Deletion of the GluA1 AMPA receptor subunit alters the expression of short-term memory

Deletion of the GluA1 AMPA receptor subunit selectively impairs short-term memory for spatial locations. We further investigated this deficit by examining memory for discrete nonspatial visual stimuli in an operant chamber. Unconditioned suppression of magazine responding to visual stimuli was measured in wild-type and GluA1 knockout mice. Wild-type mice showed less suppression to a stimulus that had been presented recently than to a stimulus that had not. GluA1 knockout mice, however, showed greater suppression to a recent stimulus than to a nonrecent stimulus. Thus, GluA1 is not necessary for encoding, but affects the way that short-term memory is expressed.     

Deletion of the GluA1 AMPA receptor subunit impairs recency-dependent object recognition memory

Deletion of the GluA1 AMPA receptor subunit impairs short-term spatial recognition memory. It has been suggested that short-term recognition depends upon memory caused by the recent presentation of a stimulus that is independent of contextual-retrieval processes. The aim of the present set of experiments was to test whether the role of GluA1 extends to nonspatial recognition memory. Wild-type and GluA1 knockout mice were tested on the standard object recognition task and a context-independent recognition task that required recency-dependent memory. In a first set of experiments it was found that GluA1 deletion failed to impair performance on either of the object recognition or recency-dependent tasks. However, GluA1 knockout mice displayed increased levels of exploration of the objects in both the sample and test phases compared to controls. In contrast, when the time that GluA1 knockout mice spent exploring the objects was yoked to control mice during the sample phase, it was found that GluA1 deletion now impaired performance on both the object recognition and the recency-dependent tasks. GluA1 deletion failed to impair performance on a context-dependent recognition task regardless of whether object exposure in knockout mice was yoked to controls or not. These results demonstrate that GluA1 is necessary for nonspatial as well as spatial recognition memory and plays an important role in recency-dependent memory processes.     

Evidence for long-term spatial memory in a parid

Many animals use spatial memory. Although much work has examined the accuracy of spatial memory, few studies have explicitly focused on its longevity. The importance of long-term spatial memory for foraging has been demonstrated in several cases. However, the importance of such long-term memory for all animals is unclear. In this study, we present the first evidence that a parid species (the black-capped chickadee, Poecile atricapillus) can remember the location of a single food item for at least 6 months under an associative-learning spatial memory paradigm with multiple reinforcements. We did not detect a significant difference in memory longevity between two populations of chickadees shown previously to differ in short-term spatial memory and hippocampal morphology, an area of the brain involved in spatial memory. Our study showed that small birds such as parids can maintain spatial memories for long periods, a feat shown previously only in corvids. Moreover, we were able to demonstrate this longevity within the context of only 16 repeated trials. We speculate that this ability may potentially be useful in relocating caches if reinforced by repeated visits. Future studies are necessary to test whether our results were specifically due to multiple reinforcements of the food-containing location and whether parids may have similar memory longevity during food-caching experiences in the wild.     

Odor preference learning and memory modify GluA1 phosphorylation and GluA1 distribution in the neonate rat olfactory bulb: testing the AMPA receptor hypothesis in an appetitive learning model

An increase in synaptic AMPA receptors is hypothesized to mediate learning and memory. AMPA receptor increases have been reported in aversive learning models, although it is not clear if they are seen with memory maintenance. Here we examine AMPA receptor changes in a cAMP/PKA/CREB-dependent appetitive learning model: odor preference learning in the neonate rat. Rat pups were given a single pairing of peppermint and 2 mg/kg isoproterenol, which produces a 24-h, but not a 48-h, peppermint preference in the 7-d-old rat pup. GluA1 PKA-dependent phosphorylation peaked 10 min after the 10-min training trial and returned to baseline within 90 min. At 24 h, GluA1 subunits did not change overall but were significantly increased in synaptoneurosomes, consistent with increased membrane insertion. Immunohistochemistry revealed a significant increase in GluA1 subunits in olfactory bulb glomeruli, the targets of olfactory nerve axons. Glomerular increases were seen at 3 and 24 h after odor exposure in trained pups, but not in control pups. GluA1 increases were not seen as early as 10 min after training and were no longer observed 48 h after training when odor preference is no longer expressed behaviorally. Thus, the pattern of increased GluA1 membrane expression closely follows the memory timeline. Further, blocking GluA1 insertion using an interference peptide derived from the carboxyl tail of the GluA1 subunit inhibited 24 h odor preference memory providing causative support for our hypothesis. PKA-mediated GluA1 phosphorylation and later GluA1 insertion could, conjointly, provide increased AMPA function to support both short-term and long-term appetitive memory.     

Competitive short-term and long-term memory processes in spatial habituation

Exposure to a spatial location leads to habituation of exploration such that, in a novelty preference test, rodents subsequently prefer exploring a novel location to the familiar location. According to Wagner's (1981) theory of memory, short-term and long-term habituation are caused by separate and sometimes opponent processes. In the present study, this dual-process account of memory was tested. Mice received a series of exposure training trials to a location before receiving a novelty preference test. The novelty preference was greater when tested after a short, rather than a long, interval. In contrast, the novelty preference was weaker when exposure training trials were separated by a short, rather than a long interval. Furthermore, it was found that long-term habituation was determined by the independent effects of the amount of exposure training and the number of exposure training trials when factors such as the intertrial interval and the cumulative intertrial interval were controlled. A final experiment demonstrated that a long-term reduction of exploration could be caused by a negative priming effect due to associations formed during exploration. These results provide evidence against a single-process account of habituation and suggest that spatial habituation is determined by both short-term, recency-based memory and long-term, incrementally strengthened memory.     

Activation and binding in verbal working memory: a dual-process model for the recognition of nonwords

The article presents a mathematical model of short-term recognition based on dual-process models and the three-component theory of working memory [Oberauer, K. (2002). Access to information in working memory: Exploring the focus of attention. Journal of Experimental Psychology: Learning, Memory, and Cognition, 28, 411-421]. Familiarity arises from activated representations in long-term memory, ignoring their relations; recollection retrieves bindings in the capacity-limited component of working memory. In three experiments participants encoded two short lists of nonwords for immediate recognition, one of which was then cued as irrelevant. Probes from the irrelevant list were rejected more slowly than new probes; this was also found with probes recombining letters of irrelevant nonwords, suggesting that familiarity arises from individual letters independent of their relations. When asked to accept probes whose letters were all in the relevant list, regardless of their conjunction, participants accepted probes preserving the original conjunctions faster than recombinations, showing that recollection accessed feature bindings automatically. The model fit the data best when familiarity depended only on matching letters, whereas recollection used binding information.     

Adult age differences in short-term memory and subsequent long-term memory for actions.

Short-term memory for actions was investigated for young adult and elderly adult subjects with the Brown-Peterson procedure at retention intervals of 0 and 15 s. The short-term memory trials were followed by the long-term recall of the prior to-be-remembered actions. The 15-s retention interval was filled either with no activity or with 1 of 3 different interfering activities. Verbal interference had little effect on short-term memory at either age level. Actions performed in the interval either by the subjects or by the experimenter produced significantly lower recall scores at each age level, with the decrement being more pronounced for the elderly than for the young subjects. The long-term memory results indicated that successful short-term recall enhanced later long-term recall, regardless of age level.     

Adult age differences in short-term memory for serial order: data and a model

Age-related deficits in short-term memory have been widely reported, but reduced overall scores could reflect increased order errors, increased omissions, or increased intrusions. Different explanations for reduced short-term memory with aging lead to different predictions. In this study, young (n = 68; M age = 20 years) and older (n = 99; M age = 65 years) adults were presented with lists of letters and were asked to recall each list immediately in the correct order. Age differences in error patterns were similar for auditory and visual presentation. For example, older adults made more errors of every type, and a greater proportion of the older adults' errors were omissions. An additional condition, in which older adults were encouraged to guess, ruled out an age increase in response threshold as a full explanation for the results. The data were modeled by an oscillator-based computational model of memory for serial order. A good fit to the aging data was achieved by simultaneously altering two parameters that were interpreted as corresponding to frontal decline and response slowing.     

The short-term storage as a buffer memory between long-term storage and the motor system: A simultaneous-processing model

It is assumed that in a free-recall task the short-term store serves as a memory buffer between the long-term store and a final motor stage of word production. Because of this the retrieval process in long-term store is not hindered by the final motor stage of word production since continued output from the long-term store queues in the buffer for motoric processing. Otherwise a time consuming communication between the two processes would be necessary. A stochastic model of this conceptualization is provided to predict the temporal course of free recall as well as a paradigm in which the contribution of the short-term store in free recall can be studied. The experimental results from this paradigm were used to test the model and to estimate short-term storage capacity on the basis of the time course of free recall. The model predictions were in good agreement with the data and the capacity estimate coincides well with estimates found by totally different methods reported in the literature.     

Independence of long-term contextual memory and short-term perceptual hypotheses: Evidence from contextual cueing of interrupted search

Observers are able to resume an interrupted search trial faster relative to responding to a new, unseen display. This finding of rapid resumption is attributed to short-term perceptual hypotheses generated on the current look and confirmed upon subsequent looks at the same display. It has been suggested that the contents of perceptual hypotheses are similar to those of other forms of memory acquired long-term through repeated exposure to the same search displays over the course of several trials, that is, the memory supporting “contextual cueing.” In three experiments, we investigated the relationship between short-term perceptual hypotheses and long-term contextual memory. The results indicated that long-term, contextual memory of repeated displays neither affected the generation nor the confirmation of short-term perceptual hypotheses for these displays. Furthermore, the analysis of eye movements suggests that long-term memory provides an initial benefit in guiding attention to the target, whereas in subsequent looks guidance is entirely based on short-term perceptual hypotheses. Overall, the results reveal a picture of both long- and short-term memory contributing to reliable performance gains in interrupted search, while exerting their effects in an independent manner.     

Verbal and visuospatial short-term memory in children: Evidence for common and distinct mechanisms

This study was designed to identify whether verbal and visuospatial short-term memory performance in children is served by common or distinct mechanisms. Five- and 8-year-old children were tested on their verbal recall of spoken letter names and digits, and on their recall of tapped sequences of blocks. The performance of the children on the verbal and visuospatial serial recall tasks was largely unrelated, extending evidence for dissociable memory systems found in adults. Detailed characteristics of recall, such as serial position functions, migration patterns, and distribution of error types, were similar in the tasks requiring recall of letters and of blocks, although order errors predominated in the block but not the letter recall task for the older children. These results appear to reflect the application of common processes specialized for the extraction of serial order information from the phonological and visuospatial components of short-term memory.     

Preservation of long-term memory and synaptic plasticity despite short-term impairments in the Tc1 mouse model of Down syndrome

Down syndrome (DS) is a genetic disorder arising from the presence of a third copy of the human chromosome 21 (Hsa21). Recently, O’Doherty and colleagues in an earlier study generated a new genetic mouse model of DS (Tc1) that carries an almost complete Hsa21. Since DS is the most common genetic cause of mental retardation, we have undertaken a detailed analysis of cognitive function and synaptic plasticity in Tc1 mice. Here we show that Tc1 mice have impaired spatial working memory (WM) but spared long-term spatial reference memory (RM) in the Morris watermaze. Similarly, Tc1 mice are selectively impaired in short-term memory (STM) but have intact long-term memory (LTM) in the novel object recognition task. The pattern of impaired STM and normal LTM is paralleled by a corresponding phenotype in long-term potentiation (LTP). Freely-moving Tc1 mice exhibit reduced LTP 1 h after induction but normal maintenance over days in the dentate gyrus of the hippocampal formation. Biochemical analysis revealed a reduction in membrane surface expression of the AMPAR (α-amino-3-hydroxy-5-methyl-4-propionic acid receptor) subunit GluR1 in the hippocampus of Tc1 mice, suggesting a potential mechanism for the impairment in early LTP. Our observations also provide further evidence that STM and LTM for hippocampus-dependent tasks are subserved by parallel processing streams.     

Neural substrates of successful working memory and long-term memory formation in a relational spatial memory task

Working memory (WM) tasks may involve brain activation actually implicated in long-term memory (LTM). In order to disentangle these two memory systems, we employed a combined WM/LTM task, using a spatial relational (object-location) memory paradigm and analyzed which brain areas were associated with successful performance for either task using fMRI. Critically, we corrected for the performance on the respective memory task when analyzing subsequent memory effects. The WM task consisted of a delayed-match-to-sample task assessed in an MRI scanner. Each trial consisted of an indoor or outdoor scene in which the exact configuration of four objects had to be remembered. After a short delay (7–13 s), the scene was presented from a different angle and spatial recognition for two objects was tested. After scanning, participants received an unexpected subsequent recognition memory (LTM) task, where the two previously unprobed objects were tested. Brain activity during encoding, delay phase and probe phase was analyzed based on WM and LTM performance. Results showed that successful WM performance, when corrected for LTM performance, was associated with greater activation in the inferior frontal gyrus and left fusiform gyrus during the early stage of the maintenance phase. A correct decision during the WM probe was accompanied by greater activation in a wide network, including bilateral hippocampus, right superior parietal gyrus and bilateral insula. No voxels exhibited supra-threshold activity during the encoding phase, and we did not find any differential activity for correct versus incorrect trials in the WM task when comparing LTM correct versus LTM incorrect trials.     

Long-term inhibition of return for spatial locations: Evidence for a memory retrieval account

It has generally been accepted that attention is inhibited from returning to previously attended locations, and that this inhibition of return (IOR) lasts just two or three seconds. Recently, Tipper, Grison, and Kessler (2003) showed that IOR can occur over much longer periods of time provided the inhibition is encoded with a context-rich event. Here we examine standard (i.e., typical time range) and long-term IOR within the same experimental paradigm as a means to compare their properties. Experiment 1 used the simple displays typical of cueing paradigms and revealed that both standard and long-term IOR can be obtained under such conditions. Experiment 2 showed that both standard and long-term IOR occurred when there was incongruence between the required response on the current trial and that stored in memory. Furthermore, IOR was not produced when there was incongruence between a target feature (colour) of the current trial and that stored in memory. These results are consistent with a memory retrieval account of IOR and suggest that the same inhibitory mechanism may underlie both standard and long-term IOR.     

Memory for targets in a multilevel simulated environment: Evidence for vertical asymmetry in spatial memory

In two experiments, adult participants explored a symmetrical three-tiered computer-simulated building that contained six distinctive objects, two on each floor. Following exploration, the objects were removed, and the participants were asked to make direction judgments from each floor, indicating the former positions of the objects on that floor and on higher and lower floors. Relative tilt error scores indicated a bias, in that targets that were higher than the test location were judged as consistently lower than their actual positions and targets that were lower than the test location were judged as consistently higher than their actual positions. Absolute tilt errors revealed an asymmetry, with more accurate and less variable tilt errors for judgments directed to lower floors than for judgments directed to higher floors. Experiment 3 ruled out an account of the findings that does not relate them to spatial memory. The results suggest that the superiority of downward over upward spatial judgments, previously reported in two-dimensional visual-spatial tasks, extends to navigational spatial memory.     

Word frequency and receiver operating characteristic curves in recognition memory: evidence for a dual-process interpretation

Dual-process models of the word-frequency mirror effect posit that low-frequency words are recollected more often than high-frequency words, producing the hit rate differences in the word-frequency effect, whereas high-frequency words are more familiar, producing the false-alarm-rate differences. In this pair of experiments, the authors demonstrate that the analysis of receiver operating characteristic (ROC) curves provides critical information in support of this interpretation. Specifically, when participants were required to discriminate between studied nouns and their plurality reversed complements, the ROC curve was accurately described by a threshold model that is consistent with recollection-based recognition. Further, the plurality discrimination ROC curves showed characteristics consistent with the interpretation that participants recollected low-frequency items more than high-frequency items.     

Neonatal tactile stimulation enhances spatial working memory, prefrontal long-term potentiation, and D1 receptor activation in adult rats

Environmental stimuli during neonatal periods play an important role in the development of cognitive function. In this study, we examined the long-term effects of neonatal tactile stimulation (TS) on spatial working memory (SWM) and related mechanisms. We also investigated whether TS-induced effects could be counteracted by repeated short periods of maternal separation (MS). Wistar rat pups submitted to TS were handled and marked transiently per day during postnatal days 2–9 or 10–17. TS/MS pups were stimulated in the same way as TS pups and then individually separated from their mother for 1 h/day. Their nontactile stimulated (NTS) siblings served as controls. In adulthood, TS and TS/MS rats showed better performance in two versions of the delayed alternation task and superior in vivo long-term potentiation of the hippocampo–prefrontal cortical pathway when compared with controls. Furthermore, there were more doses of A77636 (a selective dopamine D1 agonist) to significantly improve SWM performance in TS and TS/MS rats than in NTS rats, suggesting that activation of prefrontal D1 receptors in TS and TS/MS rats is more optimal for SWM function than in NTS rats. MS did not counteract TS-induced effects because no significant difference was found between TS/MS and TS animals. These data indicate that in early life, external tactile stimulation leads to long-term facilitative effects in SWM-related neural function.     

Transformations on sets in short-term memory: Temporal and spatial factors influencing deletion

An individual’s ability to perform a deletion operation on sets in short-term memory was explored in a reaction time (RT) experiment. Special attention was given to the importance, for deletion, of temporal and spatial variables. Ss did perform a deletion operation. The speed of correct recognition was influenced by both the delay between the deletion (D) set and a test item and the serial order correspondence between identical items in the to-be-remembered or positive (P) set and the D set.     

On the nature of nonverbal working memory fractionation: a case of selective spatial short-term memory deficit in a child

Several lines of research on adult subjects demonstrate a visual/spatial fractionation of nonverbal working memory (WM), while behavioral studies on normal children support the idea of a static/dynamic distinction. In the present paper, we report a child (Z.M.) who failed on nonverbal WM tasks. To verify the nature of his defect, we carried out two experiments: in Experiment 1, Z.M. failed on spatial WM tasks but not on visual WM tasks and was not affected by the static/dynamic format of stimulus presentation; in Experiment 2, this visual/spatial dissociation was extended to the imagery domain. These results are best accounted for within the visual/spatial fractionation of WM and confirmed the role of WM in mental imagery. Clinical and rehabilitative implications of the present findings are also discussed.     

Serial position effects in visual short-term memory for words and abstract spatial patterns

Two experiments tested the effects of list postion, and retention-interval in recognition for two distinct stimulus categories in young adults. Stimulus categories were spatial abstract patterns and words presented on a computer screen. At short delay intervals recency effects predominates and at longer delay intervals a primacy effect predominates in both experiments, indicating similar basic memory processes producing the serial position functions for the two different categories of visual stimuli, but as length of retention-interval increases, memory for first list items improves for words and remains constant for abstract patterns. Recency functions are similar for both stimulus categories tested.