Are monkeys aesthetists? Rensch (1957) revisited

Three experiments assessed whether capuchin monkeys (Cebus apella) and squirrel monkeys (Saimiri sciureus) prefer regular and symmetrical visual patterns. Pictorial representations of faces were included in 1 stimulus set. When the monkeys could pick up and manipulate small cards bearing the stimuli, all preferences expressed by capuchins and most of those expressed by squirrel monkeys were for regular stimuli. Symmetry of the patterns was influential but not essential. Some preferences were also found for faces. When images of the patterns were presented on a touch screen, capuchins continued to express preferences especially for regular and symmetrical stimuli, but they showed some avoidance of faces. Squirrel monkeys responded less discriminatingly to the touch screen stimuli. The findings provide support for B. Rensch's (1957) claim that monkeys prefer visual stimuli that humans find aesthetically pleasing.     

Reverse-reward learning in squirrel monkeys (Saimiri sciureus): retesting after 5 years, and assessment on qualitative transfer

Seven squirrel monkeys (Saimiri sciureus) previously trained on reverse-reward tasks were presented with the original "1-versus-4" task after a 5-year interval without reverse-reward experience (Experiment 1). None of them reliably selected the smaller food array; however, at around chance level, their performance was superior to when they were first exposed to the task almost 6 years previously, suggesting some long-term memory retention. One naive monkey consistently selected the larger array, as expected. In Experiment 2, trials consisting of 1 versus 1 piece of two qualitatively different types of food were interspersed among familiar 1-versus-4 trials. None of five monkeys tested reliably selected the less-preferred food to get the more preferred food as the reward, and one monkey scored below chance. However, when one piece of low-preference food was paired with four pieces of high-preference food (Experiment 3), all four monkeys tested avoided reaching for the latter and thereby obtained it as the reward; two monkeys obtained perfect scores on these trials. These two monkeys were trained on a specific qualitative reverse-reward pairing and then again tested on new pairings (Experiment 4), but transfer was incomplete. Compound trials that pit quantity against quality in novel ways appear taxing for squirrel monkeys, despite competence in reverse-reward on both dimensions separately.     

Evaluation of third-party reciprocity by squirrel monkeys (<Emphasis Type="Italic">Saimiri sciureus</Emphasis>) and the question of mechanisms

Social evaluation during third-party interactions emerges early in human ontogeny, and it has been shown in adult capuchin monkeys who witness violations of reciprocity in object exchanges: Monkeys were less inclined to accept food from humans who refused to reciprocate with another human. A recent study reporting similar evidence in marmoset monkeys raised the possibility that such evaluations might be based on species’ inherent cooperativeness. We tested a species not renowned for cooperativeness—squirrel monkeys—using the procedure used with marmosets and found a similar result. This finding rules out any crucial role for cooperative tendencies in monkeys’ responses to unfair exchanges. We then tested squirrel monkeys using procedures more similar to those used in the original study with capuchins. Squirrel monkeys again accepted food less frequently from non-reciprocators, but unlike capuchins, they also strongly preferred reciprocators. We conclude that neither squirrel monkeys nor marmoset monkeys engaged in emotional bookkeeping of the type that probably underlies social evaluation in capuchin monkeys; instead, they employed one or more simple behavioral rules. Further comparative studies are required to clarify the mechanisms underlying social evaluation processes across species.     

Gaze alternation during “pointing” by squirrel monkeys (<Emphasis Type="Italic">Saimiri sciureus</Emphasis>)?

Gaze alternation (GA) is considered a hallmark of pointing in human infants, a sign of intentionality underlying the gesture. GA has occasionally been observed in great apes, and reported only anecdotally in a few monkeys. Three squirrel monkeys that had previously learned to reach toward out-of-reach food in the presence of a human partner were videotaped while the latter visually attended to the food, a distractor object, or the ceiling. Frame-by-frame video analysis revealed that, especially when reaching toward the food, the monkeys rapidly and repeatedly switched between looking at the partner’s face and the food. This type of GA suggests that the monkeys were communicating with the partner. However, the monkeys’ behavior was not influenced by changes in the partner’s focus of attention.     

Maternal separation alters later consumption of novel liquids in the squirrel monkey

The consumption of novel, fruit-flavored drinks was measured in juvenile squirrel monkeys that had either had their mother removed from the home cage for 2 h on 80 occasions prior to weaning or had not undergone this separation procedure. Among previously separated animals, males drank more than did females during the first 30 min following presentation, whereas there was no difference in the drinking of nonseparated males and females at this time. Further, the amount of liquid consumed during the 20 h following presentation increased across days of exposure in the nonseparated, but not in the previously separated monkeys. These results show that brief maternal separation can affect the later behavior of squirrel monkeys, and are consistent with findings in rhesus macaques that maternal separation alters later exploratory behavior.     

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.     

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.     

The Thatcher illusion in squirrel monkeys (Saimiri sciureus)

Like humans, Old World monkeys are known to use configural face processing to distinguish among individuals. The ability to recognize an individual through the perception of subtle differences in the configuration of facial features plays an important role in social cognition. To test this ability in New World monkeys, this study examined whether squirrel monkeys experience the Thatcher illusion, a measure of face processing ability in which changes in facial features are difficult to detect in an inverted face. In the experiment, the monkeys were required to distinguish between a target face and each of the three kinds of distracter faces whose features were altered to be different from those of the target. For each of the pairs of target and distracter faces, four rotation-based combinations of upright and inverted face presentations were used. The results revealed that when both faces were inverted and the eyes of the distracter face were altered by rotating them at an angle of 180° from those of the target face, the monkeys' discrimination learning was obstructed to a greater extent than it was under the other conditions. Thus, these results suggest that the squirrel monkey does experience the Thatcher illusion. Furthermore, it seems reasonable to assume that squirrel monkeys can utilize information about facial configurations in individual recognition and that this facial configuration information could be useful in their social communications.     

Autoshaping and automaintenance of a key-press response in squirrel monkeys

Following exposure for a minimum of 500 to 600 trials, three of four naive squirrel monkeys eventually pressed a response key, illumination of which always preceded delivery of a food pellet. Three other naive monkeys did not press the key when the pellets were delivered randomly with respect to key illumination. Despite some similarities to autoshaping using pigeons, the data indicate many points of difference when squirrel monkeys are used as subjects. Although key-food pairings were shown to be important in the acquisition of the key-press response, they were ineffective in maintaining the response when either a negative response-reinforcer dependency was introduced, or when there was no scheduled response-reinforcer dependency (fixed trial). Not all demonstrations of autoshaping can be considered to be under the control of those processes that are primarily responsible for the phenomena obtained in pigeons.     

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.     

Interactions in multiple schedules: negative induction with squirrel monkeys

In Experiment I, lever pressing by squirrel monkeys was maintained under a sequence of variable-interval, multiple variable-interval variable-interval, and multiple variable-interval extinction schedules of food presentation. Negative induction (decreased responding in the unchanged component) occurred when one component of the multiple variable-interval variable-interval schedule was changed to extinction. Negative induction was transient over sessions; responding in the unchanged component usually recovered to a rate similar to that under the multiple variable-interval variable-interval schedule. Negative induction was not accompanied by consistent changes in the patterns of local responding within the unchanged component, and did not depend on whether component schedules were associated with localized (lever lights) or diffuse visual stimuli (houselights), or on whether the unchanged component was a 60- or 180-sec variable-interval schedule. In Experiment II, responding was maintained under a sequence of variable-interval and multiple variable-interval timeout schedules of food presentation. Negative induction occurred when responding declined gradually in the timeout component but not when responding declined abruptly. The nature of interactions in multiple schedules may depend on the species; negative induction was observed with squirrel monkeys under conditions similar to those that produce positive contrast with pigeons.     

Levels of stimulus processing by the squirrel monkey: relative and absolute judgements compared.

Nine squirrel monkeys were required to select from various sets of stimuli-differing in size or brightness-either in terms of relational criteria or on an absolute stimulus basis. The level of information processing required by each task was assessed by means of stimulus transformation techniques, variations in set size, and by the elimination of the visible context. It was found that some relational judgements make fewer processing demands on the subject than do absolute stimulus judgements; the 'middle' relation, however, appears much more difficult to use than selection of a stimulus on an absolute basis and may be beyond the competence of the squirrel monkey. The results are seen as support for the thesis as advanced by McGonigle and Jones that the criteria of judgement, when varied, change the depth of stimulus processing by monkey as well as man.     

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.     

Can squirrel monkeys (Saimiri sciureus) learn self-control? A study using food array selection tests and reverse-reward contingency

Eight squirrel monkeys (Saimiri sciureus) were presented with 2 stimulus arrays, namely 1 and 4 pieces of food, but they received only the array other than the one they reached for. In this reverse-reward condition, all monkeys initially showed a strong preference for the larger array. One monkey learned to reach toward the smaller array when a large-or-none reward contingency was applied (i.e., no reward followed a reach toward the larger array, but this array was given for a reach toward the smaller array). When correction trials and time-out were added to the large-or-none procedure, all remaining monkeys except 1 learned this form of self-control. Performance was maintained when correction trials were discontinued, the original reverse-reward condition was rerun, and novel array-size pairs were presented. This study demonstrates one form of self-control in a New World primate and shows the reverse-reward procedure to be a potentially valuable method for assessing species and individual differences in self-control and numerosity-related abilities.     

Training squirrel monkeys (Saimiri sciureus) to deceive: acquisition and analysis of behavior toward cooperative and competitive trainers

Three squirrel monkeys (Saimiri sciureus) learned to reach toward a container that covered food if a cooperative trainer rewarded such reaches by giving the food. A competitive trainer kept any food found, but wrong selections by this trainer were also rewarded. The monkeys initially reached toward the baited container indiscriminately, but gradually and with the aid of color-cued containers, all 3 reliably reached "honestly" and "deceptively" in the presence of the cooperative and competitive trainers, respectively. The monkeys did not appear to take the trainers' knowledge about the location of the food into account, and deception did not occur if food was placed under the normally unbaited container. With additional containers present, monkeys misled the competitive trainer into selecting the unbaited container farthest from the baited one. Although not indicative of mental attribution, the monkeys' behavior suggests awareness of the acquired communicative function of the reaching response.     

Detection of directed gaze in rhesus monkeys (Macaca mulatta).

To examine the ability of monkeys to detect the direction of attention of other individuals, the authors quantitatively investigated the visual scanning pattern of rhesus monkeys (Macaca mulatta) in response to visually presented images of a human frontal face. The present results demonstrated not only that monkeys predominantly gaze at the eyes as compared with other facial areas in terms of duration and number of fixations, but also that they gaze at the eyes for a longer time period and more frequently when a human face, presented as a stimulus, gazed at them than when the gaze was shifted. These results indicate that rhesus monkeys are sensitive to the directed gaze of humans, suggesting that monkeys pay more attention to the human whose attention is directed to them.     

Pain-aggression toward inanimate objects

Attack behavior was elicited from squirrel monkeys by externally applied electric shock. The shock elicited attack toward other monkeys, rats, and mice, as well as toward inanimate objects, such as a stuffed doll, and even a round ball. A method of quantifying the attack behavior was devised on the basis of the attack against inanimate objects. This method revealed that the duration and probability of attack was a direct function of the shock intensity.     

Food Avoidance Learning in Squirrel Monkeys and Common Marmosets

Using a conditioned food avoidance learning paradigm, six squirrel monkeys (Saimiri sciureus) and six common marmosets (Callithrix jacchus) were tested for their ability to (1) reliably form associations between visual or olfactory cues of a potential food and its palatability and (2) remember such associations over prolonged periods of time. We found (1) that at the group level both species showed one-trial learning with the visual cues color and shape, whereas only the marmosets were able to do so with the olfactory cue, (2) that all individuals from both species learned to reliably avoid the unpalatable food items within 10 trials, (3) a tendency in both species for quicker acquisition of the association with the visual cues compared with the olfactory cue, (4) a tendency for quicker acquisition and higher reliability of the aversion by the marmosets compared with the squirrel monkeys, and (5) that all individuals from both species were able to reliably remember the significance of the visual cues, color and shape, even after 4 months, whereas only the marmosets showed retention of the significance of the olfactory cues for up to 4 weeks. Furthermore, the results suggest that in both species tested, illness is not a necessary prerequisite for food avoidance learning but that the presumably innate rejection responses toward highly concentrated but nontoxic bitter and sour tastants are sufficient to induce robust learning and retention.     

A comparative analysis of global and local processing of hierarchical visual stimuli in young children (Homo sapiens) and monkeys (Cebus apella)

Results obtained with preschool children (Homo sapiens) were compared with results previously obtained from capuchin monkeys (Cebus apella) in matching-to-sample tasks featuring hierarchical visual stimuli. In Experiment 1, monkeys, in contrast with children, showed an advantage in matching the stimuli on the basis of their local features. These results were replicated in a 2nd experiment in which control trials enabled the authors to rule out that children used spurious cues to solve the matching task. In a 3rd experiment featuring conditions in which the density of the stimuli was manipulated, monkeys' accuracy in the processing of the global shape of the stimuli was negatively affected by the separation of the local elements, whereas children's performance was robust across testing conditions. Children's response latencies revealed a global precedence in the 2nd and 3rd experiments. These results show differences in the processing of hierarchical stimuli by humans and monkeys that emerge early during childhood.     

SOME RELATIONS BETWEEN CLASSICALLY CONDITIONED AGGRESSION AND CONDITIONED SUPPRESSION IN SQUIRREL MONKEYS

During three experiments with squirrel monkeys, stimulus and shock pairings were given in the presence of a bite tube. Experiments 1 and 2 used a conditioned-suppression procedure in which bar pressing was reinforced with food. A transparent shield prevented biting of the bar. When the stimulus was paired with shock, bar pressing decreased (conditioned suppression) and tube biting increased during the stimulus (classically conditioned aggression). When the bite tube was removed on alternate sessions in Experiment 2, there was more suppression when the tube was present, thus suggesting that biting competed with bar pressing. However, this simple competing-response interpretation was complicated by the findings of Experiment 3 where, with naive monkeys, bar pressing was never reinforced with food, yet bar pressing was induced during the stimulus and was highest when the bite tube was absent. The fact that stimulus-induced bar pressing developed indicates that bar pressing in conditioned-suppression procedures, suppressed or not, may be maintained by two types of control—the food reinforcer and induced CS control. The higher rate of induced bar pressing during the stimulus with the bite tube absent confounds a simple competing response interpretation of conditioned suppression. It suggests that shock-induced responses during conditioned suppression could be both contributing to and competing with responding maintained by food, with the net effect depending on specific but ill-defined features of the situation.