Consolidation of long-term memory: evidence and alternatives

Memory loss in retrograde amnesia has long been held to be larger for recent periods than for remote periods, a pattern usually referred to as the Ribot gradient. One explanation for this gradient is consolidation of long-term memories. Several computational models of such a process have shown how consolidation can explain characteristics of amnesia, but they have not elucidated how consolidation must be envisaged. Here findings are reviewed that shed light on how consolidation may be implemented in the brain. Moreover, consolidation is contrasted with alternative theories of the Ribot gradient. Consolidation theory, multiple trace theory, and semantization can all handle some findings well but not others. Conclusive evidence for or against consolidation thus remains to be found.     

Working memory retention systems: a state of activated long-term memory

High temporal resolution event-related brain potential and electroencephalographic coherence studies of the neural substrate of short-term storage in working memory indicate that the sustained coactivation of both prefrontal cortex and the posterior cortical systems that participate in the initial perception and comprehension of the retained information are involved in its storage. These studies further show that short-term storage mechanisms involve an increase in neural synchrony between prefrontal cortex and posterior cortex and the enhanced activation of long-term memory representations of material held in short-term memory. This activation begins during the encoding/comprehension phase and evidently is prolonged into the retention phase by attentional drive from prefrontal cortex control systems. A parsimonious interpretation of these findings is that the long-term memory systems associated with the posterior cortical processors provide the necessary representational basis for working memory, with the property of short-term memory decay being primarily due to the posterior system. In this view, there is no reason to posit specialized neural systems whose functions are limited to those of short-term storage buffers. Prefrontal cortex provides the attentional pointer system for maintaining activation in the appropriate posterior processing systems. Short-term memory capacity and phenomena such as displacement of information in short-term memory are determined by limitations on the number of pointers that can be sustained by the prefrontal control systems.     

Test-enhanced learning: taking memory tests improves long-term retention

Taking a memory test not only assesses what one knows, but also enhances later retention, a phenomenon known as the testing effect. We studied this effect with educationally relevant materials and investigated whether testing facilitates learning only because tests offer an opportunity to restudy material. In two experiments, students studied prose passages and took one or three immediate free-recall tests, without feedback, or restudied the material the same number of times as the students who received tests. Students then took a final retention test 5 min, 2 days, or 1 week later. When the final test was given after 5 min, repeated studying improved recall relative to repeated testing. However, on the delayed tests, prior testing produced substantially greater retention than studying, even though repeated studying increased students' confidence in their ability to remember the material. Testing is a powerful means of improving learning, not just assessing it.     

Very long-term memory for odors: retention of odor-name associations.

The ability to remember odor-name associations for recent odors (those associated with everyday products experienced within the past 2 years) and distant odors (those associated with children's toys not encountered for 3 years or more) was examined in two experiments. In recognition tasks, subjects attempted to match odor names to odors, or odors to odor names. In a recall task, subjects tried to identify odors by name. The results showed that although odor retention was better for recent than distant odors, significant retention remains for odors not experienced since childhood. These results are consistent with other studies that found very slow and gradual loss of odor information in memory. They extend that research by showing that odor information is still available over a much longer period of time.     

Epinephrine modulates long-term retention of an aversively motivated discrimination

These experiments examined the effects of post-training epinephrine (Epi) on retention of an aversively motivated discrimination task. Male CFW mice were trained to escape from footshock by entering one of two alleys of a Y-maze. On a 24-h retention test (six trials) the correct alley was reversed. The findings of Experiment 1 indicate that errors on the discrimination reversal varied directly with number of trials (criterion of 0, 3, or 6 successive correct choices) on the original training. These findings indicate that errors on discrimination reversal training provide a sensitive index of retention of the original training. In Experiment 2, mice were trained to a criterion of three successive correct choices and were given post-training injections of saline or Epi (0.1, 0.3, or 1.0 mg/kg ip). On a 24-h discrimination reversal test mice given the low doses of Epi made more errors than did saline controls while mice given the high dose made fewer errors. In Experiment 3, mice trained as in Exp 2 received post-training saline or Epi (0.3 or 1.0 mg/kg) and were tested for retention either 1 week or 1 month later. At each retention interval, performance was comparable to that found with a 24-h retention interval. The findings provide additional evidence that post-training Epi produces long-lasting dose-dependent modulating effects on memory storage.     

Forgetting curves in long-term memory: evidence for a multistage model of retention.

An experimental study with 20 normal healthy young adult subjects was performed to evaluate the interaction of type of memory tasks, type of learning modalities, and length of acquisition/recall interval. Four different tasks were employed (serial learning, paired learning, rote learning, and visuolinguistic transfer), some requiring a single trial learning modality others a multitrial learning modality. Acquisition/recall intervals were immediate, intermediate (3 min), and delayed. The experimental design allowed for the comparison of effects from five different delayed recall intervals (2, 8, 12, 24, and 48 hr). Results demonstrated a specific interaction on learning rates due to different ceiling effects for the different types of memory tasks. Forgetting rates, on the other hand, demonstrated a specific effect due to type of memory tasks and learning modalities only for differences between immediate and intermediate recall. These differences remained stable during the longer intervals and were not affected by length of interval. A multistage composition of long-term retention was suggested to explain these results, and a practical indication to build experimental procedures to study memory in the clinical field was evidenced.     

d-Cycloserine: effects on long-term retention of a conditioned response and on memory for contextual attributes.

d-Cycloserine (DCS), a partial agonist of the glycine recognition site of the N-methyl d-aspartate receptor, has beneficial effects on learning and memory. In order to investigate its potential to influence learning and memory of both the response and the stimulus attributes of training, male Sprague-Dawley albino rats were trained in a one-trial inhibitory avoidance task following an acute intraperitoneal injection of DCS (3 mg/kg) or an equal volume of saline. In order to measure memory for stimulus attributes, testing involved a context shift paradigm, in which subjects are tested in either the environment of training or a different one. Good memory for the contextual attributes of training is indicated by poor performance in the alternate context. Retention was assessed either 1, 7, or 14 days after training. At 1 day, Saline subjects were affected by a change in context, while DCS subjects were not. In subjects tested 1 week following training, Saline subjects were no longer affected by a change in context, in that they performed the avoidance response in both contexts. This indicates the forgetting of stimulus attributes in Saline subjects. DCS subjects did show the context shift effect at 1 week, indicating the retention of stimulus attributes. Finally, Saline subjects demonstrated the context shift rebound at 14 days, while DCS subjects performed equivalently in both contexts. Taken together, these data suggest that DCS may enhance retention of fear and slow the forgetting of stimulus attributes.     

Consolidation and interference in the perceptual memory system

Previous verbal/memory studies have indicated that perceptual processes continue to occur after the stimulus is terminated. The present study investigated whether a blank period after a nonverbal stimulus would function to strengthen or consolidate the sensory trace in memory. A “delayed-comparison task” of recognition memory for pitch was employed in two experiments. The results indicated that a blank interval after the tone to be remembered increased the memory strength of that tone when the tone’s duration was brief (.2 sec). However, an empty interval after a tone with a longer duration (.5 sec) did not affect memory performance. Memory strength also decreased over time during a retroactive interval tone. A storage-interference model described the quantitative results accurately.     

Developments in long-term explicit memory late in the first year of life: behavioral and electrophysiological indices

Coincident with developments in the temporal-cortical explicit memory network, long-term recall abilities are newly emergent late in the first year of human life. We recorded event-related potentials (ERPs) in 9-month-olds as an index of the integrity of the neural substrate underlying a task thought to reflect explicit memory, namely, deferred imitation. ERP measures of recognition memory 1 week after unique laboratory experiences predicted whether and how much infants recalled of the experiences 1 month later. The findings further imply that memory storage and consolidation processes are a major source of variability in long-term recall memory late in the first year of life.     

Cumulative learning and long-term retention of sentences

The purpose of this experiment was to study the role of the number of simultaneously presented words in the formation of higher-order units. The variable was the number of modifying elements presented over successive trails in the learning of a set of eight sentences. Results indicated that a S can integrate one new element into an already acquired structure, while he cannot process two or four new elements. After a one-week delay, the learning conditions determine the amount of retention: the progressive introduction of one or two new elements into the kernel group which makes for the organization of very strong structures, leads to a better retention.     

Dissociating retention and access in working memory: an age-comparative study of mental arithmetic

In two experiments, young and older adults solved arithmetic chain tasks with single-digit operands, with or without a concurrent memory load of three or six digits. Variables in the arithmetic tasks had to be replaced by digits from the screen or from the memory set. A task-irrelevant concurrent load impaired neither speed nor accuracy of arithmetic in younger adults. In Experiment 2, this was also true for older adults. A large decrease in arithmetic performance was observed, however, when variables in the arithmetic task had to be substituted by digits from the memory list. Older adults had specific problems with this condition in Experiment 1, where the substitution involved two successive steps, but not in Experiment 2, where the substitution from memory could be done in a single step. The results are difficult to reconcile with models assuming a common resource for storage and processing. Rather, they are compatible with the hypothesis that a concurrent memory load interferes with a processing task only during the points of access to working memory. Further, even though access to working memory was found to be the critical source of concurrent-load interference, it was found to be insensitive to the effects of adult aging.     

Organization and long-term memory search

A recognition RT paradigm was used to assess a number of plausible search strategies in LTM for categorized lists. List length was determined by factorially combining two, three, or five categories with two, three, or five words per category, and test items could be one of four types: (1) positive, (2) a repeated positive, (3) a related negative, or (4) an unrelated negative. It was found that RT increased linearly with category size for both positive and related negatives (about 30-40 msec/item); whereas the increase was much smaller for the unrelated negatives, especially for three and five categories (about 9 msec/item). With an increase in the number of categories, RT increased at the rate of about 40 msec/category for all three test items. A theory of .high-speed scanning for categorized material was proposed in which a serial and exhaustive search of the categories, is first undertaken. If a positive category match is found, a serial and exhaustive search within the contents of the positive category is initiated; if no category match is found, the search is simply terminated. Some evidence was presented that categories recently probed may provide for a short-circuiting of the category search.     

Recognition memory retention interval and information load

Two experiments were conducted to study the effect of retention interval and information load on short-term recognition memory in retarded subjects. The task consisted of an input trial of 1–15 pictures followed by a test trial of one picture, with the subject having to press different levers to indicate whether the probe picture had been present on the input trial. Retention intervals between input trial and test trial were manipulated over a range of 1–24 sec. Both accuracy and latency of response were measured. Results showed that latency increased and accuracy decreased as a function of both retention interval and number of stimuli. In addition, number of stimuli interacted with retention interval such that accuracy was not affected by retention interval when information input was small, but decreased quite dramatically at longer retention intervals when input was larger. The results were discussed in terms of current memory search models for both normal and retarded subjects.     

Very long-term retention of a novel

This study investigated the very long-term retention of a full-length novel originally studied as part of a university undergraduate course. One hundred and forty former students completed three tests designed to assess retention of Charles Dickens' Hard Times. Retention intervals ranged from 3 to 39 months. Subjects' responses when they were asked to report their most vivid and enduring memory of the novel were consistent with story grammar models which claim that components of a story which are higher in a hierarchy are remembered better than those lower in the hierarchy. A free recall test of the names and roles of the characters in the novel found that retention of both declined rapidly in the first few months following acquisition, that names were forgotten more quickly than roles, and that retention of both had stabilized above baseline before the longest retention interval. These data are interpreted in terms of a schema account of memory retention, in which retention of schematic knowledge (roles), but not non-schematic knowledge (names) can be mediated by abstract knowledge structures. The results of a fact verification test showed that memory for events of high importance in the novel was better than memory for events of low importance, consistent with models that suggest that texts and stories are represented hierarchically in memory. Confidence ratings also declined over time and showed that subjects generally assessed the accuracy of their responses correctly. The significant predictors of memory for the novel were retention interval and the mark obtained on a coursework essay on Hard Times.     

Media multitasking and memory: Differences in working memory and long-term memory

Increasing access to media in the 21st century has led to a rapid rise in the prevalence of media multitasking (simultaneous use of multiple media streams). Such behavior is associated with various cognitive differences, such as difficulty filtering distracting information and increased trait impulsivity. Given the rise in media multitasking by children, adolescents, and adults, a full understanding of the cognitive profile of media multitaskers is imperative. Here we investigated the relationship between chronic media multitasking and working memory (WM) and long-term memory (LTM) performance. Four key findings are reported (1) heavy media multitaskers (HMMs) exhibited lower WM performance, regardless of whether external distraction was present or absent; (2) lower performance on multiple WM tasks predicted lower LTM performance; (3) media multitasking-related differences in memory reflected differences in discriminability rather than decision bias; and (4) attentional impulsivity correlated with media multitasking behavior and reduced WM performance. These findings suggest that chronic media multitasking is associated with a wider attentional scope/higher attentional impulsivity, which may allow goal-irrelevant information to compete with goal-relevant information. As a consequence, heavy media multitaskers are able to hold fewer or less precise goal-relevant representations in WM. HMMs’ wider attentional scope, combined with their diminished WM performance, propagates forward to yield lower LTM performance. As such, chronic media multitasking is associated with a reduced ability to draw on the past—be it very recent or more remote—to inform present behavior.     

Short-term retention of a single word relies on retrieval from long-term memory when both rehearsal and refreshing are disrupted

Many working memory (WM) models propose that the focus of attention (or primary memory) has a capacity limit of one to four items, and therefore, that performance on WM tasks involves retrieving some items from long-term (or secondary) memory (LTM). In the present study, we present evidence suggesting that recall of even one item on a WM task can involve retrieving it from LTM. The WM task required participants to make a deep (living/nonliving) or shallow (“e”/no “e”) level-of-processing (LOP) judgment on one word and to recall the word after a 10-s delay on each trial. During the delay, participants either rehearsed the word or performed an easy or a hard math task. When the to-be-remembered item could be rehearsed, recall was fast and accurate. When it was followed by a math task, recall was slower, error-prone, and benefited from a deeper LOP at encoding, especially for the hard math condition. The authors suggest that a covert-retrieval mechanism may have refreshed the item during easy math, and that the hard math condition shows that even a single item cannot be reliably held in WM during a sufficiently distracting task—therefore, recalling the item involved retrieving it from LTM. Additionally, performance on a final free recall (LTM) test was better for items recalled following math than following rehearsal, suggesting that initial recall following math involved elaborative retrieval from LTM, whereas rehearsal did not. The authors suggest that the extent to which performance on WM tasks involves retrieval from LTM depends on the amounts of disruption to both rehearsal and covert-retrieval/refreshing maintenance mechanisms.