighbors in psychological space at the time of recall will be better remembered. We argue that currently available evidence suggests that serial position functions observed when recalling items that are presumably in semantic memory arise because of the same processes as those observed when recalling items that are presumably in episodic memory.     

Metacognition and learning about primacy and recency effects in free recall: The utilization of intrinsic and extrinsic cues when making judgments of learning

Although memory researchers know about primacy and recency effects, it is unclear whether students are aware of these effects and incorporate them when making judgments of learning (JOLs). The present research examined how participants use serial position information (extrinsic cues) when making JOLs after studying each item and showed that participants rely on the intrinsic qualities of the items and underestimate primacy and recency effects. However, when participants made JOLs prior to studying each item and engaged in multiple study-test sessions, their JOLs accurately reflected recall, as well as when serial position information was explicitly provided during the study phase. The findings are interpreted in a cue utilization framework and suggest that under certain conditions, participants can predict primacy and recency effects.     

Amnesia,rehearsal, and temporal distinctiveness models of recall

Classical amnesia involves selective memory impairment for temporally distant items in free recall (impaired primacy) together with relative preservation of memory for recency items. This abnormal serial position curve is traditionally taken as evidence for a distinction between different memory processes, with amnesia being associated with selectively impaired long-term memory. However recent accounts of normal serial position curves have emphasized the importance of rehearsal processes in giving rise to primacy effects and have suggested that a single temporal distinctiveness mechanism can account for both primacy and recency effects when rehearsal is considered. Here we explore the pattern of strategic rehearsal in a patient with very severe amnesia. When the patient’s rehearsal pattern is taken into account, a temporal distinctiveness model can account for the serial position curve in both amnesic and control free recall. The results are taken as consistent with temporal distinctiveness models of free recall, and they motivate an emphasis on rehearsal patterns in understanding amnesic deficits in free recall.     

Effects of stress hormones on traumatic memory formation and the development of posttraumatic stress disorder in critically ill patients

A majority of patients after intensive care treatment report traumatic memories from their stay in the intensive care unit (ICU). Traumatic memories can be associated with the development of posttraumatic stress disorder (PTSD) in a subpopulation of these patients. In contrast to other patient populations at risk for PTSD, patients in the ICU often receive exogenously administered stress hormones like epinephrine, norepinephrine, or cortisol for medical reasons and are extensively monitored. ICU patients therefore represent a suitable population for studying the relationship between stress hormones, traumatic memories, and the development of PTSD. Studies in long-term survivors of ICU treatment demonstrated a clear and vivid recall of different categories of traumatic memory such as nightmares, anxiety, respiratory distress, or pain with little or no recall of factual events. The number of categories of traumatic memory recalled increased with the total administered dosages of stress hormones (both catecholamines and cortisol), and the evaluation of these categories at different time points after discharge from the ICU showed better memory consolidation with higher dosages of stress hormones administered. However, the administration of stress doses of cortisol to critically ill patients resulted in more complex findings as it caused a significant reduction in PTSD symptoms measured after recovery. This effect can possibly be explained by a differential influence of cortisol on memory. Increased serum cortisol levels not only result in consolidation of emotional memory but are also known to cause a temporary impairment in memory retrieval which appears to be independent of glucocorticoid effects on memory formation. Disrupting retrieval mechanisms with glucocorticoids during critical illness may therefore act protectively against the development of PTSD by preventing recall of traumatic memories. Our findings indicate that stress hormones influence the development of PTSD through complex and simultaneous interactions on memory formation and retrieval. Our studies also demonstrate that animal models of aversive learning are useful in analyzing and predicting clinical findings in critically ill humans.     

Serial position-dependent false memory effects*

ABSTRACT

Evidence for false recognition within seconds of encoding suggests that semantic-associative influences are not restricted to long-term memory, consistent with unitary memory accounts but contrary to dual store models. The present study sought further relevant evidence using a modified free recall converging associates task where participants studied 12-item lists composed of 3 semantically distinct quartets (sublists) related to a separate, non-presented theme word (i.e., words 1–4/theme1, 5–8/theme2, and 9–12/theme3). This list construction permits assessment of false recall errors from each sublist, and, particularly, the primacy and recency sublists that have been linked to long- and short-term memory stores. Experiment 1 tested immediate free recall for items. Associative false memories were evident from all sublists, however, significantly less so from the recent sublist, which also showed the highest levels of veridical memory. By inserting a brief (3?s) distractor prior to recall, Experiment 2 selectively reduced veridical memory and increased false memory for the recent sublist while leaving the primacy sublist unaffected. These recall results converge with prior evidence indicating the immediacy of false recognition, and can be understood within a unitary framework where the differential availability of verbatim features and gist-based cues affect memory for primacy and recency sublists.     

Glucocorticoid release and memory consolidation in men and women

Glucocorticoid hormones have been shown to enhance memory consolidation when applied at low doses posttraining, but are ineffective or impair memory at high doses. In a test of whether this quadratic relationship also exists for endogenously released glucocorticoids, healthy men and women received cold-pressor stress (CPS) or a control procedure immediately after reading a relatively neutral story and were tested for retention 1 week later. Cortisol levels in response to the stressor were assayed from saliva. CPS significantly elevated salivary cortisol in both sexes, but enhanced memory only in male subjects. Among CPS-treated male subjects, there was a significant quadratic correlation between cortisol release posttraining and subsequent memory. Thus, these findings represent the first demonstration of an inverted-U relationship between activity of endogenous stress hormones and human memory.     

Judicial decision making: order of evidence presentation and availability of background information

An experiment was conducted to investigate both the effect of the order of presentation of defence and prosecution evidence and the prior availability of background information on assessment of guilt. Subjects were required to judge the defendant's probability of guilt either after each witness statement (step-by-step) or after having read all witness statements (end-of-sequence). In the step-by-step mode, an order effect was observed with later evidence exerting a greater impact on the subjects' judgment. This recency effect probably occurred because subjects used an anchoring-and-adjustment process: each new piece of evidence was averaged with an anchor judgment reflecting the overall assessment of previous items. In the end-of-sequence mode, on the other hand, the order effect depended on the background condition: if background information was provided a recency effect occurred, but if no background information was available a primacy effect was evident. This result might be explained by assuming that subjects tried to integrate witness information into a coherent cognitive pattern. As the judgment is memory-based in the end-of-sequence condition, recent information will be more available than earlier items. However, when no background information was presented, the first evidence items had to be processed at a more semantic, deeper level, resulting in a primacy effect that apparently outweighed the recency effect. © 1998 John Wiley & Sons, Ltd.     

Fluid and crystallized intelligence and primacy/recency components of short-term memory

Primacy and recency recall measures, obtained from both free and probed-recall tasks, were included in a battery of tests which also contained markers for fluid intelligence, crystallized intelligence, and cognitive speed factors. Our results confirmed previous findings that for subjects within the normal range of abilities, recency recall from probed-recall tasks is more closely linked to intelligence than is primacy recall. A new finding was also obtained: that primacy recall is correlated more with measures of cognitive speed than is recency recall. These results are discussed in terms of the concept of working memory and its relation to intelligence.     

Auditory and visual serial position functions obey different laws

Rhesus monkeys were tested in serial probe recognition tasks with either travel slide pictures or natural sounds. Tests with four-item lists produced serial position functions that were essentially opposite in shape for the two modalities and changed in opposite ways with retention interval. For visual memory, the primacy effect grew and the recency effect dissipated with retention interval. Capuchin monkeys, humans, and pigeons showed similar results. For auditory memory with rhesus monkeys, the recency effect grew and the primacy effect dissipated with retention interval. These results taken together, along with results from rehearsal tests of monkeys and humans, implicate two passive memory processes with different time courses. Interference among items within auditory lists was manipulated by varying the time between items and categories of items. Interference across lists was manipulated by varying the item pool size and, hence, item repetitions. Changes in the auditory serial position functions indicated that proactive and retroactive interference may have been instrumental in these dynamically changing serial position functions. Implications for theories and models of memory are discussed.     

Recency judgments as a function of word frequency: A framing effect and frequency misattributions

The effects of word frequency on judgments of recency of item presentation were examined in two experiments. Subjects in Experiment 1 were presented two mixed lists of high- and low-frequency words followed by a list assignment task for recognized items. It was found that subjects were biased toward assigning low-frequency words to the more recently presented list. Subjects in Experiment 2 were presented a single mixed list of high- and low-frequency words followed by either a relative recency of presentation judgment task or a relative primacy of presentation judgment task. Each word pair on the tests contained one high-frequency word and one low-frequency word. It was found that, for the recency judgment task, subjects were biased to select the low-frequency item as having been presented more recently. However, on the parallel primacy judgment task, there were no effects of word frequency; moreover, overall accuracy levels were higher with primacy than with recency instructions. We interpret the effects of word frequency on recency judgments in Experiments 1 and 2 in terms of a misattribution of frequency-related differences in recollection-based recognition. The finding that recency and primacy instructions produced different patterns of results provides further evidence (Flexser & Bower, 1974) for an effect on performance of the way in which the temporal judgment task was framed.     

Auditory List Memory in Rhesus Monkeys

Auditory memory of 2 rhesus monkeys was tested in a serial probe recognition task. Lists of four environmental or natural sounds were followed by a retention interval and a test. The test matched one of the list items on half of the trials. The retention interval was varied across sessions. Six experiments showed similar results and changes in the serial position function. At short retention intervals, there was good memory for first list items (primacy effect) and poor memory for last list items. At intermediate retention intervals, memory improved for last list items (recency effect). At long retention intervals (20 s and 30 s), the recency effect was strong, and the primacy effect had dissipated. These auditory primacy and recency effects and their changes with retention interval were opposite to those for visual memory. Implications for processes and mechanisms of memory are discussed.     

Serial position effects in recognition memory for odors: A reexamination

Seven experiments examined recognition memory for sequentially presented odors. Following Reed (2000), participants were presented with a sequence of odors and then required to identify an odor from the sequence in a test probe comprising 2 odors. The pattern of results obtained by Reed (2000, although statistically marginal) demonstrated enhanced recognition for odors presented at the start (primacy) and end (recency) of the sequence: a result that we failed to replicate in any of the experiments reported here. Experiments 1 and 3 were designed to replicate Reed (2000), employing five-item and seven-item sequences, respectively, and each demonstrated significant recency, with evidence of primacy in Experiment 3 only. Experiment 2 replicated Experiment 1, with reduced interstimulus intervals, and produced a null effect of serial position. The ease with which the odors could be verbally labeled was manipulated in Experiments 4 and 5. Nameable odors produced a null effect of serial position (Experiment 4), and hard-to-name odors produced a pronounced recency effect (Experiment 5); nevertheless, overall rates of recognition were remarkably similar for the two experiments at around 70%. Articulatory suppression reduced recognition accuracy (Experiment 6), but recency was again present in the absence of primacy. Odor recognition performance was immune to the effects of an interleaved odor (Experiment 7), and, again, both primacy and recency effects were absent. There was no evidence of olfactory fatigue: Recognition accuracy improved across trials (Experiment 1). It is argued that the results of the experiments reported here are generally consistent with that body of work employing hard-to-name visual stimuli, where recency is obtained in the absence of primacy when the retention interval is short.