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.

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.

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.

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.

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.

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.

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.

Abstract-concept learning in Black-billed magpies (Pica hudsonia).

relational concepts depend upon relationships between stimuli (e.g., same vs. different) and transcend features of the training stimuli. Recent evidence shows that learning abstract concepts is shared across a variety species including birds. Our recent work with a highly-skilled food-storing bird, Clark's nutcracker, revealed superior same/different abstract-concept learning compared to rhesus monkeys, capuchin monkeys, and pigeons. Here we test a more social, but less reliant on food-storing, corvid species, the Black-billed magpie (Pica hudsonia). We used the same procedures and training exemplars (eight pairs of the same rule, and 56 pairs of the different rule) as were used to test the other species. Magpies (n = 10) showed a level of abstract-concept learning that was equivalent to nutcrackers and greater than the primates and pigeons tested with these same exemplars. These findings suggest that superior initial abstract-concept learning abilities may be shared across corvids generally, rather than confined to those strongly reliant on spatial memory.

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.

Event-based proactive interference in rhesus monkeys.

Three rhesus monkeys (Macaca mulatta) were tested in a same/different memory task for proactive interference (PI) from prior trials. PI occurs when a previous sample stimulus appears as a test stimulus on a later trial, does not match the current sample stimulus, and the wrong response "same" is made. Trial-unique pictures (scenes, objects, animals, etc.) were used on most trials, except on trials where the test stimulus matched potentially interfering sample stimulus from a prior trial (1, 2, 4, 8, or 16 trials prior). Greater interference occurred when fewer trials separated interference and test. PI functions showed a continuum of interference. Delays between sample and test stimuli and intertrial intervals were manipulated to test how PI might vary as a function of elapsed time. Contrary to a similar study with pigeons, these time manipulations had no discernable effect on the monkey's PI, as shown by compete overlap of PI functions with no statistical differences or interactions. These results suggested that interference was strictly based upon the number of intervening events (trials with other pictures) without regard to elapsed time. The monkeys' apparent event-based interference was further supported by retesting with a novel set of 1,024 pictures. PI from novel pictures 1 or 2 trials prior was greater than from familiar pictures, a familiar set of 1,024 pictures. Moreover, when potentially interfering novel stimuli were 16 trials prior, performance accuracy was actually greater than accuracy on baseline trials (no interference), suggesting that remembering stimuli from 16 trials prior was a cue that this stimulus was not the sample stimulus on the current trial-a somewhat surprising conclusion particularly given monkeys.

Concept learning set-size functions for Clark's nutcrackers.

Same/Different abstract-concept learning by Clark's nutcrackers (Nucifraga columbiana) was tested with novel stimuli following learning of training set expansion (8, 16, 32, 64, 128, 256, 512, and 1024 picture items). The resulting set-size function was compared to those from rhesus monkeys (Macaca mulatta), capuchin monkeys (Cebus apella), and pigeons (Columba livia). Nutcrackers showed partial concept learning following initial eight-item set learning, unlike the other species (Magnotti, Katz, Wright, & Kelly, 2015). The mean function for the nutcrackers' novel-stimulus transfer increased linearly as a function of the logarithm of training set size, which intersected its baseline function at the 128-item set size. Thus, nutcrackers on average achieved full concept learning (i.e., transfer statistically equivalent to baseline performance) somewhere between set sizes of 64 to 128 items, similar to full concept learning by monkeys. Pigeons required a somewhat larger training set (256 items) for full concept learning, but results from other experiments (initial training and transfer with 32- and 64-item set sizes) suggested carryover effects with smaller set sizes may have artificially prolonged the pigeon's full concept learning. We find it remarkable that these diverse species with very different neural architectures can fully learn this same/different abstract concept, and (at least under some conditions) do so with roughly similar sets sizes (64-128 items) and numbers of training exemplars, despite initial concept learning advantages (nutcrackers), learning disadvantages (pigeons), or increasing baselines (monkeys).

Pigeon visual short-term memory directly compared to primates.

Three pigeons were trained to remember arrays of 2-6 colored squares and detect which of two squares had changed color to test their visual short-term memory. Procedures (e.g., stimuli, displays, viewing times, delays) were similar to those used to test monkeys and humans. Following extensive training, pigeons performed slightly better than similarly trained monkeys, but both animal species were considerably less accurate than humans with the same array sizes (2, 4 and 6 items). Pigeons and monkeys showed calculated memory capacities of one item or less, whereas humans showed a memory capacity of 2.5 items. Despite the differences in calculated memory capacities, the pigeons' memory results, like those from monkeys and humans, were all well characterized by an inverse power-law function fit to d' values for the five display sizes. This characterization provides a simple, straightforward summary of the fundamental processing of visual short-term memory (how visual short-term memory declines with memory load) that emphasizes species similarities based upon similar functional relationships. By closely matching pigeon testing parameters to those of monkeys and humans, these similar functional relationships suggest similar underlying processes of visual short-term memory in pigeons, monkeys and humans.

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.

Monkey visual short-term memory directly compared to humans.

Two adult rhesus monkeys were trained to detect which item in an array of memory items had changed using the same stimuli, viewing times, and delays as used with humans. Although the monkeys were extensively trained, they were less accurate than humans with the same array sizes (2, 4, & 6 items), with both stimulus types (colored squares, clip art), and showed calculated memory capacities of about 1 item (or less). Nevertheless, the memory results from both monkeys and humans for both stimulus types were well characterized by the inverse power-law of display size. This characterization provides a simple and straightforward summary of a fundamental process of visual short-term memory (STM; how VSTM declines with memory load) that emphasizes species similarities based upon similar functional relationships. By more closely matching monkey testing parameters to those of humans, the similar functional relationships strengthen the evidence suggesting similar processes underlying monkey and human VSTM.

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.

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.

Explorations of object and location memory using fMRI.

Content-specific sub-systems of visual working memory (VWM) have been explored in many neuroimaging studies with inconsistent findings and procedures across experiments. The present study employed functional magnetic resonance imaging (fMRI) and a change detection task using a high number of trials and matched stimulus displays across object and location change (what vs. where) conditions. Furthermore, individual task periods were studied independently across conditions to identify differences corresponding to each task period. Importantly, this combination of task controls has not previously been described in the fMRI literature. Composite results revealed differential frontoparietal activation during each task period. A separation of object and location conditions yielded a distributed system of dorsal and ventral streams during the encoding of information corresponding to bilateral inferior parietal lobule (IPL) and lingual gyrus activation, respectively. Differential activity was also shown during the maintenance of information in middle frontal structures bilaterally for objects and the right IPL and left insula for locations. Together, these results reflect a domain-specific dissociation spanning several cortices and task periods. Furthermore, differential activations suggest a general caudal-rostral separation corresponding to object and location memory, respectively.

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.

Episodic memory: a rat model of source memory.

A recent study using a novel procedure to test the memory of rats for a preferred (chocolate) reinforcement shows many key characteristics that define source memory and episodic memory in humans.

Visual object complexity limits pigeon short-term memory.

The study of visual memory has repeatedly shown qualitatively similar visual short-term memory (VSTM) systems between human and many nonhuman species. In studies of human VSTM using change detection, increasing visual object complexity has an inverse effect on accuracy. In the current study, we assessed the functional relationship between visual object complexity and memory performance in visual change detection in pigeons and humans. Visual object complexity was quantified for each object type within each species using visual target search. Change detection performance was inversely related to object complexity in both species, suggesting that pigeon VSTM, like human VSTM, is limited by visual object complexity. Human participants were able to use a verbal-labeling strategy to mitigate some of the effect of visual object complexity, suggesting a qualitative difference in how the two species may solve certain visual discriminations. Considering the visual complexity of novel objects may also help explain previous failures to transfer relational rules to novel visual objects.