Sociality and social learning in two species of corvids: the pinyon jay (Gymnorhinus cyanocephalus) and the Clark's nutcracker (Nucifraga columbiana)

The hypothesis that social learning is an adaptive specialization for social living predicts that social species should learn better socially than they do individually, but that nonsocial species should not exhibit a similar enhancement of performance under social learning conditions. The authors compared individual and social learning abilities in 2 corvid species: the highly social pinyon jay (Gymnorhinus cyanocephalus) and the less social Clark's nutcracker (Nucifraga columbiana). The birds were tested on 2 different tasks under individual and social learning conditions. Half learned a motor task individually and a discrimination task socially; the other half learned the motor task socially and the discrimination task individually. Pinyon jays learned faster socially than they did individually, but nutcrackers performed equally well under both learning conditions. Results support the hypothesis that social learning is an adaptive specialization for social living in pinyon jays.     

Serial reversal learning and the evolution of behavioral flexibility in three species of North American corvids (Gymnorhinus cyanocephalus, Nucifraga columbiana, Aphelocoma californica)

In serial reversal learning, subjects learn to respond differentially to 2 stimuli. When the task is fully acquired, reward contingencies are reversed, requiring the subject to relearn the altered associations. This alternation of acquisition and reversal can be repeated many times, and the ability of a species to adapt to this regimen has been considered as an indication of behavioral flexibility. Serial reversal learning of 2-choice discriminations was contrasted in 3 related species of North American corvids: pinyon jays (Gymnorhinus cyanocephalus), which are highly social; Clark's nutcrackers (Nucifraga columbiana), which are relatively solitary but specialized for spatial memory; and western scrub jays (Aphelocoma californica), which are ecological generalists. Pinyon jays displayed significantly lower error rates than did nutcrackers or scrub jays after reversal of reward contingencies for both spatial and color stimuli. The effect was most apparent in the 1st session following each reversal and did not reflect species differences in the rate of initial discrimination learning. All 3 species improved their performance over successive reversals and showed significant transfer between color and spatial tasks, suggesting a generalized learning strategy. The results are consistent with an evolutionary association between behavioral flexibility and social complexity.     

Sun compass orientation in seed-caching corvids: its role in spatial memory

The role of sun compass orientation in spatial memory of Clark’s nutcrackers, Nucifraga columbiana, and pinyon jays, Gymnorhinus cyanocephalus, was studied in a series of cache recovery experiments. Birds were tested in an octagonal outdoor aviary with sand-filled cups inserted in the floor. For caching, only 12 such cups in a 90° sector were available, while for recovery 4–7 days later all 48 cups in the entire aviary were open. In control tests, the birds concentrated their search activity in the sector where they had cached. When their internal clock was shifted 6 h between caching and recovery, pinyon jays shifted their search activity to the 90° adjacent sector, as predicted if the sun compass was used. Clark’s nutcrackers did not respond to the first clock-shift; however, they, too, shifted their search activity after a second clock-shift back to normal. This suggests that the sun compass is a component of spatial memory in both species. Clark’s nutcrackers, however, seem to rely on their sun compass to a lesser degree than pinyon jays or the previously studied scrub jays. A comparison of the findings indicates that the role of the sun in spatial memory might reflect differences in habitat and ecology of the three corvid species. Received: 18 February 1999 / Accepted after revision: 17 September 1999     

Species differences in spatial memory among Clark's nutcrackers, scrub jays, and pigeons.

An operant nonmatching to sample procedure was used to compare the spatial memory abilities of 3 avian species. A trial consisted of the presentation of a spatially defined sample, a delay interval, and a 2-choice test during which the correct location was the new location. A single spatial location served as the sample in Experiment 1. The delay interval was manipulated using a titration procedure. In Experiment 2, 1, 2, or 3 sequentially illuminated locations served as the sample. The delay was 1 of 4 predetermined intervals. In Experiment 3, sample presentation was the same as Experiment 2, but the delay interval was titrated. In all of the experiments, the performance of nutcrackers was consistently better than the performance of scrub jays and pigeons (Experiment 1) and was correlated with differences in their foraging ecology.     

Development of reference and working spatial memory in preschool children

Three groups of preschool children (aged 18 to 28, 33 to 42, and 47 to 58 months) were given a radial search test similar to the radial arm maze used with nonhuman subjects. The children searched for chocolate sweets among 10 labeled locations in a room, 5 of which were baited with a sweet. Older children outperformed the intermediate group, who in turn outperformed the youngest group in requiring fewer choices to retrieve all of the sweets. Working memory and reference memory aspects of performance were then separated: Reference memory (restriction of choices to the baited subset) in older children was superior to that in the youngest group but not to that in the intermediate group. In terms of working memory (avoidance of repeat responses to already visited locations), the older group made fewer errors than the intermediate group, who, in turn, made fewer errors than the youngest group. We concluded that working and reference components of spatial memory in children may share common elements, perhaps the ability to recognize places as familiar, although reference memory may develop earlier than working memory.     

Memory development in the second year: for events or locations?

We employed an object-placement/object-removal design, inspired by recent work on 'episodic-like' memory in scrub jays (Clayton, N. S., & Dickinson, A. (1998). Episodic-like memory during cache recovery by scrub jays. Nature, 395, 272-274), to examine the possibility that children in the second year of life have event-based memories. In one task, a successful search could have been due to the recall of an object-removal event. In the second task, a successful search could only have been caused by recall of where objects were located. Success was general in the oldest group of children (21-25 months), while performance was broadly similar on the two tasks. The parsimonious interpretation of this outcome is that the first task was performed by location memory, not by event memory. We place these data in the context of object permanence development.     

Rhesus monkeys (Macaca mulatta) demonstrate robust memory for what and where,but not when,in an open-field test of memory

We adapted a paradigm developed by Clayton and Dickinson (1998), who demonstrated memory for what, where, and when in scrub jays, for use with rhesus monkeys. In the study phase of each trial, monkeys found a preferred and a less-preferred food reward in a trial-unique array of three locations in a large room. After 1 h, monkeys returned to the test room, where they found foods placed as during study. Twenty-five hours after the study phase monkeys again searched the room, but now the preferred food was replaced with a distasteful food remnant, while the less-preferred food was still present. Although monkeys remembered the locations of the foods for up to 25 h, they did not learn that the preferred food was available after the short, but not after the long delay. Thus, monkeys demonstrated long-term memory for the type and location of food but failed to demonstrate sensitivity to when they acquired that knowledge.     

Anterior but not intralaminar thalamic nuclei support allocentric spatial memory

Medial thalamic damage is a common cause of severe memory disruption in humans. Both the anterior thalamic nuclei (ATN) and the intralaminar thalamic nuclei (ILN) have been suggested as primary sites of diencephalic injury underlying learning and memory deficits, but their respective roles have yet to be resolved. The present study explicitly compared two spatial memory tasks in male PVGc hooded rats with selective neurotoxic lesions to either (1) the ATN or (2) the rostral ILN (and adjacent lateral mediodorsal thalamic nuclei; ILN/LT lesions). As predicted, the ATN group, but not the ILN/LT group, exhibited clear deficits in the Morris water maze task for the initial acquisition of a fixed hidden platform and its reversal to a new position. The second task examined acquisition of egocentric spatial reference memory for a left or right body turn, using any three arms in an 8-arm water maze on any given trial; contrary to predictions, both lesion groups performed as well as the Sham group. The lack of deficits in ILN/LT rats on this second task contrasted with previous findings reporting a detrimental effect of ILN/LT lesions on egocentric working memory. The clear dissociation between the influence of ATN and ILN/LT lesions with respect to allocentric spatial reference memory in the Morris maze emphasizes that caution is required when interpreting the effects of non-ATN thalamic lesions on spatial memory when the lesions encroach substantial areas of the adjacent ATN region.     

A comparison of the effects of fimbria-fornix, hippocampal, or entorhinal cortex lesions on spatial reference and working memory in rats: short versus long postsurgical recovery period.

Using a radial maze task and different postoperative recovery periods, this experiment assessed and compared the reference and working memory performances of adult Long-Evans male rats subjected to entorhinal cortex, fimbria-fornix, and hippocampus lesions. Sham-operated rats were used as controls. In order to see whether the duration of the postsurgical recovery period would influence acquisition of the complex radial maze task, training began 1 month following surgery (Delay 1) for half the rats in each group, while for the other half training was started 6.5 months following surgery (Delay 2). The results indicated that at both recovery periods the entorhinal cortex lesions failed to affect either working or reference memory in the spatial task. Conversely, both fimbria-fornix and hippocampus lesions impaired both reference and working memory. While the reference memory deficit was generally similar in both fimbria-fornix and hippocampal lesion groups, analysis of the results for working memory indicated that at the longer delay rats with fimbria-fornix lesions were still impaired but in animals that had the hippocampus removed, working memory did not differ from that of controls. These results suggest that there was some recovery in those rats with hippocampal lesions (e.g., on the working memory task) but both hippocampal and fimbria-fornix animals were still impaired compared to controls when training was delayed 6.5 months following the operations.     

Search strategies used by APP transgenic mice during navigation in the Morris water maze

TgCRND8 mice represent a transgenic mouse model of Alzheimer's disease, with onset of cognitive impairment and increasing amyloid-beta plaques in their brains at 12 weeks of age. In this study, the spatial memory in 25- to 30-week-old TgCRND8 mice was analyzed in two reference and one working memory Morris water maze (MWM) tests. In reference memory tests, the mice were trained to escape to a hidden platform, which in one version of the test was marked by a visual cue. In the working memory test, the hidden platform was moved daily to different locations. The TgCRND8 mice were impaired in reference memory when trained in a hidden platform test. However, the mice developed spatial memory comparable to non-Tg littermates in a cued reference memory test. The mice showed also an impairment in spatial working memory. Analysis of search paths revealed that in contrast to non-Tg littermates, TgCRND8 mice did not use spatial strategies during their navigation. Instead, they learned to locate an escape platform using a nonspatial, chaining strategy. The study showed that (1) the impairment in the reference memory of TgCRND8 mice was reduced when a hidden platform was cued, and that (2) both working and reference memory systems of TgCRND8 mice, but not (3) the plasticity of choice between search strategies, are compromised by the transgene-induced pathology.     

Memory systems in the rat: effects of reward probability,context, and congruency between working and reference memory

The interaction of working and reference memory was studied in rats on an eight-arm radial maze. In two experiments, rats were trained to perform working memory and reference memory tasks. On working memory trials, they were allowed to enter four randomly chosen arms for reward in a study phase and then had to choose the unentered arms for reward in a test phase. On reference memory trials, they had to learn to visit the same four arms on the maze on every trial for reward. Retention was tested on working memory trials in which the interval between the study and test phase was 15 s, 15 min, or 30 min. At each retention interval, tests were performed in which the correct WM arms were either congruent or incongruent with the correct RM arms. Both experiments showed that congruency interacted with retention interval, yielding more forgetting at 30 min on incongruent trials than on congruent trials. The effect of reference memory strength on the congruency effect was examined in Experiment 1, and the effect of associating different contexts with working and reference memory on the congruency effect was studied in Experiment 2.     

东莨菪碱对大鼠空间参考记忆和工作记忆的不同影响

观察东莨菪碱对空间参考记忆和空间工作记忆的编码、保持和提取过程的作用。应用Morris水迷宫实验测定大鼠的空间参考记忆和空间工作记忆,分别在训练的不同阶段腹腔注射东莨菪碱（1mg/kg）和相同容量的生理盐水,比较各东莨菪碱组和生理盐水组之间游泳潜伏期、路径长度、轨迹和游泳速度的差异。结果发现：与注射生理盐水相比,在训练前和探测实验前注射东莨菪碱的大鼠在探测实验中对目标象限不表现出空间偏爱,说明东莨菪碱干扰参考记忆的信息编码和提取过程;而在训练结束后注射东莨菪碱的大鼠探测实验的结果与生理盐水组相比没有显著差异,说明东莨菪碱对参考记忆的保持过程没有影响。在工作记忆实验中,无论第一次测试前、第一次测试后和第2次测试前注射东莨菪碱,均造成大鼠游泳潜伏期延长,说明东莨菪碱干扰工作记忆的编码、保持和提取过程。研究提示M受体在空间工作记忆和参考记忆中发挥不同作用     

Scrub jays (Aphelocoma coerulescens) remember the relative time of caching as well as the location and content of their caches

Two experiments examined whether food-storing scrub jays (Aphelocoma coerulescens) could remember when they cached particular food items as well as what they cached and where. In Experiment 1, scrub jays cached and recovered perishable "wax worms" (wax moth larvae) and nonperishable peanuts in 2 visuospatially distinct and trial-unique trays. The birds searched preferentially for fresh wax worms if they had cached them 4 hr earlier but rapidly learned to search for peanuts and avoid decayed wax worms that had been cached 124 hr previously. This pattern also was observed when the food items were removed before recovery on test trials. These results were replicated in Experiment 2 using a procedure in which both types of food were cached in different sides of the same caching tray: On the basis of a single, trial-unique experience, scrub jays could remember the relative time of caching as well as what type of food was cached in each cache site.     

Prefrontal cortex and hippocampus subserve different components of working memory in rats

Both the medial prefrontal cortex (mPFC) and hippocampus are implicated in working memory tasks in rodents. Specifically, it has been hypothesized that the mPFC is primarily engaged in the temporary storage and processing of information lasting from a subsecond to several seconds, while the hippocampal function becomes more critical as the working memory demand extends into longer temporal scales. Although these structures may be engaged in a temporally separable manner, the extent of their contributions in the "informational content" of working memory remains unclear. To investigate this issue, the mPFC and dorsal hippocampus (dHPC) were temporarily inactivated via targeted infusions of the GABA(A) receptor agonist muscimol in rats prior to their performance on a delayed alternation task (DAT), employing an automated figure-eight maze that required the animals to make alternating arm choice responses after 3-, 30-, and 60-sec delays for water reward. We report that inactivation of either the mPFC or dHPC significantly reduced DAT at all delay intervals tested. However, there were key qualitative differences in the behavioral effects. Specifically, mPFC inactivation selectively impaired working memory (i.e., arm choice accuracy) without altering reference memory (i.e., the maze task rule) and arm choice response latencies. In contrast, dHPC inactivation increased both reference memory errors and arm choice response latencies. Moreover, dHPC, but not mPFC, inactivation increased the incidence of successive working memory errors. These results suggest that while both the mPFC and hippocampus are necessarily involved in DAT, they seem to process different informational components associated with the memory task.     

Scrub jays (Aphelocoma coerulescens) form integrated memories of the multiple features of caching episodes

Four experiments examined whether food-storing scrub jays remember when and where they cached different foods. The scrub jays cached and recovered perishable and nonperishable foods in visuospatially distinct and trial-unique cache sites. They rapidly learned to avoid searching for foods that had perished by the time of recovery, while continuing to search for the same foods after shorter retention intervals when the foods were still fresh. The temporal control of searching at recovery was also observed when the familiarity of cache sites did not provide any information about the time of caching and when the same food was cached in distinct sites at different times. The authors argue that the jays formed an integrated memory for the location and time of caching of particular foods.     

Strategy selection in a task with spatial and nonspatial components: effects of fimbria-fornix lesions in rats.

The main purpose of the present research was to investigate the ability of rats to learn a 12-arm radial maze task that requires the concurrent utilization of both spatial and intramaze cue information. The task involves in a single trial both place and cue learning as well as reference memory (RM) and working memory (WM). Since the animal can choose place and cue arms in any order, the strategies employed to learn the task can be studied as well as the kinds of memory errors that are made. The results of Experiment 1 showed that the number of errors made on the place and cue components of the task did not differ, and that more RM than WM errors were made early during learning. As the task was learned, the animals tended to choose the place arms before choosing the intramaze cue arms, thus suggesting that a spatial strategy was employed first followed by a cue strategy. In Experiment 2 lesions of the fimbria-fornix resulted in temporary impairments in both RM and WM that were especially apparent on the spatial component of the task. The lesioned rats also switched from choosing mostly place arms early during the trial to choosing more cue arms. While fimbria-fornix lesioned rats recovered from the memory impairments with training, the change in response strategy persisted throughout postoperative testing. The procedure of combining both spatial and non-spatial components concurrently in the same task should prove of value in studying response strategies in animals.     

Spatial memory in rats: A cross validation study

Two experiments were performed to investigate whether two measures of spatial memory, working memory (WM) and reference memory (RM), can be generalized over learning situations. In the first experiment, outbred WU rats were used; in the second four inbred strains. In both experiments rats were given 50 training trials in both a holeboard and a high-sided radial maze: 4 out of 16 holes and 4 out of 8 arms were baited. The number of WM (revisits to baited holes/arms) and RM (visits and revisits to never baited holes/arms) errors were calculated for 5 blocks of 10 trials; odd-even reliabilities were determined for the last 20 trials and were shown to be satisfactory for both measures in both types of apparatus. Error-decrements were analyzed by trend components. For both WM and RM, simple and canonical correlations were determined between means and significant trends in maze and holeboard as a test for construct validity; in both experiments r's and R_c's were very low. It was concluded that the concepts WM and RM are not validly generalizable over tests.     

Evidence for neocortical involvement in reference memory

Rats were trained on an eight-arm radial maze task using a procedure that provides for an assessment of both working and reference memory. Following training, rats received parietal cortex, medial prefrontal cortex, visual cortex, or nucleus basalis magnocellularis lesions. Rats with visual cortex lesions showed no change in performance on either working or reference memory. Rats with parietal cortex lesions displayed a temporary deficit in reference, but no deficit on working memory. Animals with medial prefrontal cortex lesions showed a temporary deficit on both working and reference memory. Rats with extensive lateral frontal and parietal cortex depletion of acetylcholinesterase following nucleus basalis magnocellularis lesions had a marked disruption only of reference but not of working memory. It is concluded that neocortex and possibly the cholinergic projections to neocortex play an important role in mediating reference memory.     

Amphetamine disrupts both working and reference memories of rats trained in a radial maze

To assess the effects of amphetamine on working and reference memory rats were trained on a 12-arm radial maze with six arms baited and six arms unbaited until stable performance was achieved. Administration of 2.0 mg/kg d-amphetamine sulfate increased both working and reference memory errors, but only if a 5-min delay was imposed after three successful choices. With no delay this dose had no reliable effect on either working or reference memory. Lower doses (0.5 or 1.0 mg/kg) were ineffective even when a delay was imposed during the test. We suggest that amphetamine heightens arousal, which disrupts accurate retention when the rat's attention to the relevant cues is interrupted, as during a brief delay. Alternative explanations are discussed.     

Those cheating rats: male and female rats use odor trails in a water-escape "working memory" task.

Three-month-old Sprague-Dawley rats were trained on a working memory win-stay (spatial delayed matching-to-sample) water-escape task with the escape platform location the same for all subjects on a given trial, a procedure that maximizes the buildup of an odor trail to the escape platform. In subsequent tests during which the location of the escape platform varied randomly between subjects, the rats, especially the females, while continuing to perform above chance level, made increased errors. Varying the platform location between subjects eliminated odor trail as a nonambiguous cue for locating the escape platform. In a second experiment females performed better than males on a reference memory odor trail discrimination task which involved following the path of like-gender "pathmaker" rats to the escape platform. The relatively poor use of odor trails by the males was associated with a high frequency of choosing a preferred choice section or returning to the choice section selected first on the immediately preceding trial (perseveration). Collectively, the two experiments demonstrate that rats can use either working memory or odor trails to locate an escape platform in a water maze, and that they, especially females, will use odor trails in a working memory task if odor trails are available. Clearly, the location of the escape platform should be varied randomly between subjects in tests of working memory.