“Counting” serially presented stimuli by human and nonhuman primates and pigeons

Much of Stewart Hulse's career was spent analyzing how animals can extract patterned information from sequences of stimuli. Yet an additional form of information contained in a sequence may be the number of times different elements occurred. Experiments that required numerical discrimination between different stimulus items presented in sequence are analyzed for primates and pigeons. It is shown that a model based on magnitude discrimination can account well for data from human and nonhuman primate experiments. Similar experiments carried out with pigeons showed a strong recency effect not found with primates. The pigeon data are modeled successfully, however, by assuming that representations of events decay as other events are presented.     

Left gaze bias in humans, rhesus monkeys and domestic dogs

While viewing faces, human adults often demonstrate a natural gaze bias towards the left visual field, that is, the right side of the viewee’s face is often inspected first and for longer periods. Using a preferential looking paradigm, we demonstrate that this bias is neither uniquely human nor limited to primates, and provide evidence to help elucidate its biological function within a broader social cognitive framework. We observed that 6-month-old infants showed a wider tendency for left gaze preference towards objects and faces of different species and orientation, while in adults the bias appears only towards upright human faces. Rhesus monkeys showed a left gaze bias towards upright human and monkey faces, but not towards inverted faces. Domestic dogs, however, only demonstrated a left gaze bias towards human faces, but not towards monkey or dog faces, nor to inanimate object images. Our findings suggest that face- and species-sensitive gaze asymmetry is more widespread in the animal kingdom than previously recognised, is not constrained by attentional or scanning bias, and could be shaped by experience to develop adaptive behavioural significance.     

Face processing in humans and new world monkeys: the influence of experiential and ecological factors

This study tests whether the face-processing system of humans and a nonhuman primate species share characteristics that would allow for early and quick processing of socially salient stimuli: a sensitivity toward conspecific faces, a sensitivity toward highly practiced face stimuli, and an ability to generalize changes in the face that do not suggest a new identity, such as a face differently oriented. The look rates by adult tamarins and humans toward conspecific and other primate faces were examined to determine if these characteristics are shared. A visual paired comparison (VPC) task presented subjects with either a human face, chimpanzee face, tamarin face, or an object as a sample, and then a pair containing the previous stimulus and a novel stimulus was presented. The stimuli were either presented all in an upright orientation, or all in an inverted orientation. The novel stimulus in the pair was either an orientation change of the same face/object or a new example of the same type of face/object, and the stimuli were shown either in an upright orientation or in an inverted orientation. Preference to novelty scores revealed that humans attended most to novel individual human faces, and this effect decreased significantly if the stimuli were inverted. Tamarins showed preferential looking toward novel orientations of previously seen tamarin faces in the upright orientation, but not in an inverted orientation. Similarly, their preference to look longer at novel tamarin and human faces within the pair was reduced significantly with inverted stimuli. The results confirmed prior findings in humans that novel human faces generate more attention in the upright than in the inverted orientation. The monkeys also attended more to faces of conspecifics, but showed an inversion effect to orientation change in tamarin faces and to identity changes in tamarin and human faces. The results indicate configural processing restricted to particular kinds of primate faces by a New World monkey species, with configural processing influenced by life experience (human faces and tamarin faces) and specialized to process orientation changes specific to conspecific faces.     

Spontaneous number discrimination of multi-format auditory stimuli in cotton-top tamarins (Saguinus oedipus)

Studies using operant training have demonstrated that laboratory animals can discriminate the number of objects or events based on either auditory or visual stimuli, as well as the integration of both auditory and visual modalities. To date, studies of spontaneous number discrimination in untrained animals have been restricted to the visual modality, leaving open the question of whether such capacities generalize to other modalities such as audition. To explore the capacity to spontaneously discriminate number based on auditory stimuli, and to assess the abstractness of the representation underlying this capacity, a habituation-discrimination procedure involving speech and pure tones was used with a colony of cotton-top tamarins. In the habituation phase, we presented subjects with either two- or three-speech syllable sequences that varied with respect to overall duration, inter-syllable duration, and pitch. In the test phase, we presented subjects with a counterbalanced order of either two- or three-tone sequences that also varied with respect to overall duration, inter-syllable duration, and pitch. The proportion of looking responses to test stimuli differing in number was significantly greater than to test stimuli consisting of the same number. Combined with earlier work, these results show that at least one non-human primate species can spontaneously discriminate number in both the visual and auditory domain, indicating that this capacity is not tied to a particular modality, and within a modality, can accommodate differences in format.     

Nonhuman primates prefer slow tempos but dislike music overall

Human adults generally find fast tempos more arousing than slow tempos, with tempo frequently manipulated in music to alter tension and emotion. We used a previously published method [McDermott, J., & Hauser, M. (2004). Are consonant intervals music to their ears? Spontaneous acoustic preferences in a nonhuman primate. Cognition, 94(2), B11-B21] to test cotton-top tamarins and common marmosets, two new-World primates, for their spontaneous responses to stimuli that varied systematically with respect to tempo. Across several experiments, we found that both tamarins and marmosets preferred slow tempos to fast. It is possible that the observed preferences were due to arousal, and that this effect is homologous to the human response to tempo. In other respects, however, these two monkey species showed striking differences compared to humans. Specifically, when presented with a choice between slow tempo musical stimuli, including lullabies, and silence, tamarins and marmosets preferred silence whereas humans, when similarly tested, preferred music. Thus despite the possibility of homologous mechanisms for tempo perception in human and nonhuman primates, there appear to be motivational ties to music that are uniquely human.     

Information seeking by rhesus monkeys (Macaca mulatta) and capuchin monkeys (Cebus apella)

Animal metacognition is an active, growing research area, and one part of metacognition is flexible information-seeking behavior. In Roberts et al. (2009), pigeons failed an intuitive information-seeking task. They basically refused, despite multiple fostering experiments, to view a sample image before attempting to find its match. Roberts et al. concluded that pigeons’ lack of an information-seeking capacity reflected their broader lack of metacognition. We report a striking species contrast to pigeons. Eight rhesus macaques and seven capuchin monkeys passed the Roberts et al. test of information seeking—often in their first testing session. Members of both primate species appreciated immediately the lack of information signaled by an occluded sample, and the need for an information-seeking response to manage the situation. In subsequent testing, macaques demonstrated flexible/varied forms of information management. Capuchins did not. The research findings bear on the phylogenetic distribution of metacognition across the vertebrates, and on the underlying psychological requirements for metacognitive and information-seeking performances.     

Macaques’ (Macaca mulatta) use of numerical cues in maze trials

We tested the ability of number-trained rhesus monkeys to use Arabic numeral cues to discriminate between different series of maze trials and anticipate the final trial in each series. The monkeys prior experience with numerals also allowed us to investigate spontaneous transfer between series. A total of four monkeys were tested in two experiments. In both experiments, the monkeys were trained on a computerized task consisting of three reinforced maze trials followed by one nonreinforced trial. The goal of the maze was an Arabic numeral 3, which corresponded to the number of reinforced maze trials in the series. In experiment 1 (n=2), the monkeys were given probe trials of the numerals 2 and 4 and in experiment 2 (n=2), they were given probe trials of the numerals 2–8. The monkeys receiving the probe trials 2 and 4 showed some generalization to the new numerals and developed a pattern of performing more slowly on the nonreinforced trial than the reinforced trial before it for most series, indicating the use of the changing numeral cues to anticipate the nonreinforced trial. The monkeys receiving probe trials of the numerals 2–8 did not predict precisely when the nonreinforced trial would occur in each series, but they did incorporate the changing numerals into their strategy for performing the task. This study provides the first evidence that number-trained monkeys can use Arabic numerals to perform a task involving sequential presentations.     

Grammatical pattern learning by human infants and cotton-top tamarin monkeys

There is a surprising degree of overlapping structure evident across the languages of the world. One factor leading to cross-linguistic similarities may be constraints on human learning abilities. Linguistic structures that are easier for infants to learn should predominate in human languages. If correct, then (a) human infants should more readily acquire structures that are consistent with the form of natural language, whereas (b) non-human primates' patterns of learning should be less tightly linked to the structure of human languages. Prior experiments have not directly compared laboratory-based learning of grammatical structures by human infants and non-human primates, especially under comparable testing conditions and with similar materials. Five experiments with 12-month-old human infants and adult cotton-top tamarin monkeys addressed these predictions, employing comparable methods (familiarization-discrimination) and materials. Infants rapidly acquired complex grammatical structures by using statistically predictive patterns, failing to learn structures that lacked such patterns. In contrast, the tamarins only exploited predictive patterns when learning relatively simple grammatical structures. Infant learning abilities may serve both to facilitate natural language acquisition and to impose constraints on the structure of human languages.     

A test of object permanence in a new-world monkey species,cotton top tamarins (<Emphasis Type="Italic">Saguinus oedipus</Emphasis>)

Cotton top tamarins were tested in visible and invisible displacement tasks in a method similar to that used elsewhere to test squirrel monkeys and orangutans. All subjects performed at levels significantly above chance on visible (n=8) and invisible (n=7) displacements, wherein the tasks included tests of the perseverance error, tests of memory in double and triple displacements, and "catch" trials that tested for the use of the experimenter's hand as a cue for the correct cup. Performance on all nine tasks was significantly higher than chance level selection of cups, and tasks using visible displacements generated more accurate performance than tasks using invisible displacements. Performance was not accounted for by a practice effect based on exposure to successive tasks. Results suggest that tamarins possess stage 6 object permanence capabilities, and that in a situation involving brief exposure to tasks and foraging opportunities, tracking objects' movements and responding more flexibly are abilities expressed readily by the tamarins. Electronic Publication     

Mangabeys (<Emphasis Type="Italic">Cercocebus torquatus lunulatus</Emphasis>) solve the reverse contingency task without a modified procedure

Problem solving often relies on generating new responses while inhibiting others, particularly prepotent ones. A paradigm to study inhibitory abilities is the reverse contingency task (Boysen and Berntson in J Exp Psychol Anim Behav Process 21:82–86, 1995), in which two different quantities of food are offered to an individual who receives the array he did not choose. Therefore, mastery of the task demands selecting the smaller quantity to obtain the larger one. Several non-human primates have been tested in the reverse contingency task. To date, only great apes and rhesus monkeys (Macaca mulatta) have succeeded in the original task, with no need of procedural modifications as the large-or-none contingency, correction trials or symbolic stimuli substituting for actual food quantities. Here, four mangabeys were presented with two stimulus arrays of one and four raisins in the context of the reverse contingency task. Three of them learned to perform the task well above chance without a modified procedure. They also reached above-chance performance when presented with two stimulus arrays of zero and four raisins, despite the initial difficulty of choosing a null quantity. After a period of 7–10 months, in which the animals were not tested on any task, all three subjects continued to perform well, even when presented with novel quantity pairs.