Female mini-pig performance of temporal response differentiation, incremental repeated acquisition, and progressive ratio operant tasks

Increased knowledge of the cognitive abilities of mini-pigs is needed due to their increasing use in behavioral neuroscience research. Here, six female Yucatan mini-pigs performed tasks thought to measure timing behavior (temporal response differentiation, TRD), learning (incremental repeated acquisition, IRA), and motivation (progressive ratio, PR). Daily 30-min sessions for food reinforcers required a lever press be maintained for at least 10 but no longer than 14s (TRD), learning a new sequence of lever presses each test day (IRA) or an escalating number of presses for subsequent reinforcers (PR). All animals performed PR two days/week while three performed TRD five days/week and the other three performed IRA five days/week. Over the four test weeks, no animal completed TRD training and only one appeared to progress. For this task, lever press maintenance appeared difficult since by choice, the pigs used a front hoof, rather than the snout, to press the lever. IRA subjects showed gradually increasing performance with response rates comparable to those of rats but below those of children and monkeys and accuracy below that for rats. PR response rates were higher than those typically reported for rats, but lower than for adult rhesus monkeys or children. Physical differences in the way that each species responds likely account for these differences.     

Number-Based Visual Generalisation in the Honeybee

Although the numerical abilities of many vertebrate species have been investigated in the scientific literature, there are few convincing accounts of invertebrate numerical competence. Honeybees, Apis mellifera, by virtue of their other impressive cognitive feats, are a prime candidate for investigations of this nature. We therefore used the well-established delayed match-to-sample paradigm, to test the limits of honeybees'' ability to match two visual patterns solely on the basis of the shared number of elements in the two patterns. Using a y-maze, we found that bees can not only differentiate between patterns containing two and three elements, but can also use this prior knowledge to differentiate three from four, without any additional training. However, bees trained on the two versus three task could not distinguish between higher numbers, such as four versus five, four versus six, or five versus six. Control experiments confirmed that the bees were not using cues such as the colour of the exact configuration of the visual elements, the combined area or edge length of the elements, or illusory contours formed by the elements. To our knowledge, this is the first report of number-based visual generalisation by an invertebrate.     

Video-task acquisition in rhesus monkeys (Macaca mulatta) and chimpanzees (Pan troglodytes): A comparative analysis

This study describes video-task acquisition in two nonhuman primate species. The subjects were seven rhesus monkeys (Macaca mulatta) and seven chimpanzees (Pan troglodytes). All subjects were trained to manipulate a joystick which controlled a cursor displayed on a computer monitor. Two criterion levels were used: one based on conceptual knowledge of the task and one based on motor performance. Chimpanzees and rhesus monkeys attained criterion in a comparable number of trials using a conceptually based criterion. However, using a criterion based on motor performance, chimpanzees reached criterion significantly faster than rhesus monkeys. Analysis of error patterns and latency indicated that the rhesus monkeys had a larger asymmetry in response bias and were significantly slower in responding than the chimpanzees. The results are discussed in terms of the relation between object manipulation skills and video-task acquisition.     

Effect of chronic oral methadone treatment on the growth of maturing monkeys.

Three male rhesus monkeys drank methadone hydrochloride (1.0-2.5 mg/kg/day) in Tang orange drink from age two to four years. Their rate of body weight gain was faster than that found by other experimenters. In a second study one male monkey drank 2.0 mg/kg/day methadone while two others drank only Tang from age 21/2 to 31/2 years. The rate of body weight gain was identical for the three monkeys, and was the same as that found in the previous study. The apparent augmentation of body weight gain in the first study was probably due to inter-laboratory differences in housing and feeding conditions.     

<Emphasis Type="Italic">Cebus apella</Emphasis> Tolerate Intermittent Unreliability in Human Experimenters

Monkeys form expectations for outcomes based on interactions with human experimenters. Capuchins, a cooperative New World monkey species, not only anticipate receiving rewards that the experimenter indicates, but also apparently anticipate rewards based on what the experimenter has given to their partners. However, this could be due to subjects responding to either outcomes or experimenters. Here we examine whether capuchins will continue to interact with human experimenters who are occasionally unreliable. We tested 10 monkeys with a series of familiar human experimenters using an exchange task. The experimenters had never before participated in exchange studies with these monkeys, hence the monkeys learned about their behavior during the course of testing. Occasionally experimenters were unreliable, failing to give a reward after the monkey returned the token. The monkeys did recognize these interactions as different, responding much more quickly in trials following those that were nonrewarded than in other situations with the same experimenter. However, subjects did not change their preference for experimenters when given the opportunity to choose between the unreliable exchanger and another exchanger, nor did subjects learn to prefer reliable experimenters from watching other monkeys’ interactions. Instead, subjects returned the tokens to the same location from which they received it. These results indicate that capuchins may not be sensitive to isolated instances in which experimenters are unreliable, possibly because of a strong bias to returning the token to the location from which it was donated.     

Molecular clones of SIVsm and SIVagm: experimental infection of macaques and African green monkeys

We have investigated the ability of biologically-active proviral molecular clones of SIVsm and SIVagm to infect rhesus macaques, pig-tail macaques, and African green monkeys. Two clones of SIVsm were individually inoculated into four rhesus and four pig-tail macaques. All eight macaques became infected, and two have experienced a significant decline in absolute numbers of circulating CD4+ cells. None of three African green monkeys were infected by an SIVsm molecular clone. However, one of four African green monkeys did become infected by SIVsm after receiving lymphocytes directly from an SIVsm-infected rhesus macaque. A molecular clone of SIVagm infected three of four macaques and three of three African green monkeys. None of the three infected macaques had a significant decline in circulating CD4+ cells. Interestingly, infection of pig-tail macaques (but not rhesus macaques) with uncloned SIVagm induced a significant drop in circulating CD4+ cells. These data suggest that molecular clones of SIVsm and SIVagm can be used in experimental models of AIDS for the evaluation of viral gene functions and for the study of in vivo genetic variation.     

Positive Reinforcement Training in Squirrel Monkeys Using Clicker Training

Nonhuman primates in research environments experience regular stressors that have the potential to alter physiology and brain function, which in turn can confound some types of research studies. Operant conditioning techniques such as positive reinforcement training (PRT), which teaches animals to voluntarily perform desired behaviors, can be applied to improve behavior and reactivity. PRT has been used to train rhesus macaques, marmosets, and several other nonhuman primate species. To our knowledge, the method has yet to be used to train squirrel monkeys to perform complex tasks. Accordingly, we sought to establish whether PRT, utilizing a hand‐box clicker (which emits a click sound that acts as the conditioned reinforcer), could be used to train adult male squirrel monkeys (Saimiri boliviensis, N = 14). We developed and implemented a training regimen to elicit voluntary participation in routine husbandry, animal transport, and injection procedures. Our secondary goal was to quantify the training time needed to achieve positive results. Squirrel monkeys readily learned the connection between the conditioned reinforcer (the clicker) and the positive reinforcer (food). They rapidly developed proficiency on four tasks of increasing difficulty: target touching, hand sitting, restraint training, and injection training. All subjects mastered target touching behavior within 2 weeks. Ten of 14 subjects (71%) mastered all tasks in 59.2 ± 2.6 days (range: 50–70 days). In trained subjects, it now takes about 1.25 min per monkey to weigh and administer an intramuscular injection, one‐third of the time it took before training. From these data, we conclude that clicker box PRT can be successfully learned by a majority of squirrel monkeys within 2 months and that trained subjects can be managed more efficiently. These findings warrant future studies to determine whether PRT may be useful in reducing stress‐induced experimental confounds in studies involving squirrel monkeys. Am. J. Primatol. 74:712–720, 2012. © 2012 Wiley Periodicals, Inc.     

Perception of novel changes in a familiar environment by socially‐housed rhesus monkeys

Many animals appear to have a sophisticated spatial representation of their environment. The development of these representations depends on the joint abilities of discriminating novel objects and remembering their locations. Variations of a detection of novelty paradigm were used to determine the nature and limitations of these abilities in rhesus monkeys. Socially‐housed monkeys at two facilities (UMASS Primate Laboratory and the New England Regional Primate Research Center) were exposed to novelty detection tasks using a vertical object grid arranged on a mesh wall of the animals' pens. Monkeys rapidly responded with increased exploration to the replacement of one familiar object with a novel object, to the movement of a familiar object to a novel location, and to the swapping of two familiar objects. However, novelty of object was more salient than novelty of place. In these initial studies, monkeys were given continuous access to the grid, and only one or two changes occurred on a given day. In subsequent studies, the task difficulty was varied either by reducing the length of grid exposure or increasing the number of changed objects/session. Surprisingly, only a reduction in length of exposure markedly affected novelty detecting abilities. Rhesus monkeys clearly possessed the dual novelty detecting abilities. These skills were negatively affected only when monkeys' access to the grid was limited. The procedure employed here provided a convenient way to assess complex cognitive abilities in a group setting. It also relied on rhesus monkeys' inherent attraction to novelty and required only their species‐typical behavior for assessment. Am. J. Primatol. 47:117–131, 1999. © 1999 Wiley‐Liss, Inc.     

Can Monkeys Make Investments Based on Maximized Pay-off?

Animals can maximize benefits but it is not known if they adjust their investment according to expected pay-offs. We investigated whether monkeys can use different investment strategies in an exchange task. We tested eight capuchin monkeys (Cebus apella) and thirteen macaques (Macaca fascicularis, Macaca tonkeana) in an experiment where they could adapt their investment to the food amounts proposed by two different experimenters. One, the doubling partner, returned a reward that was twice the amount given by the subject, whereas the other, the fixed partner, always returned a constant amount regardless of the amount given. To maximize pay-offs, subjects should invest a maximal amount with the first partner and a minimal amount with the second. When tested with the fixed partner only, one third of monkeys learned to remove a maximal amount of food for immediate consumption before investing a minimal one. With both partners, most subjects failed to maximize pay-offs by using different decision rules with each partner' quality. A single Tonkean macaque succeeded in investing a maximal amount to one experimenter and a minimal amount to the other. The fact that only one of over 21 subjects learned to maximize benefits in adapting investment according to experimenters' quality indicates that such a task is difficult for monkeys, albeit not impossible.     

Motor skill impairment in SIV-infected rhesus macaques with rapidly and slowly progressing disease.

A number of studies have shown that simian immunodeficiency virus (SIV) infection in rhesus macaques parallels many aspects of HIV disease in humans. The purpose of this study was to further characterize the rhesus macaque infected with neurovirulent SIV as a model of neuroAIDS. Using a motor skill task, our objective was to detect SIV-related movement impairments in behaviorally trained macaques. The motor skill task required retrieval of a food pellet from a cup in a rotating turntable across a range of speeds. Nine monkeys were infected with neurovirulent strains of SIVmac (R71/17E): four monkeys served initially as controls pre-inoculation. Seven monkeys developed simian AIDS within 4 months of inoculation (rapid progressors), and two survived more than 18 months post-inoculation (slow progressors). Of the rapid progressors, five exhibited significant deficits in this task, most showing a gradual decline in performance terminating in a sharp drop to severely impaired levels of performance. One slow progressor (AQ15) showed no performance declines. The other slow progressor (AQ94) showed a significant decrease in maximum speed that was concurrent with the onset of clinical signs. For AQ94, the role of sickness behavior related to late stage simian AIDS could not be ruled out. These results demonstrate that motor system impairment can be detected early in the course of SIV infection in rhesus macaques, further establishing the SIVmac-infected macaque monkey as a viable model of neuroAIDS.     

The Notions of Size and Shape in Old World Monkeys (<Emphasis Type="Italic">Macaca mullata</Emphasis>): A Comparative Analysis of the Formation Process

In everyday life, humans and animals occupying different rungs of the “evolutionary ladder” often have to evaluate the notions of larger/smaller size (predator/prey, rival/ally, etc.) and flat/volumetric shape (fruit/leaf, 2D/3D images, etc.). The aim of this study was to find out experimentally which of the following two tasks related to the formation of the preverbal notions of larger/smaller size or flat/volumetric shape is easier to train rhesus monkeys. The first task was to form or actualize the notion of larger or smaller size upon co-presentation of 4 flat or volumetric figures. The second task was to form or actualize the notion of flat or volumetric object among 4 figures of the same size (small, medium or large) presented simultaneously. To be rewarded during the formation of both notions, the animal was supposed to choose a figure which was different from the other three in the trial. In both tasks, the number of trials required to reach or exceed the 70% level of correct task implementation per each type of training was counted. This allowed optimization of the notion formation algorithm to rule out strong skill consolidation (overtraining) that might inhibit the formation of a new skill in further training. When the number of trials was averaged over all types of training, the notion of shape formed faster than the notion of size. This discrepancy was only observed under the difficulty of solving one of the task types–discriminating between objects poorly distinguishable (1.5 times) by their size. However, in the situation of no difficulty in discriminating between figures during their perception (more than a 2-fold difference in size), the number of trials in forming the notions of size and shape was statistically indistinguishable. Since training rates in forming the notions of larger/smaller size or flat/volumetric shape were indistinguishable in simple choice situations, we suggest that these notions are equally important for rhesus monkeys.     

Five months of daily standardized exercise for sedentary monkeys

A system to physically exercise rhesus monkeys is described, based on their natural capacity to climb. It is composed of an enclosure where a motor-driven rope is continually going down. The two stage training to this task is easily performed. The total work of each run, evaluated with the weight of the animal and the distance climbed, may be very stable. It was used to provide five sedentary monkeys with daily physical training for five months.     

RT-SHIV感染中国恒河猴及体内传代

目的了解RT-SHIV感染中国恒河猴的感染特点,研究RT-SHIV在中国恒河猴中传代特点;建立RT-SHIV中国恒河猴动物模型,为评价HIV-1药物有效性提供动物平台。方法选择4只健康恒河猴,其中两只动物经上肢静脉感染RT-SHIV病毒,感染急性期采取外周血分离CD8-PBMC,扩增病毒,将新制备的病毒静脉感染另外两只中国恒河猴,通过监测血浆病毒载量,CD4＋/CD8＋比值,CD4＋T淋巴细胞和B淋巴细胞的绝对数,了解实验猴的感染状态,同时分析病毒RT基因变异情况。结果 4只动物均获得系统性感染,且传代动物急性期表现更为强烈,RT基因在感染和传代的过程中共观察到3个氨基酸的改变。结论本研究为RT-SHIV中国恒河猴模型的建立提供了基础信息。     

Impact of path parameters on maze solution time

In order to compare spatial attention and visual processing capabilities of humans and rhesus macaques, we developed a visual maze task both could perform. Maze stimuli were constructed of orthogonal line segments displayed on a monitor. Each was octagonal in outline and contained a central square (the 'start box'). A single ('main') path, containing a random number of turns, extended outward from the start box, and either reached an exit in the maze's perimeter, or a blind ending within the maze. Subjects maintained ocular fixation within the start box, and indicated their judgment whether the path reached an exit or not by depressing one of two keys (humans) or foot pedals (monkeys). Successful maze solution by human subjects required a minimum viewing time. Replacing the maze with a masking stimulus after a variable interval revealed that the percent correct performance increased systematically with greater viewing time, reaching a plateau of approximately 85% correct if mazes were visible for 500 ms or more. A multiple linear regression analysis determined that the response time of both species depended upon several parameters of the main path, including the number of turns, total length, and exist status. Human and nonhuman primates required comparable time to process each turn in the path, whereas monkeys were faster than humans in processing each unit of path length. The data suggest that a covert analysis of the maze proceeds from the center outward along the main path in the absence of saccadic eye movements, and that both monkeys and humans undertake such an analysis during the solution of visual mazes.     

Synchronization of the menstrual cycle through the use of an oral progestin in the rhesus monkey

This study was undertaken to demonstrate the feasibility of using oral progestins for menstrual cycle synchronization in female rhesus monkeys. After a control cycle, four subjects were treated for 21 consecutive days with 0.044 mg/kg/day of the oral progestin altrenogest. During the subsequent 6-wk period the timing and occurrence of menses and ovulation were observed. During the control cycle, the four subjects ovulated over a 6-d period; following progestin treatment all subjects menstruated within a 4-d range, and three of the four subjects ovulated within 24 h of each other. This should prove to be a sufficient degree of ovulation synchrony to allow for successful embryo transfer between females.     

The relative importance of size of food and interfood distance in eliciting aggression in captive rhesus macaques (Macaca mulatta).

We conducted an experiment on a group of captive rhesus macaques (Macaca mulatta) in which we manipulated both food size and interfood distance independently to examine which factor was more important in causing aggressive competition. For each of 254 trials, the monkeys were offered simultaneously two apple pieces ranging in size from 1 to 40 g at interfood distances ranging from 1 to 5 m. In contrast to other studies, food size and interfood distance were not conflated in this study. Multiple regression analyses revealed that food size was a better predictor of aggression whereas interfood distance was a better predictor of the ability to monopolize foods. Growing evidence suggests that factors such as food size, quality and depletion time are more important than interfood distance in influencing aggression within groups.     

Functional relationships for determining similarities and differences in comparative cognition

Pigeons, capuchin monkeys and rhesus monkeys were trained in nearly identical same/different tasks with an expanding 8-item training set and showed qualitatively similar functional relationships: increasing novel-stimulus transfer (i.e., concept learning) as a function of the training-set size and the level of transfer eventually becoming equivalent to baseline training performance. There were also some quantitative functional differences: pigeon transfer increases were more gradual and baseline-equivalent transfer occurred at a larger set size (256 items) than for monkeys (128 items). Other pigeon groups trained at 32 and 64-item initial set sizes showed improved transfer (relative to expanding the 8-item training set), equivalent to the monkey species’ transfer at these same training set sizes. This finding of equivalent concept learning over a portion of the functional range (8, 32, and 64 items or 64-4096 training pairs) is discussed in terms of species differences: carryover effects from smaller-set training, evolved neural systems, cognitive and cortical modules, and general distributed learning systems for “higher-order” cognitive abilities.     

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.     

Food-exchange with humans in brown capuchin monkeys

To assess how brown capuchin monkeys (Cebus apella) delay gratification and maximize payoff, we carried out four experiments in which six subjects could exchange food pieces with a human experimenter. The pieces differed either in quality or quantity. In qualitative exchanges, all subjects gave a piece of food to receive another of higher value. When the difference of value between the rewards to be returned and those expected was higher, subjects performed better. Only two subjects refrained from nibbling the piece of food before returning it. All subjects performed two or three qualitative exchanges in succession to obtain a given reward. In quantitative exchanges, three subjects returned a food item to obtain a bigger one, but two of them nibbled the item before returning it. Individual differences were marked. Subjects had some difficulties when the food to be returned was similar or equal in quality to that expected.     

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.