A recognition test in monkeys to differentiate recollection from familiarity memory.

Episodic memory is memory for experiences within a specific temporal and spatial context. Episodic memories decline early in Alzheimer's Disease (AD). Recollection of episodic memories can fail with both AD and aging, but familiarity and recollection memory uniquely fail in AD. Finding a means to differentiate specific memory failures in animal models is critical for translational research. Four cotton top tamarins participated in an object recognition test. They were exposed to two unique objects placed in a consistent context for 5 daily sessions. Next a delay of 1 day or 1 week was imposed. Subjects' memory of the objects was tested by replacing one of the familiarized objects with a novel one. The tamarins looked longer at the novel object after both delays, an indication of remembering the familiar object. In other tests, the test pair was relocated to a new location or presented at a different time of day. With context changes, tamarins showed greater interest in the novel object after a 1-week delay but not after a 1-day delay. It seems that context changes disrupted their recollection of recent events. But the monkeys showed accurate familiarity memory across context changes with longer delays.

Is inferential reasoning a distinctly human cognitive feature? Testing reasoning in cotton-top tamarins (Saguinus oedipus).

Logical inference is often assumed a human-unique ability, although many species of apes and monkeys have shown some facility within a two-cup task in which one cup is baited, the primate is shown the cup which is empty (an exclusion cue), and subsequently chooses the other baited cup. In published reports, New World monkey species show a limited ability to choose successfully, often with half or more of the subjects tested not showing the ability with auditory cues or with exclusion cues. In this study, five cotton-top tamarins (Saguinus oedipus) were tested in a two-cup task with visual or auditory cues which revealed the presence or absence of bait, and in a second study, were tested with a four-cup array using a variety of walls to define the baiting space and a variety of visual cues including inclusion and exclusion. Tamarins demonstrated the ability to use either visual or auditory exclusion cues to find rewards in the two-cup study, although the visual cue required some exposure before accuracy was expressed. Experiment 2 revealed that two of three tamarins' first guesses to find rewards matched best a logic model. When they made errors, they typically chose cups adjacent to the cued location or made choices that seemed generated from avoiding empty cups. These results suggest that tamarins can deduce the location of food using reasoning, although the ability is only applied robustly to first guesses, while second guesses are motivated by approach/avoidance and proximity to cued locations. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

A modified version of the dimensional change card sort task tests cognitive flexibility in children (Homo sapiens) and cotton-top tamarins (Saguinus oedipus).

A modified Dimensional Change Card Sort (DCCS) task was used to test cognitive flexibility in adult cotton-top tamarins and children aged 19 months to 60 months. Subjects had to infer a rule from the experience of selecting between two cards to earn a reward, and the pairs of stimuli defined the rule (e.g., pick blue ones, not red ones, or pick trucks, not boats). Two different tests measured subjects' ability to shift to a reversal of the rule (intradimensional shift) and to shift to a new rule defined by a dimension previously irrelevant (interdimensional shift). Both adult tamarins and children aged 49-60 months were able to learn the initial rule and switch to a reversal and to a rule based on a different dimension. In contrast, the two younger groups of children, aged 19-36 months and aged 37-48 months, could switch when a reversal was imposed but took significantly longer to learn a new rule on a former irrelevant dimension. Experiment 2 presented a wider set of novel stimuli which shared some features with the original set to further explore the basis of rule learning. The result was that tamarins and 52- to 60-month-old children both chose novel stimuli that fit the rule and had no a priori associative strength, suggesting a rule application not solely based on associative strength. Importantly, novel items introduced some risk for choice, and children showed themselves to be risk-averse, whereas tamarins were risk-prone within a novel context. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Artificial grammar learning in tamarins (Saguinus oedipus) in varying stimulus contexts.

The human ability to detect regularities in sound sequences is a fundamental substrate of our language faculty. However, is this an ability exclusive to human language processing, or have we usurped a more general learning mechanism for this purpose, one shared with other species? The current study is an attempt to replicate and extend Hauser, Weiss, and Marcus's (2002) retracted study (2010) of artificial grammar learning in tamarins to determine if tamarins can detect an underlying grammatical structure in a pattern of sounds. Human language consonant-vowel (CV) combinations from Hauser et al.'s original study, newly created tone sequences, and newly created monkey vocalizations made into sequences were used to familiarize tamarins to an AAB or ABB pattern. Tests of novel sounds in each condition were presented that either were consistent with the familiarized pattern or were different from it. Longer looking times toward the sound source (an audio speaker with a specific location in the auditory field) indicated recognition of novelty. Tamarins looked toward the speaker significantly longer with inconsistent human language CV sequences and with inconsistent tone sequences but not when an inconsistent monkey vocalization was presented. Moreover, tamarins showed differential rates of habituation to the different types of sound patterns, with more robust habituation to CV sequences and tone sequences than to monkey call sequences. The implications of these findings for the generality of learning mechanisms for linguistic and nonlinguistic input across species and the importance of testing across various stimuli are discussed. (PsycINFO Database Record

Gestalt principle use in college students, children with autism, toddlers (Homo sapiens), and cotton top tamarins (Saguinus oedipus).

The use of Gestalt principles of proximity, similarity, and closure to recognize objects by configural superiority was examined in college students, low- and high-functioning children with autism, toddlers, and adult cotton top tamarin monkeys. At issue was whether the monkeys showed differences from humans in perceptual processing and whether they showed any similarities with clinical or developmental groups. The method required a pointing response to discriminate an odd item in a 4-item visual display. All subjects were trained to a high accuracy to point to the odd item before being tested with graphic stimuli that differentiated feature changes based on configural superiority. The results were that college students and high-functioning children with autism responded faster and more accurately to trials in which the odd item was easily noticed by the use of Gestalt principles and configural superiority. Toddlers also responded more accurately to the Gestalt trials, but without being faster at making the response. Low-functioning children with autism and tamarins showed no advantage to Gestalt trials but exhibited different processing styles. The implications of these findings to track the evolution of human perception and to develop a primate model for the perceptual deficits of autism are discussed.

Chasing sounds.

Prior work with Wright and others demonstrated that rhesus monkeys recognized the relative relationships of notes in common melodies. As an extension of tests of pattern similarities, tamarins were habituated to 3-sound unit patterns in an AAB or ABB form that were human phonemes, piano notes, or monkey calls. The subjects were tested with novel sounds in each category constructed either to match the prior pattern or to violate the prior habituated pattern. The monkeys attended significantly more to a violation of their habituated pattern to a new pattern when human phonemes were used, and there was a trend difference in attention toward pattern violations with melodies. Monkey call patterns generated a variety of behavioral responses, were less likely to show habituation, and did not generate a strong attention reaction to changes in the patterns. Monkeys can extract abstract rules and patterns from auditory stimuli but the stimuli, by their nature, may generate competing responses which block processing of abstract regularities.

Is a sense of inequity an ancestral primate trait? Testing social inequity in cotton top tamarins (Saguinus oedipus).

To address a controversy in the literature concerning whether monkeys show an aversion to inequity, individuals of a New World monkey species, cotton top tamarins (Saguinus oedipus) were tested in an offering task and in a bartering task. At issue was whether the monkeys rejected rewards because of a violation of expectancy of the preferred reward, or whether they rejected rewards because of a sensitivity to socially mediated inequity. The data from both tasks indicated that the subjects were more likely to reject when preferred rewards were presented, either because of another animal eating the reward (the social condition) or because of rewards being presented but inaccessible. The bartering task led to the only behavioral indication of aversion due specifically to social inequity, which was demonstrated when tamarins' sensitivity to the difference in rewards increased with exposure to other tamarins working to receive the preferred rewards. The results suggest that social inequity aversion will be assessed by tamarins, and possibly by other primates, only under conditions of limited resources and a requirement of work, which may make the situation a bit more competitive and thus drives attention toward both social and reward evaluation.

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.

Global and local processing in adult humans (Homo sapiens), 5-year-old children (Homo sapiens), and adult cotton-top tamarins (Saguinus oedipus).

This study compared adults (Homo sapiens), young children (Homo sapiens), and adult tamarins (Saguinus oedipus) while they discriminated global and local properties of stimuli. Subjects were trained to discriminate a circle made of circle elements from a square made of square elements and were tested with circles made of squares and squares made of circles. Adult humans showed a global bias in testing that was unaffected by the density of the elements in the stimuli. Children showed a global bias with dense displays but discriminated by both local and global properties with sparse displays. Adult tamarins' biases matched those of the children. The striking similarity between the perceptual processing of adult monkeys and humans diagnosed with autism and the difference between this and normatively developing human perception is discussed.

A test of the generality of perceptually based categories found in infants: attentional differences toward natural kinds by New World monkeys.

A preference to novelty paradigm used to study human infants (Quinn, 2002) examined attention to novel animal pictures at subordinate, basic and superordinate levels in tamarins. First, pairs of pictures were presented in phases, starting with a monkey species (subordinate level) and ending with mammal and dinosaur sets (superordinate levels). After each phase, tests paired novel pictures from the familiarized set with a novel broader category. Look rates toward each picture were coded. Tamarins looked significantly longer at a novel species after being familiarized with a monkey species, a species-specific effect. Subjects attended equivalently to novel primate species after habituation to four monkey species, but looked significantly longer at pictures of mammals, marking a more global-level inclusion and exclusion. Superordinate testing revealed that more novel and diverse sets were differentiated attentionally. The evidence implies that natural categorical representation occurs at an attentional level in primates in ways similar to human infants, and is affected by recent exposure and category variability.

A test of object permanence in a new-world monkey species, cotton top tamarins (Saguinus oedipus).

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.

Use of experimenter-given cues in visual co-orienting and in an object-choice task by a new world monkey species, cotton top tamarins (Saguinus oedipus).

Two methods assessed the use of experimenter-given directional cues by a New World monkey species, cotton top tamarins (Saguinus oedipus). Experiment 1 used cues to elicit visual co-orienting toward distal objects. Experiment 2 used cues to generate responses in an object-choice task. Although there were strong positive correlations between monkey pairs to co-orient, visual co-orienting with a human experimenter occurred at a low frequency to distal objects. Human hand pointing cues generated more visual co-orienting than did eye gaze to distal objects. Significant accurate choices of baited cups occurred with human point and tap cues and human look cues. Results highlight the importance of head and body orientation to induce shared attention in cotton top tamarins, both in a task that involved food getting and a task that did not.