Precocious quantitative cognition in monkeys

Basic quantitative abilities are thought to have an innate basis in humans partly because the ability to discriminate quantities emerges early in child development. If humans and nonhuman primates share this developmentally primitive foundation of quantitative reasoning, then this ability should be present early in development across species and should emerge earlier in monkeys than in humans because monkeys mature faster than humans. We report that monkeys spontaneously make accurate quantity choices by 1 year of age in a task that human children begin to perform only at 2.5 to 3 years of age. Additionally, we report that the quantitative sensitivity of infant monkeys is equal to that of the adult animals in their group and that rates of learning do not differ between infant and adult animals. This novel evidence of precocious quantitative reasoning in infant monkeys suggests that human quantitative reasoning shares its early developing foundation with other primates. The data further suggest that early developing components of primate quantitative reasoning are constrained by maturational factors related to genetic development as opposed to learning experience alone.     

Utility of habituation-dishabituation procedure for comparative cognitive studies of Callithrix jacchus and Aotus spp.: preliminary assessments

The utility of the habituation-dishabituation procedure was examined in the common marmosets (Callithrix jacchus) and the owl monkeys (Aotus spp.). The same movies were repeatedly shown to monkeys during an habituation phase, followed by a test phase during which monkeys were presented with a different movie. The time monkeys spent looking at the movie gradually decreased during the habituation phase and then significantly increased when they were presented the new movie. The limited findings indicate that these monkeys were sensitive to the habituation-dishabituation paradigm, suggesting that this procedure might be used to assess cognition and perception.     

Contrast discrimination in human infants

The ability to detect differences in spatial contrast is crucial to object recognition and identification. This ability is generally examined by measuring the contrast discrimination function. This function represents, for a variety of conditions, the smallest contrast difference required to discriminate otherwise identical patterns. We examined human infants' ability to discriminate patterns on the basis of differences in spatial contrast. The forced-choice preferential looking procedure was used to estimate contrast increment thresholds at a number of background contrasts. The Weber fractions of 6- and 12-week-old infants were about 1 log unit higher than adult values for background contrasts ranging from 0.14 to 0.55. Furthermore, the slopes of infants' discrimination functions were much shallower than those of adults. These age differences in contrast discrimination imply certain changes in the neural mechanisms that underlie contrast encoding. They also aid our understanding of the anomalies observed in early pattern vision.     

Automatic testing of cognitive performance in baboons maintained in social groups

Laboratory procedures used to study the cognitive functions of primates traditionally have involved removal of the subjects from their living quarters to be tested singly in a remote experimental room. This article presents an alternative research strategy favoring testing primates while they are maintained in their social group. The automatic learning device for monkeys (ALDM) is a computerized test system controlled by an automatic radio frequency identification of subjects. It is provided ad lib inside the social group of monkeys, for voluntary self-testing on a 24-h schedule. Nine baboons were tested with ALDM during a 7-month period. Experiments were performed to assess learning in motor control and abstract reasoning tasks. The results revealed high trial frequencies and excellent learning performance, even in tasks involving the highest cognitive complexities. A different study using ALDM with a group of 3 rhesus monkeys revealed social influences on learning. Beyond its interest for cognitive psychologists, ALDM is of interest for pharmacologists and cognitive neuroscientists working with nonhuman primates. ALDM also can serve as an enrichment tool for captive animals and may be used to study a variety of species other than primates.     

Matching visual stimuli on the basis of global and local features by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta)

This study was designed to examine whether chimpanzees and monkeys exhibit a global-to-local precedence in the processing of hierarchically organized compound stimuli, as has been reported for humans. Subjects were tested using a sequential matching-to-sample paradigm using stimuli that differed on the basis of their global configuration or local elements, or on both perceptual attributes. Although both species were able to discriminate stimuli on the basis of their global configuration or local elements, the chimpanzees exhibited a global-to-local processing strategy, whereas the rhesus monkeys exhibited a local-to-global processing strategy. The results suggest that perceptual and attentional mechanisms underlying information-processing strategies may account for differences in learning by primates. Accepted after revision: 11 September 2001 Electronic Publication     

Sex categorization of conspecific pictures in Japanese monkeys (Macaca fuscata)

We investigated whether monkeys discriminate the sex of individuals from their pictures. Whole-body pictures of adult and nonadult monkeys were used as stimuli. Two male Japanese monkeys were trained for a two-choice sex categorization task in which each of two choice pictures were assigned to male and female, respectively. Following the training, the monkeys were presented with novel monkey pictures, and whether they had acquired the categorization task was tested. The results suggested that while monkeys discriminate between the pictures of adult males and females, discrimination of nonadult pictures was difficult. Partial presentations of the pictures showed that conspicuous and sexually characteristic parts (i.e., underbellies including male scrotums or breasts including female nipples) played an important role in the sex categorization.     

Operant conditioning permits voluntary,noninvasive measurement of blood pressure in conscious,unrestrained baboons (Papio cynocephalus)

This report describes a computerized apparatus and procedure for completely automated noninvasive measurement of systolic, diastolic, and mean arterial blood pressure in conscious, unrestrained nonhuman primates. We used a specially constructed, cage-mounted oscillometric blood pressure instrument and operant reward conditioning methods to train adult baboons(Papio cynocephalus) to submit voluntarily to frequent self-initiated determinations of their blood pressures in the absence of a human operator/observer. Details concerning the operant training procedure and illustrative blood pressure data are presented. The accuracy of the method was evaluated by comparing the noninvasive blood pressure readings with simultaneously taken direct measurements obtained by means of chronically indwelling arterial catheters.     

Frequency discrimination between and within line gratings by dynamic touch

Line gratings were used to investigate the tactual discrimination thresholds for line frequency. In Experiment 1, participants were asked to discriminate between two gratings, each with a different line frequency. We used four standard frequencies in the eightfold range from 0.5 to 4 lines/cm. Thresholds were found to be constant at about 10.6%. In this experiment, we also measured hand speed and contact force. Hand speed was roughly in the range between 0.12 and 0.44 m/sec; contact force ranged from 0.62 to 2.76 N. In Experiment 2, we determined discrimination thresholds for line frequency transitions within a single grating. We used two frequencies and three transition lengths. The transition length had no effect on the threshold. In a third experiment, line frequency was modulated periodically. Varying the standard frequency and the size of the modulation period was found to have no effect on the discrimination thresholds. We conclude three things. First, Weber fractions for line frequency discrimination decrease as a function of line frequency within the experimental range. Second, discrimination thresholds are not altered by the length of the transition between two adjacent gratings with different line frequencies. And finally, the size of a modulation period in periodically modulated gratings is of no influence on the modulation detection threshold.     

Androgens and aggressive behavior in primates: A review

This review deals with possible central and peripheral effects of androgens upon primate aggressive behavior. One problem that clouds interpretation of experimental work is that measurements of dominance have often been employed, such as competition tests for food and water. Such measures often do not correlate with those obtained by quantifying aggressive interactions. It should be remembered that very few of the 188 primate species have been studied experimentally and that great behavioral and physiological diversity occurs within the order. Therefore, generalizations about the effects of androgens upon aggressive behavior in primates (including man) should be made with caution. Testosterone has an organizing influence upon the foetal brain of rhesus monkeys and may affect the development of neural mechanisms which govern aggression in males. More data are required on primates, however, since rhesus monkeys show some important differences from rodents as regards the effects of androgen upon sexual differentiation of the hypothalamus. In future, marmosets may provide a suitable model for such studies, because there is evidence that sexual differentiation of brain by androgen occurs postnatally in these monkeys. At puberty, male primates show a variety of behavioral changes and, during adulthood, males of seasonally breeding species may be more aggressive during the mating season, when testosterone levels are maximal. This does not indicate a causative relationship between testosterone and aggressive responses, because castration and androgen treatments have little effect upon aggression in prepubertal or adult males of several primate species. Androgens have pronounced effects on sexual responses in adult male monkeys, but their central effects upon aggression are much less important than among rodents. Elec trical stimulation of hypothalamic pathways has been employed to evoke aggressive behavior in marmosets and rhesus monkeys. In the rhesus, preliminary evidence indicates that such pathways show some sensitivity to androgens. In rodents it is known that these areas are richly supplied with monoaminergic neurons, which play an important role in aggressive behavior. There is little evidence on primates, however, and this remains a crucial topic for future research. Peripheral effects of androgens should also be considered. Many prosimians and New World monkeys use scent-marking behaviors and, in males, androgen-dependent chemical cues may be involved in sexual recognition and territorial behavior. This possibility awaits investigation. Finally, plasma testosterone levels may alter as a function of aggression itself; thus levels decrease if male rhesus monkeys are defeated by conspecifics. This might occur because neural events associated with giving (or receiving) aggression also influence pituitary function and hence alter gonadal testosterone secretion. Theoretically, it is possible that such changes in circulating testosterone might affect aggressive behavior via a feedback action on the brain, but the experimental evidence does not support such a view.     

Absolute auditory thresholds in three Old World monkey species (Cercopithecus aethiops, C. neglectus, Macaca fuscata) and humans (Homo sapiens)

We investigated the absolute auditory sensitivities of three monkey species (Cercopithecus aethiops, C. neglectus, and Macaca fuscata) and humans (Homo sapiens). Results indicated that species-typical variation exists in these primates. Vervets, which have the smallest interaural distance of the species that we tested, exhibited the greatest high-frequency sensitivity. This result is consistent with Masterton, Heffner, and Ravizza's (1969) observations that head size and high-frequency acuity are inversely correlated in mammals. Vervets were also the most sensitive in the middle frequency range. Furthermore, we found that de Brazza's monkeys, though they produce a specialized, low-pitched boom call, did not show the enhanced low-frequency sensitivity that Brown and Waser (1984) showed for blue monkeys (C. mitis), a species with a similar sound. This discrepancy may be related to differences in the acoustics of the respective habitats of these animals or in the way their boom calls are used. The acuity of Japanese monkeys was found to closely resemble that of rhesus macaques (M. mulatta) that were tested in previous studies. Finally, humans tested in the same apparatus exhibited normative sensitivities. These subjects responded more readily to low frequencies than did the monkeys but rapidly became less sensitive in the high ranges.     

A comparison of thresholds for 1/3-octave filtered clicks and noise bursts in infants and adults

Behavioral thresholds of 6-month-old infants and adults were determined for 1/3-octave filtered clicks and 300-msec noise bursts with center frequencies ranging from .5 to 8 kHz. For noise bursts, differences between infant and adult thresholds were largest at low frequencies and smallest at 8 kHz. For clicks, infants’ thresholds were most like adults’ at 4 kHz, and age differences increased at both lower and higher frequencies. Differences between click and noise thresholds were significantly larger for infants than for adults at .5, 1, and 8 kHz, but not at 2 and 4 kHz. These results suggest that improvements in threshold for long-duration stimuli during infancy may not be accompanied by comparable changes in threshold at short durations. The delayed development of sensitivity to low- and high-frequency clicks appears consistent with maturational trends recently described for the auditory brainstem response.     

The use of prosodic cues in language discrimination tasks by rats

Recent research with cotton-top tamarin monkeys has revealed language discrimination abilities similar to those found in human infants, demonstrating that these perceptual abilities are not unique to humans but are also present in non-human primates. Specifically, tamarins could discriminate forward but not backward sentences of Dutch from Japanese, using both natural and synthesized utterances. The present study was designed as a conceptual replication of the work on tamarins. Results show that rats trained in a discrimination learning task readily discriminate forward, but not backward sentences of Dutch from Japanese; the results are particularly robust for synthetic utterances, a pattern that shows greater parallels with newborns than with tamarins. Our results extend the claims made in the research with tamarins that the capacity to discriminate languages from different rhythmic classes depends on general perceptual abilities that evolved at least as far back as the rodents. Electronic Publication     

The effect of marker frequency disparity on the discrimination of gap duration in monkeys

Duration-discrimination thresholds of the silent interval (gap) between two successive tones (markers) were measured in four Japanese monkeys. The task was serial discrimination, and monkeys were required to release the lever when the gap duration decreased from 200 ms. Monkeys successfully acquired the task, and gap thresholds of monkeys were revealed to be larger than previous data with human subjects. Gap thresholds were not affected by marker frequency when the two markers were identical in frequency, though the thresholds increased when large frequency differences existed between markers. The effect of marker frequency disparity on gap thresholds in monkeys is discussed in terms of the difficulty in integrating information from discrete frequency channels.     

Discriminative vocal conditioning in rhesus monkeys: Evidence for volitional control?

Both emotional and volitional systems are invoked in explaining the control of human vocalizations, but vocal behavior of nonhuman primates is often believed to be totally under emotional control. Monkeys' poor performance on conditioning tasks, especially discriminative conditioning of vocalization (DCV), has been cited as evidence against volitional control. In Experiment 1, rhesus monkeys failed a DCV task in which food was given for vocalizations emitted during an arbitrary visual stimulus, but in Experiment 2, monkeys showed clear discriminative performance when an otherwise comparable shock-avoidance DCV procedure was used. This evidence that monkeys possess some degree of volitional control has implications for the relation between animal vocalizations and the origin of human speech.     

Developmental changes in infants' sensitivity to octave-band noises

Localization responses to octave-band noises with center frequencies at 200, 400, 1000, 2000, 4000, and 10,000 Hz were obtained from infants 6, 12, and 18 months of age. During an experimental trial, an octave-band noise was presented on one of two speakers located 45° to each side of the infant. A head turn to the noise (correct response) was rewarded by activating an animated toy on top of the speaker. The intensity of the noise was varied over trials (method of constant stimuli) to determine thresholds at each center frequency. Thresholds for the lower frequencies were approximately 5–8 db higher in the 6-month-old infants compared to the older infants. However, there were no consistent differences among groups at the higher frequencies. Infant thresholds were found to be 20–30 db higher than adult thresholds at the lower frequencies. At the higher frequencies thresholds for infants were approaching those of adults.     

Visual discrimination of spectral distributions

Human observers seem to be able to use different features that classify materials with a large degree of accuracy. In this paper, we look at human perception of statistical properties of the spectral distribution in a scene. We investigated whether human observers can discriminate just as accurately between coloured textures that have a spectral distribution due either to shading only or to both shading and specular reflectance as between uniform colours. Thresholds for the discrimination of coloured textures are about 15 times as high as thresholds for the discrimination of uniform colours, provided there is a sharp transition between the two colours. However, the coloured texture thresholds are only 1.5 times higher when we introduce a gradual transition between the two colours. There are also distinct qualitative differences in discrimination thresholds for different base colours. These differences cannot be predicted from discrimination thresholds for uniform colours. Human observers are surprisingly good at discriminating between a material edge and a shadow edge in complex scenes. Statistical differences in the orientation of the colour distributions in colour space might be used to accomplish this. In a second experiment we investigated how well observers can discriminate between two linear distributions in colour space that have the same base colour but different orientations. When we vary the line-length in R, G, B space, thresholds cannot be predicted completely by the conservation of the average distance between the two distributions. This means that observers use not only the maximum colour difference in the stimulus to do the task, but other cues are also involved.     

A cage-based training,cognitive testing and enrichment system optimized for rhesus macaques in neuroscience research

In neurophysiological studies with awake non-human primates (NHP), it is typically necessary to train the animals over a prolonged period of time on a behavioral paradigm before the actual data collection takes place. Rhesus monkeys (Macaca mulatta) are the most widely used primate animal models in system neuroscience. Inspired by existing joystick- or touch-screen-based systems designed for a variety of monkey species, we built and successfully employed a stand-alone cage-based training and testing system for rhesus monkeys (eXperimental Behavioral Intrument, XBI). The XBI is mobile and easy to handle by both experts and non-experts; animals can work with only minimal physical restraints, yet the ergonomic design successfully encourages stereotypical postures with a consistent positioning of the head relative to the screen. The XBI allows computer-controlled training of the monkeys with a large variety of behavioral tasks and reward protocols typically used in systems and cognitive neuroscience research.     

Conserved evolutionary history for quick detection of threatening faces

Humans quickly recognize threats such as snakes and threatening faces, suggesting that human ancestors evolved specialized visual systems to detect biologically relevant threat stimuli. Although non-human primates also detect snakes quickly, it is unclear whether primates share the efficient visual systems to process the threatening faces of their conspecifics. Primates may not necessarily process conspecific threats by facial expressions, because threats from conspecifics in natural situations are often accompanied by other cues such as threatening actions (or attacks) and vocal calls. Here, we show a similar threat superiority effect in both humans and macaque Japanese monkeys. In visual search tasks, monkeys and humans both responded to pictures of a threatening face of an unfamiliar adult male monkey among neutral faces faster than to pictures of a neutral face among threatening faces. However, the monkeys’ response times to detect deviant pictures of a non-face stimulus were not slower when it was shown among threat faces than when it was shown among neutral faces. These results provide the first evidence that monkeys have an attentional bias toward the threatening faces of conspecifics and suggest that threatening faces are evolutionarily relevant fear stimuli. The subcortical visual systems in primates likely process not only snakes, but also more general biological threat-relevant stimuli, including threatening conspecific faces.     

A SIMULTANEOUS DISCRIMINATION PROCEDURE FOR THE MEASUREMENT OF VISION IN NONVERBAL CHILDREN1

Few nonverbal developmentally disabled children ever receive adequate vision assessment because of their limited language skills. The present study details a simultaneous discrimination procedure for measuring subjective visual acuity in such children. A stimulus fading procedure was used to train a discrimination between Snellen Es differing in orientation, and a psychophysical tracking method was used to determine acuity thresholds. The procedure was tested with 11 nonverbal autistic and schizophrenic children and validated with four nonpsychotic children. Eight of the psychotic children were successfully examined in one to three sessions. Two of these children were identified as having significant acuity losses. The validity assessment showed that the experimental procedure resulted in thresholds equal to or slightly lower than those obtained with the Illiterate E chart.     

Formation of the sameness-difference concept by Japanese monkeys from a small number of color stimuli

Japanese monkeys were trained to form the sameness-difference concept. In Experiment 1, four monkeys were trained with two colors to discriminate matching stimulus pairs from nonmatching pairs by reinforcing only lever-pressing responses to matching pairs with a variable-interval schedule. Three monkeys showed successful transfer of this discrimination to two new colors, thus demonstrating that some Japanese monkeys are able to form this relational concept from a minimum number of stimuli. In Experiment 2, two monkeys were trained, in a Yes/No procedure with three colors, to press one lever under matching pairs and another lever under nonmatching pairs. Poor transfer performances to three new colors suggest that simultaneously establishing two different response patterns to matching and nonmatching pairs is ineffective in forming the concept. In Experiment 3, the amount of transfer to three new colors after mastering a standard three-color matching-to-sample task was compared with that of a modified task in which correct responses were reinforced with a within-trial variable-interval schedule. All three monkeys showed greater transfer with the modified procedure. The results suggest that the variable-interval schedule adopted within trials is effective in forming the sameness-difference concept.