Spontaneous alternation behavior in common marmosets (Callithrix jacchus).

Whether common marmosets (Callithrix jacchus) exhibit spontaneous alternation behavior was examined. Marmosets were allowed to explore one of the two arms of a Y-shaped maze, and after delays of various lengths, their preference to enter the previously entered or alternate arms was examined. The marmosets showed spontaneous alternation behavior; they preferred to enter the alternate arm after a delay of 2 hours or shorter, but such a preference was lost after a 24-hr delay. The loss of the alternation with longer delay can be discussed in terms of marmosets' foraging strategies. When the visual cue at the entered arm was changed after the initial exploration, the marmosets did not exhibit spontaneous alternation, suggesting that the visual cue had some role in the alternation behavior. Spontaneous alternation behavior in marmosets will provide an opportunity to simply measure their memory without providing specific task training.

Effects of rearing conditions on early visual development in common marmosets.

Early development of visual behavior was examined in hand-reared (HR) and parentally reared (PR) common marmosets (Callithrix jacchus). On the day of birth, most of the marmosets exhibited sensitivity to light and sound: they closed their eyes in response to light and oriented to the sound sources. The behavior of tracking moving visual stimuli was exhibited at around 10 days postnatally in PR marmosets, but the onset of this behavior was delayed to the age of 16 days in HR marmosets. The delay occurred possibly because of the poor input of optical flow under the HR environment. The onset age of head-cocking was about 2 weeks in both groups of marmosets, and the HR marmosets began head-cocking and visual tracking simultaneously. Both groups of marmosets exhibited sensitivity to optical approach at the age of around 30 days: the age to wean and increase independent locomotion. The results suggested that the onset of motion perception preceded detailed shape and depth perception in marmosets, and the developmental sequence in marmosets was similar to those in humans and macaque monkeys. Marmosets appear to be useful animal models to examine environmental effects on early visual development.

Development of a compact and general-purpose experimental apparatus with a touch-sensitive screen for use in evaluating cognitive functions in common marmosets.

Common marmosets have been used extensively in biomedical research and the recent advent of techniques to generate transgenic marmosets has accelerated the use of this model. New methods that efficiently assess the degree of cognitive function in common marmosets are needed in order to establish their suitability as non-human primate models of higher brain function disorders. Here, we have developed a new apparatus suitable for testing the cognitive functions of common marmosets. Utilizing a mini laptop PC with a touch-sensitive screen as the main component, the apparatus is small and lightweight and can be easily attached to the home cages. The ease of designing and testing new paradigms with the flexible software is another advantage of this system. We have tested visual discrimination and its reversal tasks using this apparatus and confirmed its efficacy.

Development of infant common marmosets' (Callithrix jacchus) preference for their parents over adults from another group.

Parent-offspring attachment is important for animals which have offspring that require parental care for their development. Infant attachment to the mother has been examined in macaques, but it remains poorly understood in common marmosets. Here, we examined the abilities of 14 common marmoset infants to show preference for their parents over adults from another group at the ages of 4, 10, and 15 weeks. Each infant was exposed to its parent and an adult from another group in an I-shaped maze. Although 4-week-old infants did not show a significant difference between approach behaviors toward their parents and other adults, 10- and 15-week-old infants approached and stayed longer near their parents than adults from another group. These results suggest selective approach behavior develops in marmosets by the age of 10 weeks.

Time course of vocal modulation during isolation in common marmosets (Callithrix jacchus).

Common marmosets vocalize phee calls as isolation calls, which seem to facilitate their reunion with family groups. To identify multiple acoustic properties with different time courses, we examined acoustic modulations of phees during different social contexts of isolation. Subject marmosets were totally isolated in one condition, were visually isolated and could exchange vocalizations in another condition, and were visually isolated and subsequently totally isolated in a third condition. We recorded 6,035 phees of 10 male-female marmoset pairs and conducted acoustic analysis. The marmosets frequently vocalized phees that were temporally elongated and louder during isolation, with varying time courses of these changes in acoustic parameters. The vocal rates and sound levels of the phees increased as soon as the marmosets saw their pair mates being taken away, and then gradually calmed down. The phee duration was longer in conditions during which there were no vocal responses from their pair mates. Louder vocalizations are conspicuous and seem to be effective for long-distance transmission, whereas shorter call duration during vocal exchanges might avoid possible vocal overlap between mates.

Sexual dimorphism in facial shapes and their discrimination in Japanese monkeys (Macaca fuscata).

The authors examined the ability of Japanese monkeys (Macaca fuscata) to discriminate between sexes based on facial features. The shape and position of facial features (facial morphology) were measured to quantify the differences between sexes. The distance between the chin and nose was longer in males than females, and the outline of the face around the upper jaw and upper face differed between sexes. Using operant conditioning, 2 monkeys succeeded in discriminating sex based on facial pictures. Furthermore, they successfully generalized the discrimination to novel pictures of faces. Tests with morphed pictures of faces revealed that the monkeys used facial morphology to discriminate between males and females. Our results suggest that Japanese monkeys have sexual dimorphism in facial shape and they can use the morphological differences to discriminate conspecific sex.

The effects of age and sex on interest toward movies of conspecifics in Japanese macaques (Macaca fuscata).

Previous studies have suggested that images of conspecifics are useful for environmental enrichment for nonhuman primates, but whether the age and sex of the animals alter the effectiveness of such images is unclear. We investigated preferences to movies in Japanese macaques (Macaca fuscata; male and female; age, 2 to 19 y). Each monkey was housed individually in a cage outfitted with a touch-sensitive computer display. A subject monkey that touched the display was shown 1 of 30 movies that were recorded at an open enclosure containing their conspecifics. During the experimental sessions, 25 of 38 subjects touched the display at least once. The response duration was longer when monkeys appeared in the movies. The response duration decreased with age in male monkeys but not female monkeys. The results suggested the movies of conspecifics are useful for environmental enrichment, but further consideration seems appropriate for various subpopulations, particularly aged monkeys.

Temporal rules in vocal exchanges of phees and trills in common marmosets (Callithrix jacchus).

Marmosets exchange two types of calls: phees and trills. We played back phees and trills to investigate the temporal rules of vocal exchanges using ten captive common marmosets (Callithrix jacchus). The marmosets usually emitted the same type of vocalizations just after the stimulus playbacks, and similar regularities were observed in the temporal intervals of phees and in trills. They vocalized with shorter intervals when they responded with trills rather than phees, and, after the first call, they repeatedly vocalized trills with shorter intervals than phees. These results suggest that the temporal rules between phees and trills are qualitatively similar but quantitatively different. These results might be owing to the different distances over which these contact calls are used.

Food transfer in common marmosets: parents change their tolerance depending on the age of offspring.

Food transfer is considered to provide infants with additional nutrients during weaning, and in fact, its frequency peaks around this time. However, the mechanisms underlying such food transfer remain unclear. In this study, we investigated whether adult common marmosets (Callithrix jacchus) change their tolerance to offspring begging for food depending on the offspring's age. We used four families consisting of breeding pairs, older offspring (29-49 weeks old), and younger offspring (7-15 weeks old). To directly compare the responses of a parent with its older and younger offspring, we placed one parent and one offspring in a testing space at one time. We presented foods where only the parent could reach them to ensure that the foods were transferred from the parent to offspring. Younger offspring showed more interest in food being held by the parents than older offspring. Parents refused older offspring more frequently than younger offspring and transferred food more often to younger offspring than to older offspring. There was no difference in all behavioral categories between fathers and mothers. These results suggest that both fathers and mothers are more tolerant to weanlings, but their tolerance decreases as offspring mature.

Japanese monkeys (Macaca fuscata) discriminate between pictures of conspecific males and females without specific training.

We investigated whether Japanese monkeys can discriminate pictures of conspecific males and females using a visual paired comparison (VPC) task. Whole-body pictures of adult and nonadult monkeys were used as stimuli. The monkeys were first familiarized with pairs of pictures of different monkeys from one sex category (the familiarized sex). Pairs of novel pictures of a member of the familiarized sex and the opposite sex (novel) were then presented in test. The monkeys showed a preference for novel-sex pictures of both adult and nonadult individuals, indicating that they perceive the differences between familiarized- and novel-sex pictures. These results suggest that monkeys discriminate between pictures of males and females without specific training.

Effect of others' attentional states on vocalizations in Japanese monkeys (Macaca fuscata).

We investigated the effects of other's attentional states on vocalizations in monkeys. The subjects were 14 Japanese monkeys (Macaca fuscata), which vocalized spontaneously in the feeding context. In the initial experiment, an experimenter moved towards and away from the subject monkeys. The monkeys vocalized more frequently when the experimenter moved away rather than towards them. To examine the effects of the experimenter's body orientations and moving directions separately, additional experiments were conducted. When the experimenter stood facing towards and facing away from the subject monkeys, the monkeys vocalized more frequently when the experimenter stood facing away rather than facing towards. When the experimenter moved towards and away from the subject monkeys while facing them, the monkeys vocalized more frequently when the experimenter moved away from them rather than towards them. These results suggested that the monkeys vocalized more frequently when the situation changed to that where the monkeys were not likely get food from the experimenter. It seems that monkeys recognize the attentional states of others by body orientation and modify their vocalizing behavior accordingly.

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.

Individual vocal differences of the coo call in Japanese monkeys.

We investigated individual vocal characteristics of the coo call in Japanese monkeys. The goal of the study was to determine which parameters are individual discriminators (for individuals of different ages and sexes) and to test whether those differences were similar for individuals of same age and sex. A discriminant analysis realized on eight individuals pointed out that three parameters (call duration, start and end frequencies of the fundamental component) differentiated individuals efficiently and was validated by a second discriminant analysis realized on three same-age females.

Matching vocalizations to vocalizing faces in a chimpanzee (Pan troglodytes).

Auditory-visual processing of species-specific vocalizations was investigated in a female chimpanzee named Pan. The basic task was auditory-visual matching-to-sample, where Pan was required to choose the vocalizer from two test movies in response to a chimpanzee's vocalization. In experiment 1, movies of vocalizing and silent faces were paired as the test movies. The results revealed that Pan recognized the status of other chimpanzees whether they vocalized or not. In experiment 2, two different types of vocalizing faces of an identical individual were prepared as the test movies. Pan recognized the correspondence between vocalization types and faces. These results suggested that chimpanzees possess crossmodal representations of their vocalizations, as do humans. Together with the ability of vocal individual recognition, this ability might reflect chimpanzees' profound understanding of the status of other individuals.

Vocal individual discrimination in Japanese monkeys.

The present study determines which features of the coo call are used by Japanese monkeys Macaca fuscata for vocal individual discrimination. First, two female Japanese monkeys were trained to discriminate conspecific individuals vocally, using an operant conditioning. Using as stimuli three unknown individuals with 30 calls per individual, the two monkeys succeeded in discriminating new call exemplars from the three stimulus individuals. A discriminant analysis performed on calls used as stimuli indicated that start frequency of the fundamental and call duration were variables that can differentiate individuals efficiently. Then, playbacks of acoustically modified signals were used to indicate which vocal features are used by monkeys for the individual discrimination. Stimuli signals containing modified pitch or duration, or filtered so as to keep only the fundamental component, were tested. Results indicated that Japanese monkeys use multiple acoustical cues to perform vocal individual discrimination, including at least pitch, call duration, and harmonics. However, harmonics seem to be less important for discrimination than pitch and call duration.

Identification of vocalizers by pant hoots, pant grunts and screams in a chimpanzee.

Identification of vocalizers was examined using an auditory-visual matching-to-sample task with a female chimpanzee. She succeeded in selecting the picture of the vocalizer in response to various types of vocalizations: pant hoots, pant grunts, and screams. When pant hoots by two chimpanzees were presented as a "duet", she could identify both of the vocalizers. These results suggest that researchers have underestimated the capability of vocalizer identification in chimpanzees. The chimpanzee correctly chose her own pictures in response to her vocalizations only by exclusion, and she did not show vocal self-recognition. The effect of acoustical modification (pitch shift and filtration) on the performance suggested that pitch is an important cue for the vocalizer identification.

Effect of temporal separation on tone-sequence discrimination in monkeys.

Perception of auditory spectral-temporal patterns was examined in two Japanese monkeys. The stimuli used were pairs of pure tones of different frequencies that were presented sequentially. The monkeys were required to discriminate whether the frequency of the second tone was higher or lower than the first tone. The performances of the monkeys deteriorated when a temporal gap (i.e., silence) was inserted between the component tones. A comparison experiment did not show such effects in human participants. The results suggested that monkeys use frequency transitions for tone-sequence discrimination, and that local characters are more dominant discrimination cues in monkeys than in humans.

Auditory stream segregation in Japanese monkeys.

Japanese monkeys were examined to determine whether they perceptually segregate tone sequences. Monkeys were required to discriminate two sequences of tones (target sequences) differing in frequency contours. Distractor sequences were presented simultaneously with the target sequences. Monkeys could discriminate the sequences when the frequency ranges of the target and distractor sequences did not overlap, but they could not when the ranges overlapped. Subsequent probe tests confirmed that the discrimination depended on cues other than the local pitch of the component tones regardless of the presence of the distractor sequence. The results suggest that monkeys segregate tone sequences based on frequency proximity, and they perceive global characters of the segregated streams.