The Organization of Reactivated Memory in Infancy

The specificity of memory retrieval by 3-month-old infants was examined in 3 experiments. All infants were trained in the mobile conjugate reinforcement paradigm to kick their feet to produce movement in an overhead crib mobile and were tested 2 weeks later. 24 hours prior to the test, subjects received a 3-min reminder treatment. The results of Experiment 1 demonstrated that only the moving training mobile alleviated forgetting after the 2-week retention interval; forgetting was not alleviated by exposure to the stationary training mobile or to the mobile stands and ribbon alone. The results of Experiments 2 and 3 demonstrated that, once retrieved, the reactivated memory was highly specific to the conditions of original training. Furthermore, the memory attributes that were the last to be forgotten (e.g., the general or global features) were the first to be retrieved following the reminder treatment. Conversely, those memory attributes that were forgotten first (e.g., the specific or local details) were the last to be retrieved. These findings have important implications for infant memory retrieval, reminiscence, and infantile amnesia.     

Contextual Constraints on Memory Retrieval at Six Months

In 3 experiments, 6-month-old infants learned to move a mobile by kicking and were tested 1 to 21 days later for retention of the newly acquired memory as a function of the training and testing contexts. In Experiment 1, decreasing the relative distinctiveness of the training and testing context did not impair retrieval of the newly acquired memory. In Experiment 2, however, testing in a different context completely eliminated retention after delays of 1 and 3 days, when retention was otherwise perfect; after progressively longer delays, retention improved paradoxically. The familiarity or novelty of the test context was not a factor in the failure of infants to recognize the mobile in the altered context after 1 day. In Experiment 3, the effect of an altered context was assessed in a reactivation paradigm. After the training memory was forgotten, infants were presented with the original mobile as a reminder and were tested for retention of the training memory 1 day later. When either the reminding context or the testing context was different, they exhibited no retention. These findings reveal that memory retrieval at 6 months is highly specific to the setting in which the memory is acquired. We propose that infants learn what specific events are associated with what specific places prior to the age when they can locomote independently and acquire a spatiotemporal map of the relations between those places.     

Ontogeny of long-term,nonassociative memory in the rat

The primary purpose of the present study was to assess the ontogeny of nonassociative learning and memory in 16-, 30-, and 75-day-old rats. In each of three experiments, habituation of the orienting response to a novel auditory stimulus was measured. The orienting response is an unconditioned reaction elicited by innocuous environmental stimulation that habituates with repeated stimulus presentations. Both an autonomic component (heart-rate deceleration) and a behavioral index (head jerk) of the orienting response were recorded in this study. Although no age differences in rate of habituation (i.e., rate of nonassociative learning) were found (see Experiment 1), a marked effect of age on retention of habituation was observed. Preweanling rats retained habituation of the orienting response to an auditory stimulus for less than 4 h (Experiment 2), whereas adult animals exhibited no forgetting even after a 1-week interval (Experiment 3). These results are discussed in terms of (1) demonstrations of age-related differences in associative memory, (2) the persistence of nonassociative memories in adults, and (3) the significance of the orienting response as a measure of retention of nonassociative learning.     

Order and duration of stimuli are important determinants of reactivation

Prior cuing treatments intended to alleviate the forgetting of a conditioned avexsion-to an odor were tested with 18-day-old rats. Previous experiments had shown that when such pups were conditioned with the use of a CS?/CS+ procedure, pretest presentation of the CS? or US, but not the CS+, alleviated the forgetting otherwise seen after a 3-h retention interval. In Experiment 1, it was determined that the forgetting was not alleviated if the GS? was either preceded or followed by presentation of the CS+, despite the fact that the CS?/CS+ ordering mimicked that of original conditioning. Experiment 2 was an examination of the balance of extinction and reactivation effects caused by presenting the CS+ for varying durations following the 3-h retention interval. The forgetting over this interval was alleviated if the CS+ was presented for 5 or 15 sec, but not 30 sec. With an increase in duration of exposure from 15 to 30 sec, the consequences of the CS+ as a prior cuing treatment apparently shifted from reactivation to extinction. Experiment 3 was a test of the interaction between the consequences of different lengths of CS+ exposure and the effectiveness of adding CS? to the CS+ as a reactivation treatment. The varied effectiveness of reactivation treatments is discussed interms of a change in stimulus conditions from training to reactivation.     

Further studies of pigeons’ spatial working memory in the open-field task

In Experiments 1 and 2, pigeons’ spatial working memory in an open-field setting was examined under conditions that differed in terms of working-memory load (number of sites visited prior to a retention test) at various delays between initial choices and the retention test. In Experiment 1, pigeons were tested under two conditions of memory load (three or five sites visited prior to the delay) and two delay intervals (15 and 60 min). Accuracy declined as a function of delay but was not affected significantly by memory load. In Experiment 2A, pigeons were tested under three conditions of memory load (two, four, or six sites visited prior to the delay). In separate phases, the delay was 2, 15, and 60 min. Accuracy was not affected by memory load in any of these phases. In Experiment 2B, three conditions of memory load (two, four, or six sites visited prior to the delay) were tested at two delays (2 and 60 min) within a test phase. Accuracy declined with increasing delay, but memory load again had no significant effects. These results are inconsistent with previous suggestions that pigeons’ retention of spatial information may decline as working-memory load is increased. In Experiment 3, cue-manipulation tests confirmed that pigeons’ choice behavior in the open-field task is controlled by memory for previously visitad room locations.     

Stimulus conditions influencing the development of tolerance to repeated cold exposure in rats

Tolerance to an environmental cold challenge in rats is eliminated when cold exposure occurs in a context different from the adaptation context, indicating that learning mechanisms play a role in thermoregulation (Riccio, MacArdy, & Kissinger, 1991). This finding, analogous to outcomes obtained with drug tolerance, was investigated in the present study. Experiment 1 demonstrated that a change in both proximal and distal contextual cues disrupts an established cold adaptation, an outcome consistent with the view that associative processes contribute to the tolerance. In Experiment 2, although cold tolerance persisted over a 7-day retention interval, the disruption of tolerance by a shift in context was attenuated with the delay of testing. This finding suggests that the precise stimulus attributes of the context were forgotten over the interval. Experiment 3 demonstrated that cold-tolerance disruption is due to the actual change in context and not to novelty of the test context. Experiment 4 showed that changing the context associated with each cold exposure impaired the development of tolerance. The results of these experiments provide additional evidence that cold tolerance is regulated at least partially by associative learning processes.     

The effect of modality on long-term recognition memory

Two experiments examined the effects of visual and auditory modes of input on long-term memory. In Experiment 1, 40 subjects learned a 40-word list presented in a blocked or random fashion. In the blocked conditions learners were presented half the nouns in one modality followed by the remaining 20 words in the other modality (See-Hear or Hear-See). Subjects in random conditions also received half the list in each modality, but the presentation was random (Mixed or Mixed Reverse). Following a 6-min delay, subjects completed an 80-item visual recognition test. Analysis of these data showed significantly (p < .05) greater recognition of words presented visually than those presented auditorily. Experiment 2 was designed to test the hypothesis that learners may visualize a “literal copy” of the stimulus item by controlling for the extent to which the recognition measure offered a visual cue. Two groups of 40 subjects were examined using the same procedure used in Experiment 1, with the exception that one group received a visual recognition test while the other was tested auditorily. These data showed that the lack of a visual cue hindered the recognition of visually presented words, while it had little effect on stimuli presented auditorily. The results of these experiments were interpreted as support for the hypothesis that physical characteristics of a stimulus may persist in memory well beyond immediate memory intervals. Subjects were seen to make modality-specific decisions by testing long-term memory for the presence or absence of a visual memory trace.     

Discrimination of geons by pigeons: The effects of variations in surface depiction

We explored how changes in the depiction of the surface features of a simple volume (a geon) affected the pigeon’s recognition performance. Pigeons were trained to make a different keypeck response to each of four computer-rendered single-geon objects. In Experiment 1, the pigeons were tested with images of the original stimuli in which the light source was shifted from its original position, as well as with silhouettes and line drawings of these objects. All three types of stimulus variations resulted in marked drops in performance: above chance for silhouettes and light-change stimuli, but at chance for line drawings. In Experiment 2, the pigeons were tested with images of the original stimuli in which the contrast levels were either increased or decreased. These transformations resulted in very small drops in performance (except for the complete absence of contrast-a silhouette). These results indicated that the pigeons attended to the shape of the outside contour of an object and to the relative brightness of an object’s surface contours.     

Recognition memory for lists of visual stimuli in monkeys and humans

In Experiment 1, short-term memory for lists of visual stimuli was studied in four squirrel monkeys (Saimiri sciureus). A delayed-matching procedure was used in which a subject was presented with lists containing one, three, or six stimulus patterns, and memory for serial positions was probed by requiring the subject to choose between a list item and a nonlist item. The rate of item presentation was varied, as was the delay between the final item on a list and the retention test. In Experiment 2, the same procedures were used to compare recognition memory in four monkeys and four humans. Although differences in the levels and shapes of the serial-position curves appeared between species, both monkeys and humans showed primacy and recency effects. The presentation time of stimuli had a negligible effect on performance in both monkeys and humans, whereas delay significantly affected human retention but not monkey retention.     

Differential effects of several retrieval cues over time: Evidence for time-dependent reorganization of memory

The retention performance following partial training (15 trials) of a brightness-discrimination avoidance task has been shown to fluctuate over time, with a drop in performance 1 h after training (Kamin effect), a long-term spontaneous improvement (LTSI) after 3 days, and long-term spontaneous forgetting after 21 days. The purpose of this paper was to determine if these time-dependent modulations of retention performance reflect time-dependent modifications in the organization of the attributes that constitute the memory trace. We studied the relative effectiveness of several pretest cuings on retention performance when they were delivered just before a retention test occurring 1 h, 3 days, or 21 days following initial training. Some cuing treatments were related to a particular training event (conditioned or unconditioned stimulus, experimental context). Compound cuings, composed of two or more training events, were also studied to test a possible additive effect between retrieval cues. To demonstrate time-dependent modifications in the memory trace, a differential effectiveness over time was expected for at least some retrieval cues. The results show that cuing may compensate for performance deficits (1 h or 21 days), but does not further enhance performance when spontaneously improved (3 days). No detectable additive effects of retrieval cues were obtained. However, these results provide information that suggests a time-dependent effectiveness for some cuing treatments. In the last experiment, we investigated this possibility by studying the effects of each of these treatments when delivered after either a 1-h or a 21-day retention interval. The results confirm a time-dependent decrease in effectiveness of a pretest exposure to the CS and an increase in effectiveness over time of a pretest exposure to the experimental context or to a well-ordered sequence of events. Such differential retrievability of a partially learned episode according to both the nature of the cues and the length of the retention interval suggests a time-dependent reorganization of memory attributes.     

The effect of prior practice on memory reactivation and generalization

Three experiments examined the effect of practice on memory performance by 18-month-old infants. Infants were tested using an imitation paradigm; an adult demonstrated a series of actions with objects and infants were given the opportunity to reproduce those actions following a delay. Some infants practiced the target actions before the retention interval (practice) and some did not (no practice). In Experiment 1, a reminder treatment alleviated forgetting by infants who practiced but failed to alleviate forgetting by infants who did not practice. In Experiments 2A and 2B, infants who practiced generalized to novel test stimuli after a 24-hr delay, whereas infants without practice did not. Results suggest practice influences the accessibility and generality of infants' memories.     

Counterconditioning of memory in rats

Two experiments examined the counterconditioning of an aversively motivated response in rats. Presentation of a highly palatable sugar solution (maltose in Experiment 1; sucrose in Experiment 2) to thirsty rats was used as the counterconditioning treatment. In Experiment 1, the counterconditioning procedure was found to be effective in modifying both a newly acquired and a cue-reactivated fear memory. In Experiment 2, the counterconditioning effect was shown to occur when the fear memory was reactivated with a noncontingent exposure to the unconditioned stimulus rather than the conditioned stimulus. This outcome supports the interpretation of counterconditioning as a modification of some central representation of the original training memory, rather than the acquisition of a competing peripheral response. The methodological implications of the present approach to counterconditioning are considered.     

Categorization and memory retrieval by three-month-olds

84 3-month-olds were tested in 3 studies of the acquisition and long-term retention of category-specific information. Infants who were trained with a perceptibly different member of an alphanumeric category on each of 3 days generalized responding to a novel instance of the original training category but not a novel member of a novel category during a 24-hour novelty test. 2 weeks later, when infants displayed no evidence of remembering their prior training experience, categorization was reinstated if a novel exemplar from the original training category was used as the retrieval cue in a memory reactivation procedure. A novel exemplar from a novel category was not an effective retrieval cue. The effectiveness of the category-specific retrieval cue was a function of its physical similarity to the individual exemplars encountered during training, not testing. The background against which the alphanumeric exemplars were displayed during training was not an effective retrieval cue in either the 24-hour novelty test or the memory reactivation procedure, indicating that all invariant stimulus attributes do not contribute equally as category cues. These data are the first to document retention of category-specific information after extended intervals. A popular account of categorization holds that infants abstract invariant features from individual exemplars and form a schema or distinctive memory representation of these shared features against which subsequent exemplars are compared. The present data provide support for a more parsimonious account of categorization, based on the retrieval of information about individual exemplars, that does not require an assumption of prototype formation.     

The influence of the information value provided by prior-cuing treatment on the reactivation of memory in preweanling rats

In two experiments, the influence of exposure to a CS? on the acquisition and retention of a conditioned odor aversion was examined. Preweanling rats were given exposure to the CS? either prior to (CS?/CS+) or following (CS + /CS?) the pairing of a second odor (the CS+) with footshock. The results of Experiment 1 indicated that subjects in both of the treatment conditions acquired aversions of comparable strength to the odor paired with footshock and that retention of the odor aversion was not affected by order of stimulus presentation during conditioning. Experiment 2 indicated, however, that the effectiveness of pretest exposure to various elements of the conditioning episode in reactivation of the memory for conditioningwas dependent on the order of stimulus presentation during conditioning. This differential effectiveness of the various reactivation treatments is discussed in terms of their relationship to the associative “status” of the stimuli present during conditioning and in terms of the information provided to the animal by the reactivation treatment.     

Expression of a taste aversion conditioned with an odor-taste compound: Overshadowing is relatively weak in weanlings and decreases over a retention interval in adults

Adult rats were injected with lithium chloride (LiCl) after consumption of a novel flavor (chocolate milk) that either was or was not presented together with a novel ambient odor (banana) as a compound conditioned stimulus (CS). In Experiment 1, the adults’ consumption of the flavor 24 h after conditioning was compared with that of weanling rats given the same conditioning treatment on Postnatal Day 21. The results confirmed previous indications that the reduction in aversion observed for adults conditioned with the compound CS (overshadowing) was weak or nonexistent in weanlings. After a longer retention interval (21 days), there was no evidence of overshadowing in adults despite maintained retention of the basic conditioned aversion. In Experiment 2 this decrease in overshadowing after a long retention interval was replicated with adult animals and extended to a different method of testing. The form of the effect was the same as in Experiment 1: The decrease in overshadowing occurred over the retention interval without loss in retention of the basic taste aversion; the decrease in overshadowing was a consequence of anincrease in the flavor aversion displayed by animals conditioned with the compound CS. The impaired flavor aversion (i.e., the overshadowing) observed shortly after conditioning apparently was due to factors associated with memory retrieval, rather than to reduced attentional or associative strength.     

Infants' Forgetting of Correlated Attributes and Object Recognition

Infants as young as 3 months of age can encode the relations among object features. Because object recognition depends critically upon a match between perceived feature configurations and representations of the object in long-term memory, the present experiments focused on infants' long-term memory for feature correlations. In 3 experiments with 72 3-month-olds, we documented the forgetting functions of different feature correlations, examined their relation to infants' memory for individual features, and replicated the findings with different stimuli. Infants were trained to activate a mobile composed of two kinds of blocks that differed in color, the figures displayed on them, and the figures' colors and were tested after different delays with recombinations of either the block colors, the figures, or the figure colors. Infants remembered some of the original feature combinations for up to 3 days but forgot all of them after 4 days. Even after 4 days, however, infants remembered the individual features that had entered into the original combinations. These results demonstrate that very young infants not only encode the relations among object features but also remember them for several days. Moreover, there is a dissociation in memory between features and feature relations: Feature relations are forgotten sooner than the individual features that comprise those relations.     

The choose-short effect in pigeon memory for stimulus duration: Subjective shortening versus coding models

A symbolic delayed matching procedure may be used to study memory for stimulus duration in pigeons. Short and long presentations of a light sample stimulus are mapped onto the choke of visually differentiated comparison keys. When delay is varied in such a symbolic delayed matching procedure, pigeons show increasing preference for the short-sample key as the delay becomes longer (choose-short effect), even after a long sample stimulus has been presented. Two theoretical explanations of the choose-short effect are suggested. A subjective shortening model holds that the choose-short effect arises from progressive shortening of the memory of stimulus duration as the delay proceeds. An alternative coding model suggests that the choose-short effect arises from stimulus generalization after an initial response instruction to peck the long-sample key has been forgotten. These two models were tested by training pigeons to peck a third comparison key after no sample stimulus had been presented. Shifts in key preferences over delays ranging from 0 to 21 sec clearly supported the coding model.     

The effects of rapid eye movement sleep deprivation and recovery on spatial reference memory of young rats

It is known that rapid eye movement (REM) sleep plays a crucial role in learning and memory. Previous studies have demonstrated that postlearning REM sleep deprivation (RSD) impairs memory consolidation. Most of these studies observed only the effects of RSD on learning and memory. In the present study, we not only investigated the impacts of 48-h RSD on the spatial reference memory of young rats in a Morris water maze, but also specifically examined whether an REM rebound for 24–48 h after 48-h RSD affected the maintenance of spatial reference memory. RSD was induced by the modified multiple platform method, and spatial reference memory was tested in a Morris water maze. The results demonstrated that, compared with the control groups, posttraining RSD for 48 h produced a significant impairment in the retention of acquired spatial reference memory, and the impairment continuously existed after 24 and 48 h of release from sleep deprivation, which indicates that REM sleep plays a critical role in reference memory maintenance and consolidation. Moreover, postlearning RSD may lead to a long-term impairment in the consolidation of newly acquired memories.     

Spontaneous recovery after extinction of a conditioned taste aversion

Four experiments examined whether or not spontaneous recovery could occur after extinction in the conditioned taste-aversion paradigm. After three extinction trials, spontaneous recovery was obtained over an 18-day retention interval (Experiments 1, 2, and 3). The effect was not due to changes in the unconditioned preference for saccharin over the retention interval (Experiment 2) or to an increase in a nonextinguished aversion over time, as indicated by tests with both the original, nonextinguished aversion (Experiment 1) and with a weaker one (Experiment 3). Spontaneous recovery was not obtained when extinction was overtrained (eight trials) and a 49-day retention interval was used (Experiment 4). However, saccharin intake at asymptote reached the level of baseline water intake, and not the highly preferred level shown by never-conditioned controls. Results of all four experiments suggest that extinction does not return an averted taste to the status of an unconditioned one.     

Retrograde amnesia for extinction: Similarities with amnesia for original acquisition memories

Two experiments were conducted using rats to determine whether extinction is susceptible to a traditional amnestic agent (i.e., hypothermia) and to examine whether amnesia for extinction follows the same characteristics as those that occur with original memories. In Experiment 1, rats received hypothermia immediately, 60 min, or 120 min after extinction. When tested, the subjects cooled shortly after extinction showed little memory of the extinction training. This amnesia for extinction disappeared with longer postextinction delays, demonstrating a temporal gradient. Experiment 2 replicated the basic finding and demonstrated that an amnestic-extinguished memory could be recovered by reexposing the subjects to the amnestic agent and that the recovered extinction memory did not persist. These findings provide more evidence that extinction is a form of new learning and are consistent with retrograde amnesia research for original memories showing a temporal gradient and alleviation of retrograde amnesia by reexposure to the amnestic agent.