Short-term memory for order but not for item information is impaired in developmental dyslexia

Recent findings suggest that people with dyslexia experience difficulties with the learning of serial order information during the transition from short- to long-term memory (Szmalec et al. Journal of Experimental Psychology: Learning, Memory, & Cognition 37(5): 1270-1279, 2011). At the same time, models of short-term memory increasingly incorporate a distinction of order and item processing (Majerus et al. Cognition 107: 395-419, 2008). The current study is aimed to investigate whether serial order processing deficiencies in dyslexia can be traced back to a selective impairment of short-term memory for serial order and whether this impairment also affects processing beyond the verbal domain. A sample of 26 adults with dyslexia and a group of age and IQ-matched controls participated in a 2?×?2?×?2 experiment in which we assessed short-term recognition performance for order and item information, using both verbal and nonverbal material. Our findings indicate that, irrespective of the type of material, participants with dyslexia recalled the individual items with the same accuracy as the matched control group, whereas the ability to recognize the serial order in which those items were presented appeared to be affected in the dyslexia group. We conclude that dyslexia is characterized by a selective impairment of short-term memory for serial order, but not for item information, and discuss the integration of these findings into current theoretical views on dyslexia and its associated dysfunctions.     

Short-term memory for visual and auditory stimuli in pigeons

Separate groups of pigeons were trained to perform symbolic delayed matching to sample with auditory and visual sample stimuli. For animals in the auditory group, ambient tones that varied in frequency served as sample stimuli; for animals in the visual group, ambient red and green lights served as sample stimuli. In both cases, the sample stimuli were mapped onto the yellow and blue comparison stimuli presented on left and right pecking keys. In Experiments 1 and 2, it was found that visual and auditory delayed matching were affected in the same ways by several temporal variables: delay, length of exposure to the sample stimulus, and intertrial interval. In Experiments 3, 4A, and 4B, a houselight presented during the delay interval strongly interfered with retention in both visual and auditory groups, but white noise presented during the delay had little effect in either group. These results seem to be more in line with a prospective memory model, in which visual and auditory sample stimuli are coded into the same instructional memories, than with a model based on concepts of retrospective memory and modality specificity.     

Similarities between human and animal spatial memory: Item and order information

Human subjects, sitting at the center of a circle of eight lights, were tested on analogues of radial-maze item-recognition (Roberts & Smythe, 1979) and order-recognition (Kesner & Novak, 1982) tasks. Subjects in the item-recognition condition saw a list of seven lights, and then the nonlist (eighth) light was tested against the first, fourth, or seventh light from the list. The subjects were required to point toward the nonlist light. Subjects in the order-recognition condition saw a series of eight lights, followed by a test of the first and second, fourth and fifth, or seventh and eighth serial positions. They were asked to point toward the light with the earlier serial position. Subjects’ item-recognition serial-position curves exhibited a recency effect with a 0-sec retention interval (Experiments 1 and 2), and were U-shaped (Experiment 1) or flat (Experiment 2) with a 30-sec retention interval. Subjects’ order-recognition serial-position curves were U-shaped at both retention intervals. Subjects’ reported mnemonics were, generally, unrelated to their choice accuracy. The results suggest analogous memory processes in animals and humans.     

Contextual stimuli and memory retrieval in pigeons

Pigeons were given free-operant successive discrimination training in which, on alternate days, two different interdimensional problems were employed (color positive and line angle negative; a different color negative and a different line angle positive). Between days, these problems could be construed as intradimensional ones. For one group, training was conducted on each problem in the presence of the same ambient (contextual) stimuli, while for a second group each problem was trained in a different context. For a third group, these two contexts were randomly related to the problems. Postdiscrimination stimulus generalization gradients showed that peak shifts were obtained in both the same context and the random context groups, but no peak shifts were found for the group which learned each problem in a different context. Results were consistent with Spear’s (1973) treatment of animal memory which attributes retention test performance to the operation of a “context-elicited” retrieval process. An alternative uniprocess conditioning account of these and similar data was also discussed.     

Errors in pigeons’ memory for number of events

In Experiment 1, pigeons were trained in a within-subjects design to discriminate sequences of light flashes (illumination of the feeder) that varied in number, but not in time (2f/4sec and 8f/4sec), and in time, but not in number (4f/2sec and 4f/8sec). Number samples required a response to one of two comparison dimensions (either color or line), whereas time samples required a response to the remaining comparison dimension. Delay testing revealed a significant choose-small bias following number samples and a significant choose-long bias following time samples. In Experiment 2, testing confirmed that in the absence of a sample, there was a bias to respond small to the number comparisons and long to the time comparisons. Additional tests indicated that the birds were discriminating time samples on the basis of the number of light flashes occurring during the last few seconds of the time samples, rather than on the basis of the total duration of the flash sequence. Consequently, the choose-long bias observed for time samples during delay testing was really a choose-small bias. In Experiment 3, the birds received baseline training with a 5-sec delay and were subsequently tested at shorter and longer delays. A choose-large bias occurred at delays shorter than the baseline training delay, whereas a choose-small bias was again observed at delays longer than the baseline delay. These findings provide additional empirical support for the conceptualizing of memory for number and time in terms of a common mechanism.     

Short-term spatial memory in honeybees

Foraging honeybees were trained individually in two-choice spatial problems. Differentially rewarded for spatial alternation in Experiment 1 (“win-shift” training), they showed instead a clear tendency to perseverate—that is, to prefer on each trial the location of reward on the immediately preceding trial. On the basis of the results of Experiments 2 and 3, in which one location was rewarded over shorter or longer series of consecutive trials, an associative interpretation of the perseveration found in the first experiment was rejected in favor of an interpretation in terms of short-term spatial memory. Experiment 4, in which the animals were rewarded on each trial for choosing either location, also showed perseveration. Honeybees, like rats, seem to remember a rewarded location recently visited, but tend to return to it rather than, like rats, to avoid it.     

The recency effect in pigeons’ long-term memory

Four experiments are reported in which pigeons first learned one wavelength discrimination (green S+, yellow S?) and then the reversal; finally, after various delays, they were tested for wavelength generalization in extinction. In Experiment 1, the two problems were learned in different contexts; testing in Context 1 produced maximal responding to green in only half of the subjects, even when testing was delayed 30 days. In Experiment 2, testing of the subjects repeatedly in both contexts showed good control by each context after a 30-day delay. In Experiment 3, both problems were learned in the same context, and all gradients showed recency, peaking at yellow, even after 30 days. In Experiment 4, the subjects learned a series of reversals in the same context, terminating in yellow, S+, green, S?, and their gradients peaked at yellow, even after a 30-day delay. In Experiments 3 and 4, the gradients became flatter with increasing delays, and they were flatter in Experiment 4 (after three reversals) than in Experiment 3 (after one reversal). The location of the peak was not affected by delay, but only by testing in a context that had been uniquely associated with Problem 1 (Experiments 1 and 2). It is proposed that the location of gradient peaks indicates what is being remembered, whereas the slope of the obtained gradients indicates how well the target memory has been retrieved.     

Systematic errors in pigeons’ memory for event duration: Interaction between training and test delay

Pigeons trained to choose different stimuli following short- and long-duration signals make disproportionately more “short” choices (i.e., “choose-short errors”) following an increase in the retention interval and more “choose-long errors” following a decrease in this delay. The present experiment provided a systematic investigation of how these selective errors depend on the relationship between the training delay and the test delay. Pigeons were first trained with a 0-sec delay between the signal (2- or 8-sec food presentations) and the choice stimuli (red- and blue-lit keys). On subsequent test trials with 5- and 10-sec delays, choose-short errors predominated. Next, the birds were trained with a constant 10-sec delay and then tested with shorter or longer delays on some trials. The birds now responded accurately and without selective errors at the 10-sec training delay, but made choose-long errors at shorter delays and choose-short errors at longer delays. Finally, the birds were trained with a constant 20-sec delay and then tested with shorter and longer delays. Choose-long errors again appeared at shorter test delays, choose-short errors at longer test delays, and no differential errors at the 20-sec training delay. The selectivity of these errors generally increased with the absolute difference between the training and test delay. Theoretical implications of these results are discussed.     

Delayed matching in pigeons with food and no-food samples: Further examination of backward associations

When pigeons are trained on a delayed conditional discrimination with presence versus absence samples and tested with delays, a bias to choose the comparison associated with the absence sample is observed with increasing delay. Additionally, when the samples consist of food versus no food, this trial-type performance difference is reversed on short-delay trials: a bias to choose the comparison associated with the presence sample develops with delay testing. This reversal in comparison bias at short delays has been attributed to a preference produced by backward associations between the hedonic samples and the nonhedonic choice stimuli. In the present experiment, we tested an alternative hypothesis, that the short-delay comparison bias is produced by proactive interference—in particular, from reinforcement obtained on the previous trial—by including a group trained with reinforcement on only half of the trials with a correct response. According to the proactive interference account, this group should have shown a smaller short-delay comparison bias than would the typical 100% reinforcement group. Instead, consistent with a backward-association interpretation, the magnitude of the short-delay comparison bias shown by the 50% group was significantly greater than that shown by the 100% group.     

The effect of scopolamine on reference and working memory in pigeons

A comparison of the effects of scopolamine hydrobromide on working memory and reference memory in White Carneaux pigeons was undertaken by means of a modified delayed matching-to-sample procedure. Performance on working-memory trials was disrupted by decreases in sample duration and intertriai interval and by increases in delay interval. Performance on reference memory trials was not disrupted by any of these parametric manipulations. In Experiment 1, the pigeons received injections of scopolamine hydrobromide (0.01, 0.05, or 0.1 mg/kg), scopolamine methyl bromide (0.1 mg/kg), or saline prior to test sessions. In Experiment 2, the pigeons received injections of scopolamine hydrobromide (0.01 or 0.03 mg/kg), scopolamine methyl bromide (0.03 mg/kg), or saline. In both experiments, scopolamine hydrobromide had greater disruptive effects on working-memory trials than on reference-memory trials. The centrally active form of scopolamine disrupted working-memory trial accuracy more than the peripherally active form. However, no drug dose × delay interval interaction was obtained. Thus, the interference on working-memory-trial accuracy produced by central cholinergic blockade would not appear to be due to alterations in the active maintenance of information during the delay interval.     

Processing of conflicting and redundant stimulus information by pigeons

Selective attention in processing of visual information by pigeons, trained on alternating sessions with two colors (red and green) and two forms (a diamond and an X shape) differentially associated with a left—right key choice task, was examined. A color and a form were presented together on probe trials during sessions in which, on other trials, only one of the dimensions, color or form, was shown. The dimension in effect on the surrounding trials had no influence on choice when the information provided by the two dimensions on probe trials was in conflict—color correct for one choice and form for the other. When both color and form redundantly cued the correct choice, there was no increase in accuracy in comparison with that associated with one dimension. Following separate training on the color and form discriminations, pigeons appeared to base their choices on color on some trials, on form on other trials, but not on both simultaneously. These findings are discussed in terms of an exemplar model of information processing.     

Short-term memory for haptic cues in monkeys (Macaca mulatta)

Short-term memory (STM) for haptic information was examined in a delayed matching-to-sample (DMTS) task. Three rhesus monkeys were tested in DMTS with all possible combinations of different-size spheres and cubes as the sample and comparison stimuli. The results showed that the decrease in percentage correct as a function of the retention intervals was relatively independent of the size and shape of the sample and comparison stimuli. In general, at each retention interval, percentage correct was higher when the (1) comparison stimuli differed in both size and shape than when the comparison stimuli differed in only size or shape, (2) size differences between the comparison stimuli increased, and (3) samples were spheres rather than cubes. This pattern of results suggests that dimensions of the haptic stimuli influenced discrimination but had little effect on the animals’ STM. In Experiment 2, the same three monkeys responded to the sample and comparison stimuli with the same hand or responded to the sample with one hand and the comparison stimuli with the opposite hand. The decrease in percentage correct across retention intervals was comparable for all possible hand combinations. These results suggest that the loss of information from STM is comparable when the sample and comparison stimuli are both felt with the same hand or with opposite hands.     

Spatial memory and the performance of rats and pigeons in the radial-arm maze

The resource-distribution hypothesis states that the ability of an animal to remember the spatial location of past events is related to the typical distribution of food resources for the species. It appears to predict that Norway rats would perform better than domestic pigeons in tasks requiring spatial event memory. Pigeons, tested in an eight-arm radial maze, exhibited no more than half of the memory capacity observed in rats in the same apparatus and may not have used spatial memory at all. The results were interpreted as supporting the hypothesis.     

Alterations in the memory code for temporal events induced by differential outcome expectancies in pigeons

The effect of differential outcome expectancies on memory for temporal and nontemporal information was examined. Pigeons were trained to match short (2-sec) and long (8-sec) sample durations to red and green comparison stimuli, and vertical and horizontal lines to vertical and horizontal comparison stimuli. In Experiment 1, one differential outcome (DO) group received food for correct choices on short-sample trials, whereas another received food for correct choices on long-sample trials. On line-orientation trials, half of each DO group received food for correct responses following vertical samples, whereas the other half received food for correct responses following horizontal samples. Overall retention was greater in the DO groups than in a nondifferential (NDO) group that received either food or no food for correct responses on a random half of all trials. Furthermore, although the NDO group displayed a choose-short bias for temporal samples, both DO groups displayed equivalent biases to select the comparison stimulus associated with food. In Experiment 2, differential outcome expectancies were extinguished off-baseline. Subsequently, in the first nondifferential outcome test session, the. DO groups performed less, accurately than the NDO group. These findings indicate that temporal samples are not retrospectively and analogically coded when they are differentially associated with food and no food. Instead, they are remembered in terms of the corresponding outcome expectancies.     

Developmental changes in item and source memory: evidence from an ERP recognition memory study with children, adolescents, and adults

Event-related potential (ERP) correlates of item and source memory were assessed in 18 children (7-8 years), 20 adolescents (13-14 years), and 20 adults (20-29 years) performing a continuous recognition memory task with object and nonobject stimuli. Memory performance increased with age and was particularly low for source memory in children. The ERP difference between first presentations of objects and nonobjects, reflecting generic novelty processing, showed only small developmental changes. Regarding item memory, adults showed the putative ERP correlates of familiarity and recollection, whereas ERP effects in children and adolescents suggested a strong reliance on recollection. ERP correlates of source memory refined with age, suggesting maturation of strategic recollection between childhood and adolescence and the development of postretrieval control until adulthood.     

A comparison of the short-term memory performances of pigeons and jackdaws

Two experiments employed a delayed conditional discrimination procedure in which half the trials began with the presentation of food and half with no food; following a retention interval, subjects were presented with a choice between red and green keys, a response to one of which was reinforced according to whether the trial had started with food or no food. In Experiment 1, after 38 training sessions during which the retention interval was gradually increased, pigeons performed at a moderate level with intervals of 5 to 7.5 sec. A final test produced a steep forgetting function for food trials, but not for no-food trials; performance was unaffected by the duration of the intertriai interval (10 or 40 sec). Experiment 2 used the delayed conditional discrimination procedure to compare short-term memory in jackdaws (Corvus monedulus) with that in pigeons. Although the performance of the jackdaws was below that of the pigeons at the start of training, they showed more rapid learning over long delays, and, in the final test, a shallower forgetting function for food trials than that shown by pigeons. The results suggested superior short-term memory in jackdaws, which may help to explain the better performance of corvids in general when compared with that of pigeons in certain complex learning tasks.     

Characteristics of pigeons’ spatial working memory in an open-field task

Although pigeons seem to require special training before they will display accurate spatial working memory in radial-arm mazes, they readily show accurate working memory for recently visited feeder locations in an open-field analog of the radial maze. In this task, pigeons forage among sites located on the floor of an open room, with no constraints on the path they take between sites. Experiment 1 suggested that pigeons’ working memory for recently visited sites is facilitated if they are permitted to develop a stable reference memory “map” of the location of the sites with respect to landmarks in the room: Pigeons for which the landmarks remained constant from day to day displayed more accurate working memory than did pigeons for which the landmarks were rearranged between daily trials. The second experiment investigated the durability of pigeons’ working memory, using a forced-choice procedure. Accuracy remained high for retention intervals of up to 32 min, but dropped significantly with a 2-h delay.