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.     

Development of visual preference for closely related species by infant and juvenile macaques with restricted social experience

Japanese and rhesus monkeys aged between 9 months old and 5 yrs old pressed a lever to see a variety of pictures of seven macaque species. These monkeys had various restricted social experience: namely, either reared by humans with conspecific or heterospecific peers, or cross-fostered between these two species. Rhesus monkeys tended to prefer seeing rhesus monkeys best among the pictures of the seven species without regard to their age or social experience. Japanese monkeys having restricted experience also liked to see rhesus monkeys better than Japanese monkeys, but not the best among the seven species. In a previous study, mother-reared infants of Japanese monkeys preferred seeing pictures of their own species over those of rhesus monkeys. These results suggest a dissociation of the determinants of this basic social preference: rhesus monkeys prefer to see their own species by nature while Japanese monkeys may learn to prefer their own species.     

Prefrontal cortex activity related to abstract response strategies

Many monkeys adopt abstract response strategies as they learn to map visual symbols to responses by trial and error. According to the repeat-stay strategy, if a symbol repeats from a previous, successful trial, the monkeys should stay with their most recent response choice. According to the change-shift strategy, if the symbol changes, the monkeys should shift to a different choice. We recorded the activity of prefrontal cortex neurons while monkeys chose responses according to these two strategies. Many neurons had activity selective for the strategy used. In a subsequent block of trials, the monkeys learned fixed stimulus-response mappings with the same stimuli. Some neurons had activity selective for choosing responses based on fixed mappings, others for choosing based on abstract strategies. These findings indicate that the prefrontal cortex contributes to the implementation of the abstract response strategies that monkeys use during trial-and-error learning.     

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.     

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.     

Tests of planning and the Bischof-Köhler hypothesis in rhesus monkeys (Macaca mulatta)

The Bischof-Köhler hypothesis posits that nonhuman animals cannot plan for future motivational states that differ from a current state. [Naqshbandi, M., Roberts, W.A., 2006. Anticipation of future events in squirrel monkeys Samiri scireus and rats Rattus norvegicus: tests of the Bischof-Köhler hypothesis. J. Comp. Psychol. 120, 345–357] found that two squirrel monkeys that were not thirsty at the time of choice reversed their preference for a larger amount of food when choice of a smaller amount alleviated future thirst. This apparent anticipation of future thirst contradicts the Bischof-Köhler hypothesis. We used the methods described by Naqshbandi and Roberts with rhesus monkey subjects and found that the monkeys did not alter their behavior in anticipation of future thirst. To assess which factors enhance and inhibit the ability to express planning, we then systematically modified the experimental design in four subsequent experiments and found that monkeys that were not thirsty acted to alleviate future thirst only when the delay between their behavior and the contingent outcome was brief. Taken together these results suggest that the inability of rhesus monkeys to display planning resulted from their inability to learn behavior-outcome associations across long-delay intervals as would be expected from traditional accounts of operant learning, rather than from failure to anticipate future motivational states as posited by the Bischof-Köhler hypothesis.     

Creating abstract topographic representations: Implications for coding,learning and reasoning

Topographic maps are a fundamental and ubiquitous feature of the sensory and motor regions of the brain. There is less evidence for the existence of conventional topographic maps in associational areas of the brain such as the prefrontal cortex and parietal cortex. The existence of topographically arranged anatomical projections is far more widespread and occurs in associational regions of the brain as well as sensory and motor regions: this points to a more widespread existence of topographically organised maps within associational cortex than currently recognised. Indeed, there is increasing evidence that abstract topographic representations may also occur in these regions. For example, a topographic mnemonic map of visual space has been described in the dorsolateral prefrontal cortex and topographically arranged visuospatial attentional signals have been described in parietal association cortex. This article explores how abstract representations might be extracted from sensory topographic representations and subsequently code abstract information. Finally a simple model is presented that shows how abstract topographic representations could be integrated with other information within the brain to solve problems or form abstract associations. The model uses correlative firing to detect associations between different types of stimuli. It is flexible because it can produce correlations between information represented in a topographic or non-topographic coordinate system. It is proposed that a similar process could be used in high-level cognitive operations such as learning and reasoning.     

Relative numerical middle in rhesus monkeys

Animals show vast numerical competence in tasks that require both ordinal and cardinal numerical representations, but few studies have addressed whether animals can identify the numerical middle in a sequence. Two rhesus monkeys (Macaca mulatta) learned to select the middle dot in a horizontal sequence of three dots on a touchscreen. When subsequently presented with longer sequences composed of 5, 7 or 9 items, monkeys transferred the middle rule. Accuracy decreased as the length of the sequence increased. In a second test, we presented monkeys with asymmetrical sequences composed of nine items, where the numerical and spatial middle were distinct and both monkeys selected the numerical middle over the spatial middle. Our results demonstrate that rhesus macaques can extract an abstract numerical rule to bisect a discrete set of items.     

The gag-specific cytotoxic T lymphocytes in rhesus monkeys infected with the simian immunodeficiency virus of macaques

The simian immunodeficiency virus of macaques (SIVmac) is a lentivirus which induces an AIDS-like disease in rhesus monkeys. We have explored the virus-specific cellular immune response in SIVmac-infected rhesus monkeys. Con A-activated, IL-2 expanded PBL of some SIVmac-infected rhesus monkeys lyse autologous B lymphoblastoid cell lines infected with a recombinant vaccinia virus that carries the SIVmac gag gene. This lysis is mediated by CD8+ lymphocytes and is MHC class I restricted. Moreover, these effector lymphocytes do not express the NK cell-associated molecules NKH1 or CD16. These cells are, therefore, CTL. In a limited prospective study of SIVmac-infected rhesus monkeys, the presence of the SIVmac gag-specific CTL activity in PBL correlated with both a reduced efficiency in isolating SIVmac from PBL of these monkeys and their extended survival. This method for assessing SIVmac gag-specific cellular immunity in rhesus monkeys will be important not only in investigating the immunopathogenesis of SIVmac-induced disease, but also in evaluating the capacity of candidate AIDS vaccines to elicit a cell-mediated immune response in this animal model.     

Vicarious learning from human models in monkeys

We examined whether monkeys can learn by observing a human model, through vicarious learning. Two monkeys observed a human model demonstrating an object-reward association and consuming food found underneath an object. The monkeys observed human models as they solved more than 30 learning problems. For each problem, the human models made a choice between two objects, one of which concealed a piece of apple. In the test phase afterwards, the monkeys made a choice of their own. Learning was apparent from the first trial of the test phase, confirming the ability of monkeys to learn by vicarious observation of human models.     

Natural and experimental simian cytomegalovirus infections at a primate center

Simian cytomegalovirus infections were studied in captive, naturally infected primates and in experimentally infected rhesus monkeys. Neutralizing antibody to simian cytomegalovirus was prevalent in selected species of Old World Monkeys. Naturally infected, rhesus monkeys shed virus in their urine during the entire two-year period of study. Similarly, experimentally infected rhesus monkeys showed neutralizing antibody and viruria for more than two years. The indirect fluorescent antibody procedure was found more sensitive than the neutralization antibody technique but appeared less specific for antibody to cytomegalovirus strains.     

Easy Rider: Monkeys Learn to Drive a Wheelchair to Navigate through a Complex Maze

The neurological bases of spatial navigation are mainly investigated in rodents and seldom in primates. The few studies led on spatial navigation in both human and non-human primates are performed in virtual, not in real environments. This is mostly because of methodological difficulties inherent in conducting research on freely-moving monkeys in real world environments. There is some incertitude, however, regarding the extrapolation of rodent spatial navigation strategies to primates. Here we present an entirely new platform for investigating real spatial navigation in rhesus monkeys. We showed that monkeys can learn a pathway by using different strategies. In these experiments three monkeys learned to drive the wheelchair and to follow a specified route through a real maze. After learning the route, probe tests revealed that animals successively use three distinct navigation strategies based on i) the place of the reward, ii) the direction taken to obtain reward or iii) a cue indicating reward location. The strategy used depended of the options proposed and the duration of learning. This study reveals that monkeys, like rodents and humans, switch between different spatial navigation strategies with extended practice, implying well-conserved brain learning systems across different species. This new task with freely driving monkeys provides a good support for the electrophysiological and pharmacological investigation of spatial navigation in the real world by making possible electrophysiological and pharmacological investigations.     

Intestinal microbial patterns of the common marmoset and rhesus macaque

The intestinal microflora of common marmosets and rhesus monkeys were compared by enumerating bacteria from the small and large intestines. Rhesus monkeys had a consistent microflora pattern manifest by higher concentrations of total and Gram-negative aerobic and facultatively anaerobic bacteria, as well as aerobic and anaerobic Lactobacilli, in the large intestine as compared to the small intestine. In contrast, the marmoset microflora were considerably more variable. Approximately two-thirds of the marmosets (designated group A) had an overall profile that resembled the rhesus monkeys, but they had significantly higher concentrations of Gram-negative microflora in their large intestines than the rhesus monkeys. The remaining marmosets (group B) had higher concentrations of bacteria in the small intestine as compared to the large intestine, with the large intestinal concentrations being significantly lower than in the rhesus monkeys and group A marmosets. Moreover, the marmosets did not have detectable levels of aerobic Lactobacilli, and anaerobic Lactobacilli concentrations were significantly lower than in the rhesus macaques. Although it is unknown why microflora differ across species, it is likely that evolutionary adaptations in anatomy and functioning of the gastrointestinal tract influence the concentration and types of bacteria residing as the normal intestinal microflora.     

Rhesus monkey (Macaca mulatta) complex learning skills reassessed

Results from three experiments on basic learning and transfer in rhesus monkeys (Macaca mulatta) are reported in which fully automated testing paradigms, afforded by the Language Research Center's Computerized Test System (LRC-CTS), were employed. Performance levels for discrimination learning set, transfer index, and mediational-learning testing were uniformly higher than was predicted from the literature, in contrast to previous reports of compromised learning under similar conditions (automated apparatus, planimetric stimuli, spatial discontiguity between stimuli and response loci). Analyses reveal relatively advanced learning set performance, transfer-index ratios, and positive transfer of learning even at stringent criterion levels. Moreover, the data suggest that rhesus monkeys tested in these experiments exhibit mediational instead of associative learning strategies, as do great apes and in contrast to previous reports of rhesus learning. We argue that the LRC-CTS enhances learning by nonhuman primate subjects, obviating those factors, reported in the literature from experiments in which manual or other automated systems were employed, that compromise learning.     

Differences between neural activity in prefrontal cortex and striatum during learning of novel abstract categories

Learning to classify diverse experiences into meaningful groups, like categories, is fundamental to normal cognition. To understand its neural basis, we simultaneously recorded from multiple electrodes in lateral prefrontal cortex and dorsal striatum, two interconnected brain structures critical for learning. Each day, monkeys learned to associate novel abstract, dot-based categories with a right versus left saccade. Early on, when they could acquire specific stimulus-response associations, striatum activity was an earlier predictor of the corresponding saccade. However, as the number of exemplars increased and monkeys had to learn to classify them, PFC activity began to predict the saccade associated with each category before the striatum. While monkeys were categorizing novel exemplars at a high rate, PFC activity was a strong predictor of their corresponding saccade early in the trial before the striatal neurons. These results suggest that striatum plays a greater role in stimulus-response association and PFC in abstraction of categories.     

The influence of day-night cycles and the additive effects of methamphetamine and illumination on the spontaneous activity in rhesus monkeys (Macaca mulatta)

The spontaneous activity of rhesus monkeys in a cage situation was measured under 12 hr. day-night cycles in Exp. I. Without exception, all the subjects (n=10) proved to be more active in the daytime than at night. In Exp. II the effect of methamphetamine upon spontaneous activity was investigated in light and dark conditions. It is supposed in the present study that methamphetamine and illumination raise the arousal level of the subjects and increase their spontaneous activity. The results show that the spontaneous activity of rhesus monkeys, which are thought to be visually dominant, greatly depends on illumination. That is, rhesus monkeys move around well in light conditions but little in dark conditions. Methamphetamine increases spontaneous activity, however, in dark as well as in light conditions. Interaction between methamphetamine and illumination effects was not significant. It would appear from these results that both internal and external factors—methamphetamine and illumination—feed into a common pool of the arousal level which controls spontaneous activity.     

Suppression of simian immunodeficiency virus replication in vitro by CD8+ lymphocytes

The AIDS-like disease in rhesus monkeys induced by the simian immunodeficiency virus (SIV) has been used as a model to explore the nature of the T lymphocyte response after infection with viruses of the human immunodeficiency virus family. Activated CD8+ lymphocytes are present in increased numbers in the paracortex of lymph nodes of SIV-infected rhesus monkeys with a lymphadenopathy syndrome. We demonstrate that SIV is more readily isolated from CD8+ lymphocyte-depleted PBL of SIV-infected animals than from their unfractionated PBL. Rather than reflecting the fact that the CD8+ lymphocyte-depleted cell populations are simply enriched for CD4+ lymphocytes, this indicates that CD8+ cells themselves are critical in this regulatory interaction. In fact, CD8+ lymphocytes from SIV-infected but not uninfected rhesus monkeys can block SIV replication in vitro in PBL populations. A T lymphocyte population that blocks replication of viruses of the HIV family may contribute to containing the progression of AIDS.     

Reproductive biology of rhesus and Japanese macaques

This paper offers a comparison of the reproductive biology of the Japanese macaques of Arashiyama, Japan and the free-ranging rhesus macaques of Silver Springs, Florida, U.S.A. The data indicate that rhesus macaques of Silver Springs have a higher reproductive rate than the Japanese macaques of Arashiyama. The reproducive rate of the rhesus monkeys over three birth seasons is 82% and that for the Japanese macaque is 53%. The higher reproductive rate of rhesus monkeys is accomplished through an earlier onset of sexual maturation (4 and 5 years for the rhesus and 5 and 6 years for the Japanese monkeys) and a shorter interbirth interval (14.27±5.54 months for rhesus and 18.00±6.57 months for Japanese monkeys). It is suggested that, because of the relatively harsh winters experienced by Japanese macaques, the slower reproductive rate of the Japanese monkeys has been selected for in order to enable females to lengthen the time in which maternal care is extended to their offspring.     

Complex behavior forms in the lower monkeys in the process of identification of quantitative signs of visual stimuli

Complex behavior forms and the ability of monkeys to recognize and to compare by identity the two-dimensional images and three-dimensional objects of various colors in the amount from 5 to 9 were studied. The study was carried out on two species of the lower monkeys of different levels of phylogenetic development: on rhesus monkeys (Macaca mulatta) and on brown capuchins (Cebus apella). It has been established that the representatives of the studied monkey species are able to differentiate large counted multitudes of two-dimensional (images of squares) and three-dimensional (objects of round shape) stimuli of red, yellow, and green colors in different quantitative ratios—from 5 to 9 at solving modifications of task of the type “choice by the sample.” In the course of learning, species-related differences of the monkeys’ behavior are revealed. The brown capuchins managed solving all tasks and their combinations better than rhesus monkeys. The obtained data indicate the capability for recognition of counted multitudes (from 5 to 9) regardless of color of the stimuli and the existence of quantitative notions of the idea of “quantity” in the lower monkeys.