Same/different concept learning by primates and birds.

Same/different abstract-concept learning experiments were conducted with two primate species and three avian species by progressively increasing the size of the training stimulus set of distinctly different pictures from eight to 1,024 pictures. These same/different learning experiments were trained with two pictures presented simultaneously. Transfer tests of same and different learning employed interspersed trials of novel pictures to assess the level of correct performance on the very first time of subjects had seen those pictures. All of the species eventually performed these tests with high accuracy, contradicting the long-accepted notion that nonhuman animals are unable to learn the concept of same/different. Capuchin and rhesus monkeys learned the concept more readily than did pigeons. Clark's nutcrackers and black-billed magpies learned as readily as monkeys, and even showed a slight advantage with the smallest training stimulus sets. Those tests of same/different learning were followed by delay procedures, such that a delay was introduced after the subjects responded to the sample picture and before the test picture. In the sequential same/different task, accuracy was shown to diminish when the stimulus on a previous trial matched the test picture previously shown on a different trial. This effect is known as proactive interference. The pigeons' proactive interference was greater at 10-s delays than 1-s delays, revealing time-based interference. By contrast, time delays had little or no effect on rhesus monkeys' proactive interference, suggesting that rhesus monkeys have better explicit memory of where and when they saw the potential interfering picture, revealing better event-based memory.

Comparing cognition by integrating concept learning, proactive interference, and list memory.

This article describes an approach for training a variety of species to learn the abstract concept of same/different, which in turn forms the basis for testing proactive interference and list memory. The stimulus set for concept-learning training was progressively doubled from 8, 16, 32, 64, 128 . . . to 1,024 different pictures with novel-stimulus transfer following learning. All species fully learned the same/different abstract concept: capuchin and rhesus monkeys learned more readily than pigeons; nutcrackers and magpies were at least equivalent to monkeys and transferred somewhat better following initial training sets. A similar task using the 1,024-picture set plus delays was used to test proactive interference on occasional trials. Pigeons revealed greater interference with 10-s than with 1-s delays, whereas delay time had no effect on rhesus monkeys, suggesting that the monkeys' interference was event based. This same single-item same/different task was expanded to a 4-item list memory task to test animal list memory. Humans were tested similarly with lists of kaleidoscope pictures. Delays between the list and test were manipulated, resulting in strong initial recency effects (i.e., strong 4th-item memory) at short delays and changing to a strong primacy effect (i.e., strong 1st-item memory) at long delays (pigeons 0-s to 10-s delays; monkeys 0-s to 30-s delays; humans 0-s to 100-s delays). Results and findings are discussed in terms of these species' cognition and memory comparisons, evolutionary implications, and future directions for testing other species in these synergistically related tasks.

Corvids Outperform Pigeons and Primates in Learning a Basic Concept.

Corvids (birds of the family Corvidae) display intelligent behavior previously ascribed only to primates, but such feats are not directly comparable across species. To make direct species comparisons, we used a same/different task in the laboratory to assess abstract-concept learning in black-billed magpies ( Pica hudsonia). Concept learning was tested with novel pictures after training. Concept learning improved with training-set size, and test accuracy eventually matched training accuracy-full concept learning-with a 128-picture set; this magpie performance was equivalent to that of Clark's nutcrackers (a species of corvid) and monkeys (rhesus, capuchin) and better than that of pigeons. Even with an initial 8-item picture set, both corvid species showed partial concept learning, outperforming both monkeys and pigeons. Similar corvid performance refutes the hypothesis that nutcrackers' prolific cache-location memory accounts for their superior concept learning, because magpies rely less on caching. That corvids with "primitive" neural architectures evolved to equal primates in full concept learning and even to outperform them on the initial 8-item picture test is a testament to the shared (convergent) survival importance of abstract-concept learning.

Monkeys and humans take local uncertainty into account when localizing a change.

Since sensory measurements are noisy, an observer is rarely certain about the identity of a stimulus. In visual perception tasks, observers generally take their uncertainty about a stimulus into account when doing so helps task performance. Whether the same holds in visual working memory tasks is largely unknown. Ten human and two monkey subjects localized a single change in orientation between a sample display containing three ellipses and a test display containing two ellipses. To manipulate uncertainty, we varied the reliability of orientation information by making each ellipse more or less elongated (two levels); reliability was independent across the stimuli. In both species, a variable-precision encoding model equipped with an "uncertainty-indifferent" decision rule, which uses only the noisy memories, fitted the data poorly. In both species, a much better fit was provided by a model in which the observer also takes the levels of reliability-driven uncertainty associated with the memories into account. In particular, a measured change in a low-reliability stimulus was given lower weight than the same change in a high-reliability stimulus. We did not find strong evidence that observers took reliability-independent variations in uncertainty into account. Our results illustrate the importance of studying the decision stage in comparison tasks and provide further evidence for evolutionary continuity of working memory systems between monkeys and humans.

The oddity preference effect and the concept of difference in pigeons.

Previous work in discrimination learning has shown that nonmatching (oddity) tasks are learned faster and more accurately than comparable matching tasks. This learning advantage has been coined the oddity preference effect (Wright & Delius in Journal of Experimental Psychology: Animal Behavior Processes, 31, 425-432. doi: 10.1037/0097-7403.31.4.425 , 2005). Pigeons trained in a nonmatching task, following training in a same/different (S/D) task, learned the abstract concept of difference (Daniel et al., in Animal Cognition, 18(4), 831-837, 2015), but they did not show the expected faster acquisition or high levels of transfer from the oddity preference effect. In the present study, experimentally naïve pigeons were trained in an identical nonmatching task to examine whether they would show the oddity preference effect on abstract-concept learning. These experimentally naïve pigeons did show an oddity preference effect; their transfer to novel configurations was above chance with the initial (smallest) set size (3-item set) and was substantially more accurate than novel transfer in similar match-to-sample (MTS) or S/D tasks (Bodily et al., in Journal of Experimental Psychology: Animal Behavior Processes, 34, 178-184. doi: 10.1037/0097-7403.34.1.178 , 2008; Katz & Wright in Journal of Experimental Psychology: Animal Behavior Processes, 32, 80-86. doi: 10.1037/0097-7403.32.1.80 , 2006). As the number exemplars in the training set increased, transfer to novel configurations increased and reached equivalence to trained-stimulus performance with a 24-item set. Despite this transfer being equal to baseline performance with a 24-item set, subsequent transfers following training with larger set sizes declined before eventually rising again to baseline performance. This unusual set-size function (with inflection points at the 24- and 96-set sizes) suggests that these pigeons may have combined item-specific and relational learning strategies with differing emphasis as they acquired the abstract concept.

Abstract-concept learning of difference in pigeons.

Many species have demonstrated the capacity to learn abstract concepts. Recent studies have shown that the quantity of stimuli used during training plays a critical role in how subjects learn abstract concepts. As the number of stimuli available in the training set increases, so too does performance on novel combinations. The role of set size has been explored with learning the concept of matching and same/different but not with learning the concept of difference. In the present study, pigeons were trained in a non-matching-to-sample task with an initial training set of three stimuli followed by transfer tests to novel stimuli. The training set was progressively doubled eight times with learning and transfer following each expansion. Transfer performance increased from chance level (50 %) at the smallest set size to a level equivalent to asymptotic training performance at the two largest training set sizes (384, 768). This progressive novel-stimulus transfer function of a non-matching (difference) rule is discussed in comparison with results from a similar experiment where pigeons were trained on a matching rule.

Superior abstract-concept learning by Clark's nutcrackers (Nucifraga columbiana).

The ability to learn abstract relational concepts is fundamental to higher level cognition. In contrast to item-specific concepts (e.g. pictures containing trees versus pictures containing cars), abstract relational concepts are not bound to particular stimulus features, but instead involve the relationship between stimuli and therefore may be extrapolated to novel stimuli. Previous research investigating the same/different abstract concept has suggested that primates might be specially adapted to extract relations among items and would require fewer exemplars of a rule to learn an abstract concept than non-primate species. We assessed abstract-concept learning in an avian species, Clark's nutcracker (Nucifraga columbiana), using a small number of exemplars (eight pairs of the same rule, and 56 pairs of the different rule) identical to that previously used to compare rhesus monkeys, capuchin monkeys and pigeons. Nutcrackers as a group (N = 9) showed more novel stimulus transfer than any previous species tested with this small number of exemplars. Two nutcrackers showed full concept learning and four more showed transfer considerably above chance performance, indicating partial concept learning. These results show that the Clark's nutcracker, a corvid species well known for its amazing feats of spatial memory, learns the same/different abstract concept better than any non-human species (including non-human primates) yet tested on this same task.

The same type of visual working memory limitations in humans and monkeys.

Rhesus monkeys are widely used as an animal model for human memory, including visual working memory (VWM). It is, however, unknown whether the same principles govern VWM in humans and rhesus monkeys. Here, we tested both species in nearly identical change-localization paradigms and formally compared the same set of models of VWM limitations. These models include the classic item-limit model and recent noise-based (resource) models, as well as hybrid models that combine a noise-based representation with an item limit. By varying the magnitude of the change in addition to the typical set size manipulation, we were able to show large differences in goodness of fit among the five models tested. In spite of quantitative performance differences between the species, we find that the variable-precision model--a noise-based model--best describes the behavior of both species. Adding an item limit to this model does not help to account for the data. Our results suggest evolutionary continuity of VWM across primates and help establish the rhesus monkey as a model system for studying the neural substrates of multiple-item VWM.

Testing visual short-term memory of pigeons (Columba livia) and a rhesus monkey (Macaca mulatta) with a location change detection task.

Change detection is commonly used to assess capacity (number of objects) of human visual short-term memory (VSTM). Comparisons with the performance of non-human animals completing similar tasks have shown similarities and differences in object-based VSTM, which is only one aspect ("what") of memory. Another important aspect of memory, which has received less attention, is spatial short-term memory for "where" an object is in space. In this article, we show for the first time that a monkey and pigeons can be accurately trained to identify location changes, much as humans do, in change detection tasks similar to those used to test object capacity of VSTM. The subject's task was to identify (touch/peck) an item that changed location across a brief delay. Both the monkey and pigeons showed transfer to delays longer than the training delay, to greater and smaller distance changes than in training, and to novel colors. These results are the first to demonstrate location-change detection in any non-human species and encourage comparative investigations into the nature of spatial and visual short-term memory.

How to be proactive about interference: lessons from animal memory.

Processes of proactive interference were explored using the pigeon as a model system of memory. This study shows that proactive interference extends back in time at least 16 trials (and as many minutes), revealing a continuum of interference and providing a framework for studying memory. Pigeons were tested in a delayed same/different task containing trial-unique pictures. On interference trials, sample pictures from previous trials reappeared as test pictures on different trials. Proactive-interference functions showed greatest interference from the most recent trial and with the longer of two delays (10 s vs. 1 s). These interference functions are accounted for by a time-estimation model based on signal detection theory. The model predicts that accuracy at test is determined solely by the ratio of the elapsed time since the offset of the current-trial sample to the elapsed time since the offset of the interfering sample. Implications for comparing memory of different species and different types of memory (e.g., familiarity vs. recollection) are discussed.

WITHDRAWN: fMRI correlates of visual working memory: What vs. where.

This article has been withdrawn at the request of the authors. The Publisher apologizes for any inconvenience this may cause. The full Elsevier Policy on Article Withdrawal can be found at http://www.elsevier.com/locate/withdrawalpolicy. This article has been withdrawn at the request of the editor. The Publisher apologizes for any inconvenience this may cause. The full Elsevier Policy on Article Withdrawal can be found at http://www.elsevier.com/locate/withdrawalpolicy.

Differential outcomes facilitate same/different concept learning.

Commonly recognized, the training procedure one employs often affects the results they obtain. Here, we demonstrate for the first time that abstract-concept learning is affected by employing a differential-outcomes procedure. The differential-outcome effect has been shown to occur for item-specific strategies but has not been established for relational strategies. To test whether different-outcome expectancies can facilitate a relational strategy, eight pigeons were trained and tested in a two-item same/different task with pictures. After pecking an upper picture, they pecked a lower picture if the pictures were the same or a white rectangle if the pictures were different. Two groups of pigeons were rewarded with either different outcomes (sounds and food amounts) or same outcomes. Both groups were trained to criterion with successively larger picture sets (8-1,024 items) and were transfer tested with novel pictures following each acquisition. With the smallest training sets, neither group showed any novel-stimulus transfer. But after acquiring the task with 32 pictures, the different-outcomes group responded more accurately to novel pictures than the same-outcome group. As the training set-size increased, both groups' transfer performance converged and became equivalent to training performance. These results show for the first time that training with different outcomes facilitates abstract-concept learning.

Abstract-concept learning carryover effects from the initial training set in pigeons (Columba livia).

Three groups of pigeons were trained in a same/different task with 32, 64, or 1,024 color-picture stimuli. They were tested with novel transfer pictures. The training-testing cycle was repeated with training-set doublings. The 32-item group learned the same/different task as rapidly as a previous 8-item group and transferred better than the 8-item group at the 32-item training set. The 64- and 1,024-item groups learned the task only somewhat slower than other groups, but their transfer was better and equivalent to baseline performances. These results show that pigeons trained with small sets (e.g., 8 items) have carryover effects that hamper transfer when the training set is expanded. Without carryover effects (i.e., initial transfer from the 32- and 64-item groups), pigeons show the same degree of transfer as rhesus and capuchin monkeys at these same set sizes. This finding has implications for the general ability of abstract-concept learning across species with different neural architectures.

Sensory and working memory in a spatial change-detection task by pigeons and humans.

Judgements of items viewed less than 100 ms prior are predominantly supported by a sensory, or iconic, memory system. Iconic memory is of high-capacity, but is also volatile and limited in duration. Judgements after longer delays increasingly rely on a working memory system, which is lower in capacity and volatility than sensory memory, but is longer in duration. In four experiments, several factors (e.g., length of delay, number of items, time to view items, presence of a visual mask) were manipulated during a spatial change-detection task conducted with humans and pigeons. Both species were exposed to trials with an array of colored circles (2, 3, and 4 circles in Experiment 1 and 2a; 4, 6, and 8 circles in Experiment 2b) followed by a brief delay (0, 50, and 100 ms in Experiment 1a; 0, 100, and 1000 ms in Experiments 1b and 2), and then were presented with a test display in which the position of one of the items had changed. Pigeons, like humans, were less accurate in selecting the changed item with more items in the display and after longer delays. Pigeons were equally accurate on trials with 0 and 100-ms delays, but worse on trials with a 1000-ms delay; whereas, humans were equally accurate on 100-ms and 1000-ms delays, but better on 0-ms delay trials. Accurate change detection was disrupted in both species when a visual mask was inserted between the sample and test display after a short (100 ms), but not a long (1000 ms) delay. The results support similarity between species in the functional relationships between delay and memory systems, despite time course differences related to sensory memory.

An fMRI analysis of object priming and workload in the precuneus complex.

Drawings depicting familiar objects and unreal structures were presented twice, and participants (N=16) determined whether line drawings were real (familiar) or unreal (unfamiliar). The second presentation (repetition) of a drawing was typically responded to faster and more accurately than the first presentation and was accompanied by reduced activation in occipitotemporal (fusiform) and lateral precuneus regions, and increased activation in medial precuneus regions. The behavioral effects and reduced activations (e.g., lateral precuneus) on the second presentation were less pronounced for unreal objects than for real objects. Activation changes in the medial precuneus - increased activation on repetition and reduced activation for novel unreal objects - was further supported by the increased activation in this area during rest and reduced activation when workload was increased (i.e., processing novel unreal objects). The results from the present study in conjunction with those from several previous studies converge on the conclusion that the occipitotemporal and lateral regions of the precuneus are primarily involved in object priming, whereas the medial portion of precuneus primarily activates and deactivates as a function of workload.

Matching-to-sample abstract-concept learning by pigeons.

Abstract concepts--rules that transcend training stimuli--have been argued to be unique to some species. Pigeons, a focus of much concept-learning research, were tested for learning a matching-to-sample abstract concept. Five pigeons were trained with three cartoon stimuli. Pigeons pecked a sample 10 times and then chose which of two simultaneously presented comparison stimuli matched the sample. After acquisition, abstract-concept learning was tested by presenting novel cartoons on 12 out of 96 trials for 4 consecutive sessions. A cycle of doubling the training set followed by retraining and novel-testing was repeated eight times, increasing the set size from 3 to 768 items. Transfer performance improved from chance (i.e., no abstract-concept learning) to a level equivalent to baseline performance (>80%) and was similar to an equivalent function for same/different abstract-concept learning. Analyses assessed the possibility that item-specific choice strategies accounted for acquisition and transfer performance. These analyses converged to rule out item-specific strategies at all but the smallest set-sizes (3-24 items). Ruling out these possibilities adds to the evidence that pigeons learned the relational abstract concept of matching-to-sample.

Learning strategies in matching to sample: if-then and configural learning by pigeons.

Pigeons learned a matching-to-sample task with a split training-set design in which half of the stimulus displays were untrained and tested following acquisition. Transfer to the untrained displays along with no novel-stimulus transfer indicated that these pigeons learned the task (partially) via if-then rules. Comparisons to other performance measures indicated that they also partially learned the task via configural learning (learning the gestalt of the whole stimulus display). Differences in the FR-sample requirement (1 vs. 20) had no systematic effect on the type of learning or level of learning obtained. Differences from a previous study [Wright, A.A., 1997. Concept learning and learning strategies. Psychol. Sci. 8, 119-123] are discussed, including the effect of displaying the stimuli vertically (traditional display orientation) or horizontally from the floor.

Testing complex animal cognition: Concept learning, proactive interference, and list memory.

This article describes an approach for assessing and comparing complex cognition in rhesus monkeys and pigeons by training them in a sequence of synergistic tasks, each yielding a whole function for enhanced comparisons. These species were trained in similar same/different tasks with expanding training sets (8, 16, 32, 64, 128 … 1024 pictures) followed by novel-stimulus transfer eventually resulting in full abstract-concept learning. Concept-learning functions revealed better rhesus transfer throughout and full concept learning at the 128 set, versus pigeons at the 256 set. They were then tested in delayed same/different tasks for proactive interference by inserting occasional tests within trial-unique sessions where the test stimulus matched a previous sample stimulus (1, 2, 4, 8, 16 trials prior). Proactive-interference functions revealed time-based interference for pigeons (1, 10 s delays), but event-based interference for rhesus (no effect of 1, 10, 20 s delays). They were then tested in list-memory tasks by expanding the sample to four samples in trial-unique sessions (minimizing proactive interference). The four-item, list-memory functions revealed strong recency memory at short delays, gradually changing to strong primacy memory at long delays over 30 s for rhesus, and 10 s for pigeons. Other species comparisons and future directions are discussed.

Episodic Memory: Manipulation and Replay of Episodic Memories by Rats.

Rats exposed to variable-length, unique-odor lists were tested in distinctive contexts for odors second or forth from list-end. Accurate ability to recall odors backwards from the end of lists points to their ability to manipulate and replay odor-list episodic memories.

Generalization hypothesis of abstract-concept learning: learning strategies and related issues in Macaca mulatta, Cebus apella, and Columba livia.

The generalization hypothesis of abstract-concept learning was tested with a meta-analysis of rhesus monkeys (Macaca mulatta), capuchin monkeys (Cebus apella), and pigeons (Columba livia) learning a same/different (S/D) task with expanding training sets. The generalization hypothesis states that as the number of training items increases, generalization from the training pairs will increase and could explain the subjects' accurate novel-stimulus transfer. By contrast, concept learning is learning the relationship between each pair of items; with more training items subjects learn more exemplars of the rule and transfer better. Having to learn the stimulus pairs (the generalization hypothesis) would require more training as the set size increases, whereas learning the concept might require less training because subjects would be learning an abstract rule. The results strongly support concept or rule learning despite severely relaxing the generalization-hypothesis parameters. Thus, generalization was not a factor in the transfer from these experiments, adding to the evidence that these subjects were learning the S/D abstract concept.