Cardiac startle and orienting responses in the great apes.

Cardiac patterns of startle and orienting in response to auditory and vibrotactile stimuli were investigated in the infant chimpanzee and gorilla. Results revealed a notable cardiac acceleration in response to the initial presentations of stimuli of either modality. This acceleratory response appeared to reflect the cardiac correlate of startle and was closely associated with the elicitation of somatic startle responses. This initial cardiac acceleration was subject to rapid habituation and was replaced on subsequent trials by cardiac deceleration, which appeared to reflect the orienting response. Results from the chimpanzees and the gorilla were similar, although a slower rate of habituation was apparent in the gorilla. Taken together, these results are highly consistent with those obtained from humans and monkeys, and they provide the first characterization of cardiac patterns associated with startle and orienting responses in the great apes.

Specificity of the cardiac response to conspecific vocalization in chimpanzees.

Heart rate measures were used to examine the functional response of young chimpanzees and orangutans to acoustic stimuli, including white noise and chimpanzee vocalizations (threat, stress, and alarm). The initial response of the animals to all stimuli was characterized by a prominent cardiac deceleration and an increase in heart period variability. The deceleratory responses persisted with repeated presentations of the noise, stress, and alarm stimuli. In contrast, the response of chimpanzees to the conspecific threat stimulus reverted over trials to a notable cardiac acceleration. This acceleratory response was not attributable to potential patterns of evoked somatic responses. The features of the cardiac response, together with the results of frequency-domain analyses of heart period variability, suggest that this acceleratory response was consistent with the evocation of an aversive or a defensive reaction characterized by sympathetic activation. This pattern of cardiac response appeared early in ontogeny (within 48 hr postnatally) and was not manifest in orangutans. Taken together, the results suggest the existence of specialized perceptual processing mechanisms for vocal stimuli in the chimpanzee. Further examination of these mechanisms may contribute to our understanding of central perceptual processes and the evolution of vocal communication.

Neurobehavioral organization and the cardinal principle of evaluative bivalence.

The principle of evaluative bivalence asserts that behavioral processes often organize along the evaluative dimension, due to a fundamental pattern of bivalent neurobehavioral organization extending throughout the neuraxis. This principle offers a powerful approach to the explication of complex behavioral relationships and the integration of diverse literatures. It also offers a guiding conceptual framework for the study of neurobehavioral relationships which holds the promise of integrating rather than diversifying the study of neural mechanisms for disparate behavioral phenomena.

Responses to quantity: perceptual versus cognitive mechanisms in chimpanzees (Pan troglodytes).

Two chimpanzees were trained to select among 2 different amounts of candy (1-6 items). The task was designed so that selection of either array by the active (selector) chimpanzee resulted in that array being given to the passive (observer) animal, with the remaining (nonselected) array going to the selector. Neither animal was able to select consistently the smaller array, which would reap the larger reward. Rather, both animals preferentially selected the larger array, thereby receiving the smaller number of reinforcers. When Arabic numerals were substituted for the food arrays, however, the selector animal evidenced more optimal performance, immediately selecting the smaller numeral and thus receiving the larger reward. These findings suggest that a basic predisposition to respond to the perceptual-motivational features of incentive stimuli can interfere with task performance and that this interference can be overridden when abstract symbols serve as choice stimuli.

Language-naive chimpanzees (Pan troglodytes) judge relations between relations in a conceptual matching-to-sample task.

Three chimpanzees with a history of conditional and numeric token training spontaneously matched relations between relations under conditions of nondifferential reinforcement. Heretofore, this conceptual ability was demonstrated only in language-trained chimpanzees. The performance levels of the language-naive animals in this study, however, were equivalent to those of a 4th animal--Sarah--whose history included language training and analogical problem solving. There was no evidence that associative factors mediated successful performance in any of the animals. Prior claims of a profound disparity between language-trained and language-naive chimpanzees apparently can be attributed to prior experience with arbitrary tokens consistently associated with abstract relations and not language per se.

Quantity-based interference and symbolic representations in chimpanzees (Pan troglodytes).

Five chimpanzees with training in counting and numerical skills selected between 2 arrays of different amounts of candy or 2 Arabic numerals. A reversed reinforcement contingency was in effect, in which the selected array was removed and the subject received the nonselected candies (or the number of candies represented by the nonselected Arabic numeral). Animals were unable to maximize reward by selecting the smaller array when candies were used as array elements. When Arabic numerals were substituted for the candy arrays, all animals showed an immediate shift to a more optimal response strategy of selecting the smaller numeral, thereby receiving the larger reward. Results suggest that a response disposition to the high-incentive candy stimuli introduced a powerful interference effect on performance, which was effectively overridden by the use of symbolic representations.

Numerical competence in a chimpanzee (Pan troglodytes).

A chimpanzee (Pan troglodytes), trained to count foods and objects by using Arabic numbers, demonstrated the ability to sum arrays of 0-4 food items placed in 2 of 3 possible sites. To address representational use of numbers, we next baited sites with Arabic numbers as stimuli. In both cases performance was significantly above chance from the first sessions, which suggests that without explicit training in combining arrays, the animal was able to select the correct arithmetic sum for arrays of foods or Arabic numbers under novel test conditions. These findings demonstrate that counting strategies and the representational use of numbers lie within the cognitive domain of the chimpanzee and compare favorably with the spontaneous use of addition algorithms demonstrated in preschool children.

Cardiac correlates of individual recognition in the chimpanzee (Pan troglodytes).

The ability of a chimpanzee to recognize individuals depicted in photographs was evaluated through the use of heart rate measures. Heart rate was recorded before and during photographic projections of human caregivers, familiar individuals, strangers, and blank control slides. In the absence of explicit training or reinforcement, the chimpanzee displayed a differential pattern of heart rate response to the stimulus categories. Although heart rate responses to all stimuli were predominantly deceleratory, the photographs of caregivers yielded consistently larger responses than other stimuli. Results indicate that the chimpanzee is able to recognize individual humans from novel photographic representations and that heart rate can provide an objective measure of such recognition.

Spontaneous discrimination of natural stimuli by chimpanzees (Pan troglodytes).

Six chimpanzees (Pan troglodytes) were presented with pairs of color photographic images of 5 different categories of animals (cat, chimp, gorilla, tiger, fish). The subjects responded to each pair using symbols for "same" and "different." Both within- and between-category discriminations were tested, and all chimpanzees classified the image pairs in accordance with the 5 experimenter-defined categories under conditions of nondifferential reinforcement. Although previous studies have demonstrated identification or discrimination of natural categories by nonhuman animals, subjects were typically differentially reinforced for their responses. The present findings demonstrate that chimpanzees can classify natural objects spontaneously and that such classifications may be similar to those that would be observed in human subjects.

The effect of response contingencies on scale model task performance by chimpanzees (Pan troglodytes).

The effects of modified procedures on chimpanzees' (Pan troglodytes) performance in a scale model comprehension task were examined. Seven chimpanzees that previously participated in a task in which they searched an enclosure for a hidden item after watching an experimenter hide a miniature item in the analogous location in a scale model were retested under procedures incorporating response costs. In Experiment 1, chimpanzees were trained under procedures that rewarded only item retrievals occurring on the 1st search attempt. During test trials, 6 chimpanzees performed above chance, including 4 that were previously unsuccessful under the original procedures (V. A. Kuhlmeier, S. T. Boysen, & K. L. Mukobi, 1999). Experiment 2 compared performance under the new and original procedures. Results indicated that for some chimpanzees, performance depended on procedures that decreased the use of competing search strategies and encouraged strategies based on information from the scale model.

Conspecific recognition in the chimpanzee (Pan troglodytes): cardiac responses to significant others.

The ability of a chimpanzee (Pan troglodytes) to recognize photographs of conspecifics was evaluated with heart-rate measures. Heart rate was recorded before, during, and after viewing photographs of an aggressive chimpanzee, a friendly companion animal, and an unfamiliar chimpanzee. The subject displayed a differential pattern of heart-rate response to the stimulus animals, without prior experience with the photographs. Responses to the aggressive animal were acceleratory, which suggests a defensive response. Respiratory sinus arrhythmia suggested that this response was associated with sympathetic activation. In contrast, responses to the familiar animal were minimal, whereas cardiac deceleration was observed in response to the strange chimp, which likely reflects an orienting response. Results suggest the chimpanzee is able to recognize photographs of individual conspecifics and that heart-rate change can reflect the nature of established social relationships between chimpanzees.

Simian scribbles: a reappraisal of drawing in the chimpanzee (Pan troglodytes).

Three chimpanzees (Pan troglodytes) were provided with 18 different stimulus pages for drawing. The resulting 618 drawings were coded for drawn marks, and results were compared with early reports on ape drawing (Morris, 1962; Schiller, 1951) and with more recent systematic studies (Smith, 1973). The findings of the present study confirm Smith's observations of a tendency for the animals to draw closer to the center and toward the bottom of the page. No evidence for perceptual balancing was observed in drawings produced on pages with lateral figures, nor was any evidence for closure apparent with complex figures. The present results agree with earlier findings that chimpanzees will engage in drawing activities without training or reinforcement, and this behavior may reflect their intrinsic interest in exploratory and manipulative play.

Comprehension of cause-effect relations in a tool-using task by chimpanzees (Pan troglodytes).

Five chimpanzees (Pan troglodytes) were tested to assess their understanding of causality in a tool task. The task consisted of a transparent tube with a trap-hole drilled in its middle. A reward was randomly placed on either side of the hole. Depending on which side the chimpanzee inserted the stick into, the candy was either pushed out of the tube or into the trap. In Experiment 1, the success rate of 2 chimpanzees rose highly above chance, but that of the other subjects did not. Results show that the 2 successful chimpanzees selected the correct side for insertion beforehand. Experiment 2 ruled out the possibility that their success was due to a distance-based associative rule, and the results favor an alternative hypothesis that relates success to an understanding of the causal relation between the tool-using action and its outcome.

Inferences about guessing and knowing by chimpanzees (Pan troglodytes).

The visual perspective-taking ability of 4 chimpanzees (Pan troglodytes) was investigated. The subjects chose between information about the location of hidden food provided by 2 experimenters who randomly alternated between two roles (the guesser and the knower). The knower baited 1 of 4 obscured cups so that the subjects could watch the process but could not see which of the cups contained the reward. The guesser waited outside the room until the food was hidden. Finally, the knower pointed to the correct cup while the guesser pointed to an incorrect one. The chimpanzees quickly learned to respond to the knower. They also showed transfer to a novel variation of the task, in which the guesser remained inside the room and covered his head while the knower stood next to him and watched a third experimenter bait the cups. The results are consistent with the hypothesis that chimpanzees are capable of modeling the visual perspectives of others.

Size matters: impact of item size and quantity on array choice by chimpanzees (Pan troglodytes).

The authors previously reported that chimpanzees (Pan troglodytes) showed a striking bias to select the larger of 2 candy arrays, despite a reversed reward contingency in which the animals received the smaller, nonselected array as a reward, except when Arabic numerals were used as stimuli. A perceptual or incentive-based interference occurred that was overcome by symbolic stimuli. The authors of the present study examined the impact of element size in choice arrays, using 1 to 5 large and small candies. Five test-sophisticated chimpanzees selected an array from the 2 presented during each trial. Their responses were not optimal, as animals generally selected arrays with larger total mass; thus, they received the smaller remaining array as a reward. When choice stimuli differed in size and quantity, element size was more heavily weighted, although choices reflected total candy mass. These results replicate previous findings showing chimpanzees' difficulties with quantity judgments under reverse reward contingencies and also show that individual item size exerts a more powerful interference effect.

Scale-model comprehension by chimpanzees (Pan troglodytes).

The ability of chimpanzees (Pan troglodytes) to recognize the correspondence between a scale model and its real-world referent was examined. In Experiments 1 and 2, an adult female and a young adult male watched as an experimenter hid a miniature model food in 1 of 4 sites in a scale model. Then, the chimpanzees were given the opportunity to find the real food item that had been hidden in the analogous location in the real room. The female performed significantly above chance, whereas the male performed at chance level. Experiments 3 and 4 tested 5 adult and 2 adolescent chimpanzees in a similar paradigm, using a scale model of the chimpanzees' outdoor area. Results indicate that some adult chimpanzees were able to reliably demonstrate an understanding of the relationship between a scale model and the larger space it represented, whereas other subjects were constrained by inefficient and unsuccessful search patterns.

Processing of ordinality and transitivity by chimpanzees (Pan troglodytes).

Three chimpanzees (Pan troglodytes) were trained to discriminate among pairs of boxes in an ABCDE-ordered series. The 2nd member of each pair was reinforced, until all 4 training pairs were learned. During novel tests the nonadjacent BD pair was presented, and all 3 animals reliably selected D. In Experiment 2, numerals 1-5 served as stimuli. One chimpanzee reliably selected the larger numeral 4 during testing with a nonadjacent pair (2-4), and 2 chimps showed no preference. In a 2nd phase, the same chimp demonstrated proficiency at reversing the task, reliably selecting the smaller of the 2-4 pair. In Experiment 4, after additional training, a 2nd test, which included novel test pairs composed of numbers that had not been used during training, was completed. Two of 3 animals were 100% correct on Trial 1 for all novel pairs. The results suggest that chimpanzees with experience in number concepts may recognize the ordinal character of numbers.

Indicating acts during counting by a chimpanzee (Pan troglodytes).

A chimpanzee (Pan troglodytes) experienced in counting arrays of 0-7 items and trained for comprehension of number symbols, spontaneously displayed a variety of indicating acts (e.g., pointing, touching, and rearranging items) during counting. Twenty-five sessions were videotaped, and all trials were evaluated for the relations among number of items presented, number of indicating acts displayed, and the Arabic number selected to represent the array. Significant correlations included the relations between number of items and the cardinal number selected by the animal, between the number of items and indicating acts displayed by the chimpanzee, and between the number of indicating acts and the numeral selected. These data suggest that the use of indicating acts by this animal may have functional significance and serves as an organizing schema, comparable to similar behaviors observed in children in the early stages of learning to count.

Raking it in: the impact of enculturation on chimpanzee tool use.

Recent evidence for different tool kits, proposed to be based upon culture-like transmission, have been observed across different chimpanzee communities across Western Africa. In light of these findings, the reported failures by seven captive juvenile chimpanzees tested with 27 tool use tasks (Povinelli 2000) seem enigmatic. Here we report successful performance by a group of nine captive, enculturated chimpanzees, and limited success by a group of six semi-enculturated chimpanzees, on two of the Povinelli tasks, the Flimsy Tool task, and the Hybrid Tool task. All chimpanzees were presented with a rake with a flimsy head and a second rake with a rigid head, either of which could be used to attempt to retrieve a food reward that was out of reach. The rigid rake was constructed such that it had the necessary functional features to permit successful retrieval, while the flimsy rake did not. Both chimpanzee groups in the present experiment selected the functional rigid tool correctly to use during the Flimsy Tool task. All animals were then presented with two "hybrid rakes" A and B, with one half of each rake head constructed from flimsy, non-functional fabric, and the other half of the head was made of wood. Food rewards were placed in front of the rigid side of Rake A and the flimsy side of Rake B. To be successful, the chimps needed to choose the rake that had the reward in front of the rigid side of the rake head. The fully enculturated animals were successful in selecting the functional rake, while the semi-enculturated subjects chose randomly between the two hybrid tools. Compared with findings from Povinelli, whose non-enculturated animals failed both tasks, our results demonstrate that chimpanzees reared under conditions of semi-enculturation could learn to discriminate correctly the necessary tool through trial-and-error during the Flimsy Tool task, but were unable to recognize the functional relationship necessary for retrieving the reward with the "hybrid" rake. In contrast, the enculturated chimpanzees were correct in their choices during both the Flimsy Tool and the Hybrid Tool tasks. These results provide the first empirical evidence for the differential effects of enculturation on subsequent tool use capacities in captive chimpanzees.

Visual evoked potentials in the great apes.

Visual evoked potentials (VEPs) in response to flash stimuli were recorded from occipital and central-scalp electrodes in the chimpanzee and gorilla. The most notable occipital component of the VEP was a surface-positive wave (P90), the latency of which decreased with development. Central scalp responses, apparent only in older animals, included a characteristic long-latency 'vertex wave' (N125-P225). Observed responses are similar to those reported for humans and monkeys, but appear to share more specific features of human VEPs.