Mechanisms of same/different concept learning in primates and avians

Mechanisms of same/different concept learning by rhesus monkeys, capuchin monkeys, and pigeons were studied in terms of how these species learned the task (e.g., item-specific learning versus relational learning) and how rapidly they learned the abstract concept, as the training set size was doubled. They had similar displays, training stimuli, test stimuli, and contingencies. The monkey species learned the abstract concept at similar rates and more rapidly than pigeons, thus showing a quantitative difference across species. All species eventually showed full concept learning (novel-stimulus transfer equivalent to baseline: 128-item set size for monkeys; 256-item set for pigeons), thus showing a qualitative similarity across species. Issues of stimulus regularity/symmetry, generalization from item pairs, and familiarity processing were not considered to be major factors in the final performances, converging on the conclusion that these species were increasingly controlled by the sample-test relationship (i.e., relational processing) leading to full abstract-concept learning.     

Conceptual thresholds for same and different in old-(Macaca mulatta) and new-world (Cebus apella) monkeys

Learning of the relational same/different (S/D) concept has been demonstrated to be largely dependent upon stimulus sets containing more than two items for pigeons and old-world monkeys. Stimulus arrays containing several images for use in same/different discrimination procures (e.g. 16 identical images vs. 16 nonidentical images) have been shown to facilitate and even be necessary for learning of relational concepts ( [Flemming et al., 2007], [Wasserman et al., 2001] and [Young et al., 1997]). In the present study, we investigate the threshold at which a new world primate, the capuchin (Cebus apella) may be able to make such a discrimination. Utilizing a method of increasing entropy, rather than conventional procedures of decreasing entropy, we demonstrate unique evidence that capuchin monkeys are readily capable of making 2-item relational S/D conditional discriminations. In another experiment, we examine the supposed level of difficulty in making S/D discriminations by rhesus monkeys (Macaca mulatta). Whereas pigeons (Columba livia) and baboons (Papio papio) have shown marked difficulty simultaneously discriminating same from different arrays at all when composed of fewer than 8 items each, rhesus monkeys seem to understand that pairs of stimuli connote sameness and difference just the same (Flemming et al., 2007). With sustained accurate performance of 2-item S/D discriminations, both experienced and task-naïve rhesus monkeys appear quite certain in their conceptual knowledge of same and different. We conclude that learning of the same/different relational concept may be less dependent upon high levels of entropy contrast than originally hypothesized for nonhuman primates.     

Same/Different Abstract Concept Learning by Archerfish (Toxotes chatareus)

While several phylogenetically diverse species have proved capable of learning abstract concepts, previous attempts to teach fish have been unsuccessful. In this report, the ability of archerfish (Toxotes chatareus) to learn the concepts of sameness and difference using a simultaneous two-item discrimination task was tested. Six archerfish were trained to either select a pair of same or different stimuli which were presented simultaneously. Training consisted of a 2-phase approach. Training phase 1: the symbols in the same and different pair did not change, thereby allowing the fish to solve the test through direct association. The fish were trained consecutively with four different sets of stimuli to familiarize them with the general procedure before moving on to the next training phase. Training phase 2: six different symbols were used to form the same or different pairs. After acquisition, same/different concept learning was tested by presenting fish with six novel stimuli (transfer test). Five fish successfully completed the first training phase. Only one individual passed the second training phase, however, transfer performance was consistent with chance. This individual was given further training using 60 training exemplars but the individual was unable to reach the training criterion. We hypothesize that archerfish are able to solve a limited version of the same/different test by learning the response to each possible stimulus configuration or by developing a series of relatively simple choice contingencies. We conclude that the simultaneous two-item discrimination task we describe cannot be successfully used to test the concepts of same and different in archerfish. In addition, despite considerable effort training archerfish using several tests and training methods, there is still no evidence that fish can learn an abstract concept-based test.     

Natural conceptual behavior in squirrel monkeys (saimiri sciureus): An experimental investigation

Natural conceptual discriminations have been tested in many different species, including pigeons and a variety of non-human primates. The ability of four male squirrel monkeys (Saimiri sciureus) to learn and use the natural concept ‘squirrel monkey’ was investigated in this study. After a training phase, subjects were presented with novel stimuli in transfer and test trials. All subjects performed at a rate significantly above chance on the first test trial (p<.001), indicating that squirrel monkeys can utilize natural concepts in the laboratory.     

Conceptualization of above and below relationships by an insect

Relational rules such as 'same' or 'different' are mastered by humans and non-human primates and are considered as abstract conceptual thinking as they require relational learning beyond perceptual generalization. Here, we investigated whether an insect, the honeybee (Apis mellifera), can form a conceptual representation of an above/below spatial relationship. In experiment 1, bees were trained with differential conditioning to choose a variable target located above or below a black bar that acted as constant referent throughout the experiment. In experiment 2, two visual stimuli were aligned vertically, one being the referent, which was kept constant throughout the experiment, and the other the target, which was variable. In both experiments, the distance between the target and the referent, and their location within the visual field was systematically varied. In both cases, bees succeeded in transferring the learned concept to novel stimuli, preserving the trained spatial relation, thus showing an ability to manipulate this relational concept independently of the physical nature of the stimuli. Absolute location of the referent into the visual field was not a low-level cue used by the bees to solve the task. The honeybee is thus capable of conceptual learning despite having a miniature brain, showing that such elaborated learning form is not a prerogative of vertebrates.     

Same/different concept learning by capuchin monkeys in matching-to-sample tasks

The ability to understand similarities and analogies is a fundamental aspect of human advanced cognition. Although subject of considerable research in comparative cognition, the extent to which nonhuman species are capable of analogical reasoning is still debated. This study examined the conditions under which tufted capuchin monkeys (Cebus apella) acquire a same/different concept in a matching-to-sample task on the basis of relational similarity among multi-item stimuli. We evaluated (i) the ability of five capuchin monkeys to learn the same/different concept on the basis of the number of items composing the stimuli and (ii) the ability to match novel stimuli after training with both several small stimulus sets and a large stimulus set. We found the first evidence of same/different relational matching-to-sample abilities in a New World monkey and demonstrated that the ability to match novel stimuli is within the capacity of this species. Therefore, analogical reasoning can emerge in monkeys under specific training conditions.     

Same or different? Abstract relational concept use in juvenile bamboo sharks and Malawi cichlids

Sorting objects and events into categories and concepts is an important cognitive prerequisite that spares an individual the learning of every object or situation encountered in its daily life. Accordingly, specific items are classified in general groups that allow fast responses to novel situations. The present study assessed whether bamboo sharks Chiloscyllium griseum and Malawi cichlids Pseudotropheus zebra can distinguish sets of stimuli (each stimulus consisting of two abstract, geometric objects) that meet two conceptual preconditions, i.e., (1) “sameness” versus “difference” and (2) a certain spatial arrangement of both objects. In two alternative forced choice experiments, individuals were first trained to choose two different, vertically arranged objects from two different but horizontally arranged ones. Pair discriminations were followed by extensive transfer test experiments. Transfer tests using stimuli consisting of (a) black and gray circles and (b) squares with novel geometric patterns provided conflicting information with respect to the learnt rule “choose two different, vertically arranged objects”, thereby investigating (1) the individuals’ ability to transfer previously gained knowledge to novel stimuli and (2) the abstract relational concept(s) or rule(s) applied to categorize these novel objects. Present results suggest that the level of processing and usage of both abstract concepts differed considerably between bamboo sharks and Malawi cichlids. Bamboo sharks seemed to combine both concepts—although not with equal but hierarchical prominence—pointing to advanced cognitive capabilities. Conversely, Malawi cichlids had difficulties in discriminating between symbols and failed to apply the acquired training knowledge on new sets of geometric and, in particular, gray-level transfer stimuli.     

The learning skills of primates: The rhesus macaque in comparative perspective

Twenty-month-old rhesus monkeys were tested in a modified discrimination-reversal paradigm, which was designed to distinguish abstract learning from stimulus-response associational learning. Previous studies indicate that talapoin monkeys learn associationally and great apes via forming abstract concepts. Adult rhesus monkeys are apparently capable of forming simple abstractions, but learn primarily through associational process. The results of this study show the adolescent rhesus monkeys to be associational learners, with their response patterns indicating more complexity than the talapoins but less than the adult rhesus monkeys. The data suggest that rhesus monkeys develop their low-level capacity of abstract learning with maturation.     

Species discrimination and concept formation by rhesus monkeys (Macaca mulatta)

There are 19 species in genusMacaca and some of them are living in sympatry (Fooden, 1980). Although inter-specific hybrids are relatively easy to produce under artificial conditions, hybridization does not occur naturally. What is preventing that among the species of genusMacaca? Three rhesus monkeys acquired a discrimination between pictures with rhesus monkeys and without rhesus monkeys. All subjects showed positive transfer of this discrimination to new pictures with rhesus monkeys and without rhesus monkeys. A further test showed that these monkeys could discriminate between pictures of rhesus monkeys and pictures of Japanese monkeys. The results suggest that rhesus monkeys recognize rhesus monkeys as a class, independent of the actual stimuli such as a picture or an individual monkey. The ability to recognize members of their own species and the opportunities for such learning may be an important factor preventing hybridization among the species of genusMacaca.     

Picture perception in monkeys and pigeons: Transfer of rightside-up versus upside-down discrimination of photographic objects across conceptual categories

Monkeys and pigeons were trained to discriminate between normally oriented full frontal pictures of humans and upside-down reversals of the same pictures as stimuli. Monkeys displayed a high level of transfer to the new pictures of full frontal and rear views of humans and silhouettes, but failed to transfer to the close-up and far human faces. Pigeons showed poorer transfer to the silhouettes and higher transfer to the far human faces than did monkeys. Further transfer tests were performed with non-human pictures, including monkeys, birds, mammals, and man-made objects. Pigeons failed to transfer to the non-human pictures. This indicates that the pigeons had learned to classify the pictures based on some concrete features specific to the humans and that the transfer to the new versions of human pictures could be explained by simple stimulus generalization based on perceptual similarity. Two out of four monkeys did transfer fairly well to the non-human pictures, except for the man-made objects. High levels of transfer to the non-human natural pictures suggested that the monkeys classified the pictures on the basis of the orientation of objects represented by the pictorial displays. A preliminary report was presented by the first author (M. J.) at the 13th Congress of the International Primatological Society, Nagoya, Japan, 1990. The present research was supported in part by a Grant-in-Aid for General Scientific Research, the Ministry of Education, Science, and Culture, No. 02301017 (principal researcher:Tadasu Oyama, Nihon University) to M. J. The monkey experiments were conducted at the Primate Research Institute, Kyoto University, and the pigeon experiments at the Department of Psychology, Chiba University.     

Conceptual learning by miniature brains

Concepts act as a cornerstone of human cognition. Humans and non-human primates learn conceptual relationships such as ‘same’, ‘different’, ‘larger than’, ‘better than’, among others. In all cases, the relationships have to be encoded by the brain independently of the physical nature of objects linked by the relation. Consequently, concepts are associated with high levels of cognitive sophistication and are not expected in an insect brain. Yet, various works have shown that the miniature brain of honeybees rapidly learns conceptual relationships involving visual stimuli. Concepts such as ‘same’, ‘different’, ‘above/below of’ or ‘left/right are well mastered by bees. We review here evidence about concept learning in honeybees and discuss both its potential adaptive advantage and its possible neural substrates. The results reviewed here challenge the traditional view attributing supremacy to larger brains when it comes to the elaboration of concepts and have wide implications for understanding how brains can form conceptual relations.     

Prenatal learning in an Australian songbird: habituation and individual discrimination in superb fairy-wren embryos

Embryos were traditionally considered to possess limited learning abilities because of the immaturity of their developing brains. By contrast, neonates from diverse species show behaviours dependent on prior embryonic experience. Stimulus discrimination is a key component of learning and has been shown by a handful of studies in non-human embryos. Superb fairy-wren embryos (Malurus cyaneus) learn a vocal password that has been taught to them by the attending female during incubation. The fairy-wren embryos use the learned element as their begging call after hatching to solicit more parental feeding. In this study, we test whether superb fairy-wren embryos have the capacity to discriminate between acoustical stimuli and whether they show non-associative learning. We measured embryonic heart rate response using a habituation/dishabituation paradigm with eggs sourced from nests in the wild. Fairy-wren embryos lowered their heart rate in response to the broadcasts of conspecific versus heterospecific calls, and in response to the calls of novel conspecific individuals. Thus, fairy-wrens join humans as vocal-learning species with known prenatal learning and individual discrimination.     

Auditory Same/Different Concept Learning and Generalization in Black-Capped Chickadees (Poecile atricapillus)

Abstract concept learning was thought to be uniquely human, but has since been observed in many other species. Discriminating same from different is one abstract relation that has been studied frequently. In the current experiment, using operant conditioning, we tested whether black-capped chickadees (Poecile atricapillus) could discriminate sets of auditory stimuli based on whether all the sounds within a sequence were the same or different from one another. The chickadees were successful at solving this same/different relational task, and transferred their learning to same/different sequences involving novel combinations of training notes and novel notes within the range of pitches experienced during training. The chickadees showed limited transfer to pitches that was not used in training, suggesting that the processing of absolute pitch may constrain their relational performance. Our results indicate, for the first time, that black-capped chickadees readily form relational auditory same and different categories, adding to the list of perceptual, behavioural, and cognitive abilities that make this species an important comparative model for human language and cognition.     

Prosimian learning capacities

A survey of the literature on learning by prosimian primates contradicts a traditional view that they are untrainable. They learn simple operants such as bar pressing readily, work well for the usual rewards, and respond in predictable fashion on schedules of partial reinforcement. Two-dimensional visual discriminations involving pattern and brightness also are learned, as are three-dimensional object discriminations. In the area of complex learning, they not only acquire a variety of difficult tasks, but they also reach a final level of performance that is at or near the level of anthropoids. In each of the following areas, at least one experiment is described in which a prosimian species did as well as one or more anthropoid species: object discrimination learning set, discrimination reversal, delayed response, instrumentation, oddity, and relational problems. The anthropoids to which they are most apt to compare favorably are New World monkeys, a group which they resemble physically, especially with respect to degree of manipulativeness, cortical development, and visual acuity.     

Characterization of the fecal microbiome from non-human wild primates reveals species specific microbial communities

Background

Host-associated microbes comprise an integral part of animal digestive systems and these interactions have a long evolutionary history. It has been hypothesized that the gastrointestinal microbiome of humans and other non-human primates may have played significant roles in host evolution by facilitating a range of dietary adaptations. We have undertaken a comparative sequencing survey of the gastrointestinal microbiomes of several non-human primate species, with the goal of better understanding how these microbiomes relate to the evolution of non-human primate diversity. Here we present a comparative analysis of gastrointestinal microbial communities from three different species of Old World wild monkeys.

Methodology/Principal Findings

We analyzed fecal samples from three different wild non-human primate species (black-and-white colobus [Colubus guereza], red colobus [Piliocolobus tephrosceles], and red-tailed guenon [Cercopithecus ascanius]). Three samples from each species were subjected to small subunit rRNA tag pyrosequencing. Firmicutes comprised the vast majority of the phyla in each sample. Other phyla represented were Bacterioidetes, Proteobacteria, Spirochaetes, Actinobacteria, Verrucomicrobia, Lentisphaerae, Tenericutes, Planctomycetes, Fibrobacateres, and TM7. Bray-Curtis similarity analysis of these microbiomes indicated that microbial community composition within the same primate species are more similar to each other than to those of different primate species. Comparison of fecal microbiota from non-human primates with microbiota of human stool samples obtained in previous studies revealed that the gut microbiota of these primates are distinct and reflect host phylogeny.

Conclusion/Significance

Our analysis provides evidence that the fecal microbiomes of wild primates co-vary with their hosts, and that this is manifested in higher intraspecies similarity among wild primate species, perhaps reflecting species specificity of the microbiome in addition to dietary influences. These results contribute to the limited body of primate microbiome studies and provide a framework for comparative microbiome analysis between human and non-human primates as well as a comparative evolutionary understanding of the human microbiome.     

Domain is a moving target for relational learning

The domain for relational learning was manipulated by varying the training set size for pigeons that had learned the same/different (S/D) concept. Six pigeons that had learned a S/D task with pairs of pictures with a set size of 1024 picture items had their training set size reduced to 8 items. Training on the reduced 8-item set was followed by transfer testing that was repeated four times. Transfer performance following reduction of the training set to 8 items was 9.2% less than it had been when the pigeons were trained with the 1024-item set, but 25.8% above chance. This partial abstract-concept learning remained constant over the four tests with novel stimuli. The results show that a broad domain established by a large expanding training set can once again become restricted by further training with a small training set.     

Suffixation influences receivers' behaviour in non-human primates

Compared to humans, non-human primates have very little control over their vocal production. Nonetheless, some primates produce various call combinations, which may partially offset their lack of acoustic flexibility. A relevant example is male Campbell''s monkeys (Cercopithecus campbelli), which give one call type (‘Krak’) to leopards, while the suffixed version of the same call stem (‘Krak-oo’) is given to unspecific danger. To test whether recipients attend to this suffixation pattern, we carried out a playback experiment in which we broadcast naturally and artificially modified suffixed and unsuffixed ‘Krak’ calls of male Campbell''s monkeys to 42 wild groups of Diana monkeys (Cercopithecus diana diana). The two species form mixed-species groups and respond to each other''s vocalizations. We analysed the vocal response of male and female Diana monkeys and overall found significantly stronger vocal responses to unsuffixed (leopard) than suffixed (unspecific danger) calls. Although the acoustic structure of the ‘Krak’ stem of the calls has some additional effects, subject responses were mainly determined by the presence or the absence of the suffix. This study indicates that suffixation is an evolved function in primate communication in contexts where adaptive responses are particularly important.     

Behavioural responses to photographs by pictorially naïve baboons (Papio anubis), gorillas (Gorilla gorilla) and chimpanzees (Pan troglodytes)

This study assessed how pictorially naïve nonhuman primates understand pictures. Fifty-five baboons with no prior exposure to pictures were trained to grasp a slice of banana presented against a pebble in a two alternative forced choice task. Post-training testing involved three stimulus pairs: (1) real banana slice vs. its picture, (2) the banana picture vs. a real pebble and (3) banana picture vs. a pebble picture which were presented twice. Preliminary data were also collected on naïve gorillas (n = 4) and chimpanzees (n = 7) using the same procedure. Baboons revealed a preference for the food picture in (2) and (3) and often ate this stimulus, but the food item and its picture were accurately discriminated in (1). These results suggest that baboons mistook the pictorial stimulus and its referent, but processed the banana pictures as poor exemplars of the real banana category. Among apes, only gorillas ate the banana pictures, suggesting that picture–object confusion may also occur in this species. Findings are discussed as pertaining to the general issue of representational abilities in nonhuman primates, and its evolution.     

MM-MDS: A Multidimensional Scaling Database with Similarity Ratings for 240 Object Categories from the Massive Memory Picture Database

Cognitive theories in visual attention and perception, categorization, and memory often critically rely on concepts of similarity among objects, and empirically require measures of “sameness” among their stimuli. For instance, a researcher may require similarity estimates among multiple exemplars of a target category in visual search, or targets and lures in recognition memory. Quantifying similarity, however, is challenging when everyday items are the desired stimulus set, particularly when researchers require several different pictures from the same category. In this article, we document a new multidimensional scaling database with similarity ratings for 240 categories, each containing color photographs of 16–17 exemplar objects. We collected similarity ratings using the spatial arrangement method. Reports include: the multidimensional scaling solutions for each category, up to five dimensions, stress and fit measures, coordinate locations for each stimulus, and two new classifications. For each picture, we categorized the item''s prototypicality, indexed by its proximity to other items in the space. We also classified pairs of images along a continuum of similarity, by assessing the overall arrangement of each MDS space. These similarity ratings will be useful to any researcher that wishes to control the similarity of experimental stimuli according to an objective quantification of “sameness.”     

Hepatitis viruses in non-human primates

BACKGROUND: Previous epidemiological studies of rural human populations in Gabon reveal a high prevalence of human hepatitis A, B, C and D viruses. In order to investigate the prevalence of the blood-born hepatitis viruses in apes and monkeys living in the same area, we performed an epidemiological survey of HBV, HCV and HDV in wild-born non-human primates. METHODS: We tested 441 wild-born non-human primates from Gabon and Congo and 132 imported monkeys for the presence of serological markers of HBV, HCV and HDV infections. RESULTS: None of Cercopithecidae monkeys were reactive against HBV/HDV and HCV. In contrast, 29.2% of wild-born great apes (154 chimpanzees and 14 gorillas) were positive for HBV serological markers. Nine chimpanzees were in the replicative phase of HBV infection. None of these HBV infected chimpanzees exhibited symptoms or significant changes in serum clinical chemistry related to HBV infection. CONCLUSIONS: The negativity to HCV-related viruses and the negativity of the Cercopithecidae species tested against HBV/HDV do not allow us to definitively rule out the presence of an animal counterpart of human hepatitis viruses in non-human primates.