Nonverbal working memory of humans and monkeys: Rehearsal in the sketchpad?

Investigations of working memory tend to focus on the retention of verbal information. The present experiments were designed to characterize the active maintenance rehearsal process used in the retention of visuospatial information. Rhesus monkeys (Macaca mulatta;N=6) were tested as well as humans (totalN=90) because these nonhuman primates have excellent visual working memory but, unlike humans, cannot verbally recode the stimuli to employ verbal rehearsal mechanisms. A series of experiments was conducted using a distractor-task paradigm, a directed forgetting procedure, and a dual-task paradigm. No evidence was found for an active maintenance process for either species. Rather, it appears that information is maintained in the visuospatial sketchpad without active rehearsal.     

Motivational systems of social behavior in male rats and monkeys: Are they homologous?

A comparison is presented between the behaviors of male rats and male stumptail macaques that occur when two unfamiliar males are paired for 10 min. Results which have been presented in detail in separate papers elsewhere are compared and discussed here in terms of the hypothetical organization of motivational systems. The following motivational mechanisms appear to be homologous in the rat and monkey: offense, defense, submission, male sex, self grooming, and allogrooming. Two motivational mechanisms are analogous but not homologous: patrol/marking in the rat and display in the monkey. There is a shift in sensory modality of motivating stimuli from olfaction in the rat to complex visual and auditory stimuli in the monkey. There is also a shift in the modalities of motor patterns from predominant use of the mouth by the rat to use of the hands by the monkey. Both shifts affect most or all motivational systems of social behavior. It is hypothesized that the outer parts of motivational systems, their sensory and motor interfaces with the environment, change more rapidly and incrementally during the course of mammalian evolution than does the inner part, the integrational portion that consists of the motivational mechanisms.     

Do apes and monkeys rely upon conceptual reversibility?

The ability to seriate nesting cups as a sensorimotor task has posed interesting questions for cognitive scientists. Greenfield et al. [(1972) Cognit Psychol 3:291–310] found parallels between children's combinatorial activity with nesting cups and patterns of phonological and grammatical constructions. The parallels suggested the possibility of a neurally based developmental homology between language and instrumental action [Greenfield (1991) Behav Brain Sci 14:531–595]. Children who predominantly used subassembly, a hierarchical method of combining cups, succeeded at seriating nesting cups more often than those who did not. Greenfield and others [e.g., Piaget and Inhelder (1969) The psychology of the child. Basic Books, New York; DeLoache et al. (1985) Child Dev 56:928–939] argued that success in seriation reflects the child's growing recognition of a reversible relationship: a particular element in a series is conceived of as being smaller than the previous element and larger than the subsequent element. But is a concept of reversibility or a hierarchical form of object manipulation necessary to seriate cups? In this article, we review studies with very young children and nonhuman primates to determine how individuals that do not evidence conceptual reversibility manage the seriation task. We argue that the development of skill in seriation is experientially, rather than conceptually, driven and that it may be unnecessary to link seriation with cognitive conceptions of reversibility or linguistic capacities. Rather, in ordering a set of objects by size, perceptual-motor learning may enable contemplative refinement. Accepted after revision: 10 September 2001 Electronic Publication     

Is the inversion effect in rhesus monkeys face-specific?

This study investigated the face inversion effect in rhesus monkeys (Macaca mulatta). Face stimuli consisted of ten black-and-white examples of unfamiliar rhesus monkey faces, brown capuchin faces, and human faces. Two non-face categories included ten examples of automobiles and abstract shapes. All stimuli were presented in a sequential matching-to-sample format using an automated joystick-testing paradigm. Subjects performed significantly better on upright than on inverted presentations of automobiles, rhesus monkey and capuchin faces, but not human faces or abstract shapes. These results are inconsistent with data from humans and chimpanzees that show the inversion effect only for categories of stimuli for which subjects have developed expertise. The inversion effect in rhesus monkeys does not appear to be face-specific, and should therefore not be used as a marker of specialized face processing in this species. Received: 18 November 1998 / Accepted after revision: 9 May 1999     

Call combinations in monkeys: compositional or idiomatic expressions?

Syntax is widely considered the feature that most decisively sets human language apart from other natural communication systems. Animal vocalisations are generally considered to be holistic with few examples of utterances meaning something other than the sum of their parts. Previously, we have shown that male putty-nosed monkeys produce call series consisting of two call types in response to different events. They can also be combined into short sequences that convey a different message from those conveyed by either call type alone. Here, we investigate whether ‘pyow-hack’ sequences are compositional in that the individual calls contribute to their overall meaning. However, the monkeys behaved as if they perceived the sequence as an idiomatic expression rather than decoding the sequence. Nonetheless, while this communication system lacks the generative power of syntax it enables callers to increase the number of messages that can be conveyed by a small and innate call repertoire.     

How monkeys see the eyes: cotton-top tamarins’ reaction to changes in visual attention and action

Among social species, the capacity to detect where another individual is looking is adaptive because gaze direction often predicts what an individual is attending to, and thus what its future actions are likely to be. We used an expectancy violation procedure to determine whether cotton-top tamarins (Saguinus oedipus oedipus) use the direction of another individual’s gaze to predict future actions. Subjects were familiarized with a sequence in which a human actor turned her attention toward one of two objects sitting on a table and then reached for that object. Following familiarization, subjects saw two test events. In one test event, the actor gazed at the new object and then reached for that object. From a human perspective, this event is considered consistent with the causal relationship between visual attention and subsequent action, that is, grabbing the object attended to. In the second test event, the actor gazed at the old object, but reached for the new object. This event is considered a violation of expectation. When the actor oriented with both her head-and-eyes, subjects looked significantly longer at the second test event in which the actor reached for the object to which she had not previously oriented. However, there was no difference in looking time between test events when the actor used only her eyes to orient. These findings suggest that tamarins are able to use some combination of head orientation and gaze direction, but not gaze direction alone, to predict the actions of a human agent. Received: 17 February 1999 / Accepted after revision: 9 May 1999     

Exploration and learning in capuchin monkeys (Sapajus spp.): the role of action–outcome contingencies

Animals have a strong propensity to explore the environment. Spontaneous exploration has a great biological significance since it allows animals to discover and learn the relation between specific behaviours and their consequences. The role of the contingency between action and outcome for learning has been mainly investigated in instrumental learning settings and much less in free exploration contexts. We tested 16 capuchin monkeys (Sapajus spp.) with a mechatronic platform that allowed complex modules to be manipulated and to produce different outcomes. Experimental subjects could manipulate the modules and discover the contingencies between their own specific actions and the outcomes produced (i.e., the opening and lighting of a box). By contrast, Control subjects could operate on the modules, but the outcomes experienced were those performed by their paired Experimental subjects (“yoked-control” paradigm). In the exploration phase, in which no food reward was present, Experimental subjects spent more time on the board and manipulated the modules more than Yoked subjects. Experimental subjects outperformed Yoked subjects in the following test phase, where success required recalling the effective action so to open the box, now baited with food. These findings demonstrate that the opportunity to experience action–outcome contingencies in the absence of extrinsic rewards promotes capuchins’ exploration and facilitates learning processes. Thus, this intrinsically motivated learning represents a powerful mechanism allowing the acquisition of skills and cognitive competence that the individual can later exploit for adaptive purposes.     

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.     

Individual differences in the responses of naïve rhesus monkeys to snakes

The authors demonstrated individual differences in inhibited behavior and withdrawal responses of laboratory-born rhesus monkeys when initially exposed to a snake. Most monkeys displayed a small significant increase in their behavioral inhibition in the presence of a snake. A few monkeys had marked responses, and some actively withdrew. Although the responses of the most extreme laboratory-born monkeys were comparable to feral-born monkeys, the responses of the laboratory-born monkeys rapidly habituated. The individual differences in the responses of na?ve monkeys likely reflect a continuum from orienting to wariness to fear. A neurobiological model is presented that addresses potential mechanisms underlying these individual differences, their relation to fear, and how they may predispose to phobia development.     

Can rhesus monkeys spontaneously subtract?

Animals, including pigeons, parrots, raccoons, ferrets, rats, New and Old World monkeys, and apes are capable of numerical computations. Much of the evidence for such capacities is based on the use of techniques that require training. Recently, however, several studies conducted under both laboratory and field conditions have employed methods that tap spontaneous numerical representations in animals, including human infants. In this paper, we present the results of 11 experiments exploring the capacity of semi-free-ranging adult rhesus monkeys to spontaneously compute (i.e. single trial, no training) the outcome of subtraction events. In the basic design, we present one quantity of objects on one stage, a second quantity on a second stage, occlude both stages, and then remove one or no objects from each stage. Having watched these events, a subject is then allowed to approach one stage and eat the food objects behind the occluder. Results show that rhesus monkeys correctly compute the outcome of subtraction events involving three or less objects on each stage, even when the identity of the objects is different. Specifically, when presented with two food quantities, rhesus monkeys select the larger quantity following subtractions of one piece of food from two or three; this preference is maintained when subjects must distinguish food from non-food subtractions, and when food is subtracted from either one or both initial quantities. Furthermore, rhesus monkeys are capable of representing zero as well as equality when two identical quantities are contrasted. Results are discussed in light of recent attempts to determine how number is represented in the brains of animals lacking language.     

Metacognitive monkeys or associative animals? Simple reinforcement learning explains uncertainty in nonhuman animals

Monkeys will selectively and adaptively learn to avoid the most difficult trials of a perceptual discrimination learning task. Couchman, Coutinho, Beran, and Smith (2010) have recently demonstrated that this pattern of responding does not depend on animals receiving trial-by-trial feedback for their responses; it also obtains if experience of the most difficult trials occurs only under conditions of deferred feedback. Couchman et al. argued that this ruled out accounts based on low-level processes of associative learning and instead required explanation in terms of metacognitive processes of decision monitoring. Contrary to this argument, a simple associative model of reinforcement learning is shown to account for the key findings of Couchman et al.'s empirical study, along with several other findings that have previously been claimed to challenge associative models.     

Stroop-like effects for monkeys and humans: processing speed or strength of association?

Abstract— Stroop-like effects have been found using a variety of paradigms and subject groups In the present investigation, 6 rhesus monkeys (Macaca mulatta) and 28 humans exhibited Stroop-like inserference and facilitation in a relativenumerousness task Monkeys, like humans, processed the meanings of the numerical symbols automatically—despite the fact that these meanings were irrelevant to task performance These data also afforded direct comparison of interpretations of the Stroop effect in terms of processing speed versus association strength These findings were consistent with parallel-processing models of Stroop-like interference proposed elsewhere, but not with processing-speed accounts posited frequently to explain the effect     

Do rhesus monkeys (Macaca mulatta) attribute knowledge and ignorance to others?

The ability of 4 rhesus monkeys (Macaca mulatta) to understand the causal connection between seeing and knowing was investigated. The subjects were tested to determine if they could discriminate between information provided by experimenters who randomly alternated between roles of guesser and knower. In a series of tests, the knower either hid food under 1 of 3 cups or watched as someone else hid the food. The guesser waited outside the room or covered her or his head until the food was hidden. The subjects watched this procedure occur but could not see which cup the food was hidden under. The knower pointed to the correct cup while the guesser pointed to an incorrect one. None of the macaques provided any evidence that they realized the different states of knowledge possessed by the guesser and knower. The results are consistent with the hypothesis that rhesus macaques are incapable of making inferences about the mental states of others.     

Essentialism in the absence of language? Evidence from rhesus monkeys (Macaca mulatta)

We explored whether rhesus monkeys (Macaca mulatta) share one important feature of human essentialist reasoning: the capacity to track category membership across radical featural transformations. Specifically, we examined whether monkeys – like children ( Keil, 1989 ) – expect a transformed object to have the internal properties of its original category. In two experiments, monkeys watched as an experimenter visually transformed a familiar fruit (e.g. apple) into a new kind of fruit (e.g. coconut) either by placing a fruit exterior over the original, or by removing an exterior shell and revealing the inside kind of fruit. The experimenter then pretended to place an inside piece of the transformed fruit into a box which the monkey was allowed to search. Results indicated that monkeys searched the box longer when they found a piece of fruit inconsistent with the inside kind, suggesting that the monkeys expected that the inside of the transformed fruit would taste like the innermost kind they saw. These results suggest that monkeys may share at least one aspect of psychological essentialism: They maintain category‐specific expectations about an object’s internal properties even when that object’s external properties change. These results therefore suggest that some essentialist expectations may emerge in the absence of language, and thus raise the possibility that such tendencies may emerge earlier in human development than has previously been considered.     

Capuchin monkeys’ use of human and conspecific cues to solve a hidden object-choice task

Learning by watching others can provide valuable information with adaptive consequences, such as identifying the presence of a predator or locating a food source. The extent to which nonhuman animals can gain information by reading the cues of others is often tested by evaluating responses to human gestures, such as a point, and less often evaluated by examining responses to conspecific cues. We tested whether ten brown capuchin monkeys (Cebus [Sapajus] apella) were able to use cues from monkeys and a pointing cue from a human to obtain hidden rewards. A monkey could gain access to a reward hidden in one of two locations by reading a cue from a conspecific (e.g., reaching) or a human pointing. We then tested whether they could transfer this skill from monkeys to humans, from humans to monkeys, and from one conspecific to another conspecific. One group of monkeys was trained and tested using a conspecific as the cue-giver and was then tested with a human cue-giver. The second group of monkeys was trained and tested with a human cue-giver and was then tested with a monkey cue-giver. Monkeys that were successful with a conspecific cue-giver were also tested with a novel conspecific cue-giver. Monkeys learned to use a human point and conspecific cues to obtain rewards. Monkeys that had learned to use the cues of a conspecific to obtain rewards performed significantly better than expected by chance when they were transferred to the cues of a novel conspecific. Monkeys that learned to use a human point to obtain rewards performed significantly better than expected by chance when tested while observing conspecific cues. Some evidence suggested that transferring between conspecific cue-givers occurred with more facility than transferring across species. Results may be explained by simple rules of association learning and stimulus generalization; however, spontaneous flexible use of gestures across conspecifics and between different species may indicate capuchins can generalize learned social cues within and partially across species.     

Do monkeys compare themselves to others?

Social comparisons are a fundamental characteristic of human behaviour, yet relatively little is known about their evolutionary foundations. Adapting the co-acting paradigm from human research (Seta in J Pers Soc Psychol 42:281–291, 1982. doi: 10.1037//0022-3514.42.2.281), we examined how the performance of a partner influenced subjects’ performance in long-tailed macaques (Macaca fascicularis). Using parallel testing in touch screen setups in which subjects had to discriminate familiar and novel photographs of men and women, we investigated whether accuracy and reaction time were influenced by partner performance and relationship quality (affiliate vs. non-affiliate). Auditory feedback about the alleged performance of the co-actor was provided via playback; partner performance was either moderately or extremely better or worse than subject performance. We predicted that subjects would assimilate to moderately different comparison standards as well as to affiliates and contrast away from extreme standards and non-affiliates. Subjects instantly generalized to novel pictures. While accuracy was not affected by any of the factors, long reaction times occurred more frequently when subjects were tested with a non-affiliate who was performing worse, compared to one who was doing better than them (80 % quantile worse: 5.1, better: 4.3 s). For affiliate co-actors, there was no marked effect (worse: 4.4, better: 4.6 s). In a control condition with no auditory feedback, subjects performed somewhat better in the presence of affiliates (M = 77.8 % correct) compared to non-affiliates (M = 71.1 %), while reaction time was not affected. Apparently, subjects were sensitive to partner identity and performance, yet variation in motivation rather than assimilation and contrast effects may account for the observed effects.     

Audiovisual integration facilitates monkeys’ short-term memory

Many human behaviors are known to benefit from audiovisual integration, including language and communication, recognizing individuals, social decision making, and memory. Exceptionally little is known about the contributions of audiovisual integration to behavior in other primates. The current experiment investigated whether short-term memory in nonhuman primates is facilitated by the audiovisual presentation format. Three macaque monkeys that had previously learned an auditory delayed matching-to-sample (DMS) task were trained to perform a similar visual task, after which they were tested with a concurrent audiovisual DMS task with equal proportions of auditory, visual, and audiovisual trials. Parallel to outcomes in human studies, accuracy was higher and response times were faster on audiovisual trials than either unisensory trial type. Unexpectedly, two subjects exhibited superior unimodal performance on auditory trials, a finding that contrasts with previous studies, but likely reflects their training history. Our results provide the first demonstration of a bimodal memory advantage in nonhuman primates, lending further validation to their use as a model for understanding audiovisual integration and memory processing in humans.     

Does own experience affect perception of others’ actions in capuchin monkeys (Cebus apella)?

Anticipating another’s actions is an important ability in social animals. Recent research suggests that in human adults and infants one’s own action experience facilitates understanding and anticipation of others’ actions. We investigated the link between first-person experience and perception of another’s action in adult tufted capuchin monkeys (Sapajus apella spp., formerly Cebus apella spp.). In Experiment 1, the monkeys observed a familiar human (actor) trying to open a container using either a familiar or an unfamiliar action. They looked for longer when the actor tried to open the container using a familiar action. In Experiment 2, the actor performed two novel actions on a new container. The monkeys looked equally at the two actions. In Experiment 3, the monkeys were trained to open the container using one of the novel actions in Experiment 2. After training, we repeated the same procedure as in Experiment 2. The monkeys looked for longer when the actor manipulated the container using the action they had practiced than when she used the unfamiliar action. These results show that knowledge derived from one’s own experience impacts perception of another’s action in these New World monkeys.     

How do tufted capuchin monkeys (Cebus apella) understand causality involved in tool use?

Four tufted capuchin monkeys (Cebus apella) were trained to choose from 2 hook-like tools, 1 of which successfully led to collecting food, whereas the other did not because of inappropriate spatial arrangement of the tool and the food. In Experiment 1, all of the monkeys successfully learned the basic task. The monkeys performed successfully with tools of novel colors and shapes in Experiments 2-5. These results demonstrate that the monkeys used the spatial arrangement of the tool and the food as a cue. However, they failed when there were obstacles (Experiment 6) or traps (Experiment 7) on the path along which the monkeys dragged tools. These results may suggest that capuchin monkeys understand the spatial relationship between 2 items, namely, food and the tool, but do not understand the spatial relationship among 3 items, namely, food, tool, and the environmental condition. The possible role of stimulus generalization is also considered.