Task preparation in macaque monkeys (<Emphasis Type="Italic">Macaca mulatta</Emphasis>)

We investigated whether macaque monkeys possess the ability to prepare abstract tasks in advance. We trained two monkeys to use different stimulus-response (S-R) mappings. On each trial, monkeys were first informed with a visual cue which of two S-R mapping to use. Following a delay, a visual target was presented to which they would respond with a left or right button-press. We manipulated delay time between cue and target and found that performance was faster and more accurate with longer delays, suggesting that monkeys used the delay time to prepare each task in advance. Electronic Publication     

Visually guided facial actions in rhesus monkeys

We trained 2 monkeys to display facial actions in response to corresponding arbitrary visual cues. Each monkey executed the task successfully, and each displayed two different facial actions corresponding to either hand-sign or color cues. More than 90% of the responses were correct for each monkey. These results provide evidence that monkeys can execute facial actions in response to conditioned visual cues in the absence of social context. These data suggest that facial actions of monkeys are flexible enough for use in further laboratory investigations—for example, in studies on the neural mechanisms underlying the execution of actions.     

Behavior controlled by scheduled injections of cocaine in squirrel and rhesus monkeys.

Rates and patterns of key-press responding maintained under schedules in which responding resulted in intravenous injections of cocaine were studied in squirrel monkeys and rhesus monkeys. Each injection was followed by a 60- or 100-sec timeout period. Schedule-controlled behavior was obtained at appropriate cocaine doses in each species. Under FR 10 or FR 30 schedules, performance was characterized by high rates of responding (usually more than one response per second) in each ratio. Under FI 5-min schedules, performance was characterized by an initial pause, followed by acceleration of responding to a final rate that was maintained until the end of the interval. Under multiple fixed-ratio fixed-interval schedules, rates and patterns of responding appropriate to each schedule component were maintained. Responding seldom occurred during timeout periods under any schedule studied. At doses of cocaine above or below those that maintained characteristic schedule-controlled behavior, rates of responding were relatively low and patterns of responding were irregular. Characteristic fixed-interval responding was maintained over a wider range of cocaine doses than characteristic fixed-ratio responding. Complex patterns of responding controlled by discriminative stimuli under fixed-ratio or fixed-interval schedules can be maintained by cocaine injections in squirrel monkeys and rhesus monkeys.     

Deterioration of planning ability with age in Japanese monkeys (Macaca fuscata)

To investigate the ability of aged monkeys to plan and the effect of aging on this ability, performance in a food retrieval task was assessed in aged and younger Japanese monkeys (Macaca fuscata). In this task, the monkeys had to retrieve food items by selecting from a set of 9 holes, each of which contained 1 food item. Results showed that task performance declined significantly with age. All monkeys showed, to a greater or lesser extent, some consistent patterns in their sequence of selecting holes for retrieving the food item. An analysis of these selection patterns indicated that the younger monkeys showed more consistent sequences in selection than the aged monkeys. Furthermore, success in the task performance correlated strongly with higher consistency in the sequence of selecting holes. The authors simulated performance for this task by monkeys without any strategies or plans. The results suggest that the empirical data were far more systematic than the simulated data. Thus, the authors conclude that Japanese monkeys have the ability to plan and that this ability to plan deteriorates with age.     

恒河猴数相加能力的初步研究

本实验训练恒河猴对两组其和不超过8的刺激实体(卡片上的黑色圆点)进行相加,再与第三组刺激实体进行数多少的比较判断。实验共有9个训练程序,课题逐次由易到难,刺激的数目也由少到多。有一只恒河猴达到了全部9个程序的训练标准。证明恒河猴的确具有学会把两个数进行相加的能力。这种相加不可能是数数的结果,极可能是在知觉上将它们融合或接合在一起。     

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.     

Goal-oriented, flexible use of numerical operations by monkeys

Previous studies have shown that elementary aspects of numerical abilities have developed in non-human primates. In the present study, we explored the potential for the development of a novel ability in the use of numerical operations by macaque monkeys (Macaca fuscata): adequate selection of a series of numerical actions toward achieving a behavioral goal. We trained monkeys to use a pair of devices to selectively add or subtract items to/from a digital array in order to match a previously viewed sample array. The monkeys determined whether to add or subtract on the basis of the feedback about numerosity given to the monkeys, which was displayed as an outcome of each step of the numerical operation. We also found that monkeys adapted flexibly to changes in the numerical rule that determined the relationship between device use and numerical operation. Our model analysis found that the numerosity-based model was a better fit for the monkeys’ performance than was the reward-expectation-based model. Such a capacity for goal-oriented selection of numerical operations suggests a mechanism by which monkeys use numerical representations for purposeful behaviors.     

Tolerance to and residual effects of cocaine in squirrel monkeys depend on reinforcement-schedule parameter.

Lever pressing by 4 squirrel monkeys was maintained under a three-component multiple fixed-ratio schedule of food presentation; components differed with respect to ratio size. For each monkey, acute administration of cocaine (0.03 to 1.3 mg/kg, i.m.) produced dose-dependent decreases in overall response rate in each component. During repeated daily administration of 1.0 mg/kg of cocaine, tolerance developed to the rate-decreasing effects under each of the ratio contingencies, but developed to a greater extent and was evident in earlier parts of sessions for performance under the smaller ratios. Response rates of 2 monkeys increased above nondrug control levels despite the putative reinforcer not being consumed during the session. When saline or a smaller dose of cocaine was substituted for 1.0 mg/kg, response rates often were suppressed below nondrug control-level responding. This suppressive effect was observed in each monkey and was more likely to be observed and/or to be of greater magnitude in large-ratio components for 3 of the 4 monkeys. When saline was administered chronically at the end of the chronic-drug phase, response rates remained suppressed in the large-ratio component for 2 of the monkeys. There was, therefore, a schedule-dependent dissociation between behavioral tolerance and the residual effects: Tolerance was greater when small ratios were arranged, whereas the residual effects were more pronounced when larger ratios were arranged.     

Control of responding by sound location in monkeys: rapid acquisition in darkness.

Rapid control of responding by sound location is obtained in squirrel monkeys when sound stimuli are presented from one of two loudspeakers, each one adjacent to a response key. With this arrangement of loudspeakers and response keys, squirrel monkeys quickly learn to respond on the key near the source of the sound stimulus, and this pattern is the same whether or not responses near the sound source are differentially reinforcedmthis result may depend on a pre-experimental tendency in squirrel monkeys to orient head and eyes toward a sound, which would lead the animal to look at the response key in front of the loudspeaker producing the sound. The present experiment sought to determine whether visual stimuli are necessary for rapid control of responding by sound location. Two monkeys were trained in darkness in a sound-localization task similar to that described above. Results were similar to those obtained from animals trained in light, indicating that visual stimuli are not required for rapid acquisition of sound-localization behavior in monkeys.     

Rhesus monkeys (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) discriminate between knowing and not knowing and collect information as needed before acting

Humans use memory awareness to determine whether relevant knowledge is available before acting, as when we determine whether we know a phone number before dialing. Such metacognition, or thinking about thinking, can improve selection of appropriate behavior. We investigated whether rhesus monkeys (Macaca mulatta) are capable of a simple form of metacognitive access to the contents of short-term memory. Monkeys chose among four opaque tubes, one of which concealed food. The tube containing the reward varied randomly from trial to trial. On half the trials the monkeys observed the experimenter baiting the tube, whereas on the remaining trials their view of the baiting was blocked. On each trial, monkeys were allowed a single chance to select the tube containing the reward. During the choice period the monkeys had the opportunity to look down the length of each tube, to determine if it contained food. When they knew the location of the reward, most monkeys chose without looking. In contrast, when ignorant, monkeys often made the effort required to look, thereby learning the location of the reward before choosing. Looking improved accuracy on trials on which monkeys had not observed the baiting. The difference in looking behavior between trials on which the monkeys knew, and trials on which they were ignorant, suggests that rhesus monkeys discriminate between knowing and not knowing. This result extends similar observations made of children and apes to a species of Old World monkey, suggesting that the underlying cognitive capacities may be widely distributed among primates.     

Contrasting effects of lateral striate and superior colliculus lesions on visual discrimination performance in rhesus monkeys.

Rhesus monkeys with lesions of lateral striate cortex, monkeys with superior colliculus lesions, and unoperated monkeys were tested for retention of a preoperatively acquired pattern discrimination. The three groups of monkeys were then tested in two-choice, color, color discrimination tests, one involving varying degrees of stimulus-response (S-R) separation and the other, administered several months later, involving various directions of S-R separations. The monkeys were also tested in a series of two-choice pattern discriminations, following each of which they were tested for relearning when the patterns were masked with bars or circles. The monkeys with lateral striate lesions were moderately retarded in retention of the pattern discrimination, whereas those with superior colliculus lesions were not. The monkeys with colliculus lesions, but not those with lateral striate lesions, were impaired in both S-R separation tests, which demonstrates that their deficit was not transient or solely due to a difficulty in shifting the gaze in one direction. The lateral striate monkeys, unlike those with colliculus lesions, were dificient in relearning discriminations between masked patterns. These findings suggest that superior colliculus and striate cortex may be involved in two different aspects of attention: respectively, shifting attention (and orientation) from one spatial locus to another and maintaining attention on fixated stimuli. Alternative interpretations of the effects of the lesions, based on their retinotopic loci, are discussed.     

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.     

Responding maintained under fixed-interval and fixed-time schedules of electric shock presentation

Following initial histories under a schedule of electric shock postponement, lever pressing in squirrel monkeys was maintained under fixed-interval and fixed-time schedules of electric shock presentation. No difference in either rate or pattern of responding was obtained when these schedules were presented as components of a multiple schedule. When they were presented singly for long periods of time, the fixed-interval schedule consistently maintained a higher response rate than the fixed-time schedule. The pattern of responding under both schedules was similar, typically consisting of a pause at the beginning of each interval followed by either a steady or a positively accelerating rate of responding. The results suggest that the response-shock dependency is of critical importance in the maintenance of high rates of responding under schedules of electric shock presentation, and support the general view that such responding may be conceptualized as operant behavior under control of many of the same variables that control responding under comparable schedules of food or water reinforcement.     

Early maternal availability and prefrontal correlates of reward-related memory

Early emotional experiences affect developing brain systems that subsequently mediate adult learning and memory in rodents. Here we test for similar effects in squirrel monkeys (Saimiri sciureus) four years after disruptions in early maternal availability. These conditions were previously shown to generate differences in emotional behavior, hypothalamic-pituitary-adrenal stress physiology, and right ventral medial prefrontal volumes determined in adulthood by magnetic resonance imaging. This report identifies in the same monkeys variability in reward-related memory on tests with a spatial reversal. Adult monkeys that more often selected locations repeatedly rewarded before each reversal had larger right ventral medial prefrontal volumes, but not hippocampal nor dorsolateral prefrontal volumes on the left or right brain side. Differences in performance were also discerned after each spatial reversal. These findings indicate that maternal availability alters developing ventral medial prefrontal brain regions involved in reward-related memory.     

Multiple perceptual strategies used by macaque monkeys for face recognition

Successful integration of individuals in macaque societies suggests that monkeys use fast and efficient perceptual mechanisms to discriminate between conspecifics. Humans and great apes use primarily holistic and configural, but also feature-based, processing for face recognition. The relative contribution of these processes to face recognition in monkeys is not known. We measured face recognition in three monkeys performing a visual paired comparison task. Monkey and humans faces were (1) axially rotated, (2) inverted, (3) high-pass filtered, and (4) low-pass filtered to isolate different face processing strategies. The amount of time spent looking at the eyes, mouth, and other facial features was compared across monkey and human faces for each type of stimulus manipulation. For all monkeys, face recognition, expressed as novelty preference, was intact for monkey faces that were axially rotated or spatially filtered and was supported in general by preferential looking at the eyes, but was impaired for inverted faces in two of the three monkeys. Axially rotated, upright human faces with a full range of spatial frequencies were also recognized, however, the distribution of time spent exploring each facial feature was significantly different compared to monkey faces. No novelty preference, and hence no inferred recognition, was observed for inverted or low-pass filtered human faces. High-pass filtered human faces were recognized, however, the looking pattern on facial features deviated from the pattern observed for monkey faces. Taken together these results indicate large differences in recognition success and in perceptual strategies used by monkeys to recognize humans versus conspecifics. Monkeys use both second-order configural and feature-based processing to recognize the faces of conspecifics, but they use primarily feature-based strategies to recognize human faces.     

KNOWLEDGE OF THE ORDINAL POSITION OF LIST ITEMS IN RHESUS MONKEYS

Abstract —What is learned during mastery of a serial task: associations between adjacent and remote items, associations between an item and its ordinal position, or both? A dear answer to this question is lacking in the literature on human serial memory because it is difficult to control for a "naive" subject's linguistic competence and extensive experience with serial tasks. In this article, we present evidence that rhesus monkeys encode the ordinal positions of items of an arbitrary list when there is no requirement to do so. First, monkeys learned four nonverbal lists (1–4). each containing four novel items (photographs of natural objects). The monkeys then learned four 4-item lists that were derived exclusively and exhaustively from Lists 1 through 4, one item from each list. On two derived lists, each item s original ordinal position was maintained. Those lists were acquired with virtually no errors. The two remaining derived lists, on which the original ordinal position of each item was changed, were as difficult to learn as novel lists. The immediate acquisition of lists on which ordinal position was maintained shows that knowledge of ordinal position can develop without the benefit of language, extensive list-learning experience, or explicit instruction to encode ordinal information.     

Pictorial similarity judgments and the organization of visual memory in the rhesus monkey

The organization of visual memory for pictures was studied in the rhesus monkey. Two monkeys were tested in a same/different task in which sequentially presented pictures were compared to each other in a pair-wise fashion. The resulting confusion matrixes were analyzed using a multidimensional scaling procedure to obtain two- and three-dimensional graphic representations of the stimulus space. In Experiment 1, the monkeys' confusion errors caused pictures of human and rhesus monkey faces to fall in the same region of multidimensional space, which suggested that the monkeys categorized facial stimuli. A similar effect was found for pictures of different types of fruit. Experiment 2 replicated the categorization of faces with a more diverse collection of human and nonhuman primate faces. Experiment 3 explored the fruit category by varying stimulus attributes orthogonally. The results from this experiment showed that both monkeys encoded the pictures in this category by type of fruit (apples or grapes) and color (red or yellow). Taken together, these studies indicate that rhesus monkeys will treat some classes of pictorial stimuli categorically in visual memory.     

Probability-reward preferences of rhesus monkeys

The relative preferences of rhesus monkeys for reward probability versus amount were investigated with procedures which contrasted general experience with specific instructions, and evaluated the relationship between probability-amount combinations and preference strength. Four stimulus objects, each signifying a different combination of reward frequency and amount (100% with one unit; 50% with two units; 33% with three units; or 25% with four units), were presented in pairs, one pair per daily session, with trial schedules providing the same amount of reward within each set of 12 trials. In Phase A, 4 monkeys (Group 1) were tested on the six choice-pairs with no preliminary training. In Phase B, Group 1 was joined by an additional 4 monkeys (Group 2), and each of the tasks was preceded by a demonstration of the relevant stimuli, one at a time, together with their associated probabilities and amounts. Group 1 animals developed preferences during Phase A for the more frequently rewarded objects, which persisted into Phase B, whereas Group 2 animals showed no preferences. This result indicates that preliminary instructions concerning the reward combinations associated with stimulus objects can prevent the development of a preference for greater probability over greater amount of reward, but cannot extinguish it once it has been formed or reestablished within the context of a particular task.     

Concurrent access to two concentrations of orally delivered phencyclidine: effects of feeding conditions.

Two experiments addressed the effects of food satiation and deprivation on oral self-administration of two concurrently available phencyclidine concentrations. In the first experiment, 8 rhesus monkeys self-administered either of two concentrations of phencyclidine ("PCP, angel dust") and water under concurrent fixed-ratio 16 schedules. One concentration was always held constant (0.25 mg/mL) while a series of other phencyclidine concentrations, ranging from 0 (water) to 1.0 mg/mL, was presented in a nonsystematic order. Initially the monkeys were tested while food satiated, and the procedure was then repeated during food deprivation. The monkeys usually selected the higher concentration within the first few minutes of the session, indicating that taste and/or other immediate postingestional effects were important factors. Contrary to a number of previous reports, there were no consistent differences across subjects in the mean number of liquid deliveries or mean drug intake (mg/kg) during food satiation and deprivation. However, for all monkeys the within-session time course of responding during food satiation consistently differed from that during deprivation. A second experiment assessed whether the failure to find consistent differences in drug intake during food satiation and deprivation had been due to the history of concurrent access to different phencyclidine concentrations or to the extended experience with phencyclidine under food-satiation conditions. Six additional monkeys (Group 2) were exposed to the phencyclidine self-administration procedure (during food satiation and deprivation) for the same length of time as the monkeys in Experiment 1 (Group 1), except they received only concurrent access to phencyclidine (0.25 mg/mL) and water. Both groups then received concurrent access to phencyclidine and water during five repeated cycles of food deprivation and satiation. There were also marked individual differences in Group 2: During food satiation, 2 of the monkeys' responding increased, 1 showed no change, and 3 decreased. Examination of a number of historical variables indicated that the greater the percentage of total sessions spent during food satiation with phencyclidine available (before these experiments began), the greater the amounts of phencyclidine consumed during food satiation and the smaller the differences in phencyclidine intake when the two feeding conditions were compared.     

Learning from others’ mistakes in capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>)

We investigated whether tufted capuchin monkeys (Cebus apella) learn from others' mistakes. We prepared three kinds of transparent containers having the same appearance: one that could be opened by the lid, one that could be opened from the bottom, and one that could be opened either way. Using each of the first two one-way-open type containers, the monkeys were trained to copy the human demonstrator's action to open the container and obtain a piece of sweet potato contained therein. After this training, the demonstrator showed the monkeys an action that would open or fail to open the third, two-way-open type container. None of the monkeys reliably opened the container by spontaneously compensating for the demonstrator's failure (Experiment 1). In Experiment 2, the same subjects were trained to correct their own mistakes immediately after failure, before we introduced the same test as in Experiment 1. This experience did not result in subjects using the demonstrator's failure to produce a successful action. In Experiment 3, we placed two monkeys face to face. In this situation, the second monkey was presented with the container after the first monkey failed to open it. As a result, two capuchin monkeys capitalized on the partner's failure to correctly guide his/her behavior. Thus, the monkeys monitored not only the outcome of the others' action, but also that action per se. This result suggests that not only humans and apes, but also monkeys may understand the meaning of others' actions in social learning.