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Parr, L. A. (2001). Cognitive and physiological markers of emotional awareness in chimpanzees (Pan troglodytes). Anim. Cogn., 4(3), 223–229.
Abstract: The ability to understand emotion in others is one of the most important factors involved in regulating social interactions in primates. Such emotional awareness functions to coordinate activity among group members, enable the formation of long-lasting individual relationships, and facilitate the pursuit of shared interests. Despite these important evolutionary implications, comparative studies of emotional processing in humans and great apes are practically nonexistent, constituting a major gap in our understanding of the extent to which emotional awareness has played an important role in shaping human behavior and societies. This paper presents the results of two experiments that examine chimpanzees' responses to emotional stimuli. First, changes in peripheral skin temperature were measured while subjects viewed three categories of emotionally negative video scenes; conspecifics being injected with needles (INJ), darts and needles alone (DART), and conspecific directing agonism towards the veterinarians (CHASE). Second, chimpanzees were required to use facial expressions to categorize emotional video scenes, i.e., favorite food and objects and veterinarian procedures, according to their positive and negative valence. With no prior training, subjects spontaneously matched the emotional videos to conspecific facial expressions according to their shared emotional meaning, indicating that chimpanzee facial expressions are processed emotionally, as are human expressions. Decreases in peripheral skin temperature, indicative of negative sympathetic arousal, were significantly lower when subjects viewed the INJ and DART videos, compared to the CHASE videos, indicating greater negative arousal when viewing conspecifics being injected with needles, and needles themselves, than when viewing conspecifics engaged in general agonism.
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Parr, L. A., Winslow, J. T., & Hopkins, W. D. (1999). Is the inversion effect in rhesus monkeys face-specific? Anim. Cogn., 2(3), 123–129.
Abstract: 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.
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Parr, L. A., Matheson, M. D., Bernstein, I. S., & De Waal, F. B. M. (1997). Grooming down the hierarchy: allogrooming in captive brown capuchin monkeys, Cebus apella. Anim. Behav., 54(2), 361–367.
Abstract: Observations of captive female brown capuchin monkeys in five groups revealed that grooming is primarily the occupation of dominant females at both the individual and dyadic levels. When categorized according to rank class, alpha females were the only class to perform significantly more grooming than they received. These results are inconsistent with reports on vervets, baboons and macaques, and suggest that grooming in capuchin monkeys may have different functions from those reported for cercopithecine primates. A dyadic analysis revealed, however, that grooming occurred more often between closely ranked females, similar to what is seen in several Old World monkey species. Therefore, some aspects of grooming in capuchins are similar to that seen in Old World monkeys, but the way they distribute grooming is different, which may prompt a re-evaluation of current theories regarding the social function of allogrooming in non-human primates.
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Parr, L. A., Waller, B. M., & Fugate, J. (2005). Emotional communication in primates: implications for neurobiology. Curr. Opin. Neurobiol., 15(6), 716–720.
Abstract: The social brain hypothesis proposes that large neocortex size in Homonoids evolved to cope with the increasing demands of complex group living and greater numbers of interindividual relationships. Group living requires that individuals communicate effectively about environmental and internal events. Recent data have highlighted the complexity of chimpanzee communication, including graded facial expressions and referential vocalizations. Among Hominoids, elaborate facial communication is accompanied by specializations in brain areas controlling facial movement. Finally, the evolution of empathy, or emotional awareness, might have a neural basis in specialized cells in the neocortex, that is, spindle cells that have been associated with self-conscious emotions, and mirror neurons that have recently been shown to activate in response to communicative facial gestures.
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Hopkins, W. D., & Parr, L. A. (1998). Lateralized behavior and lymphocyte counts in chimpanzees (pan troglodytes): A cross-sectional and longitudinal assessment. Developmental Neuropsychology, 14(4), 519–533.
Abstract: Cross?sectional and longitudinal assessment of lymphocyte count and behavioral laterality was examined in a sample of captive chimpanzees (Pan troglodytes) to assess the validity of the Geschwind?Behan?Galaburda (GBG) theory of cerebral lateralization. For the cross?sectional analysis, chimpanzees classified as right?handed for feeding exhibited lower lymphocyte counts than chimpanzees classified as either ambiguously handed or left?handed. Longitudinal analysis indicated that some measures of laterality within the first 3 months of life predicted (a) direction of hand preference at 2 to 5 years of age and (b) lymphocyte counts for the first 3 years of life. The association between lymphocyte count and behavioral laterality was more evident in males than females. Taken together, the results support some aspects of the GBG theory.
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Taubert, J., Weldon, K. B., & Parr, L. A. (2016). Robust representations of individual faces in chimpanzees (Pan troglodytes) but not monkeys (Macaca mulatta). Anim. Cogn., , 1–9.
Abstract: Being able to recognize the faces of our friends and family members no matter where we see them represents a substantial challenge for the visual system because the retinal image of a face can be degraded by both changes in the person (age, expression, pose, hairstyle, etc.) and changes in the viewing conditions (direction and degree of illumination). Yet most of us are able to recognize familiar people effortlessly. A popular theory for how face recognition is achieved has argued that the brain stabilizes facial appearance by building average representations that enhance diagnostic features that reliably vary between people while diluting features that vary between instances of the same person. This explains why people find it easier to recognize average images of people, created by averaging multiple images of the same person together, than single instances (i.e. photographs). Although this theory is gathering momentum in the psychological and computer sciences, there is no evidence of whether this mechanism represents a unique specialization for individual recognition in humans. Here we tested two species, chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta), to determine whether average images of different familiar individuals were easier to discriminate than photographs of familiar individuals. Using a two-alternative forced-choice, match-to-sample procedure, we report a behaviour response profile that suggests chimpanzees encode the faces of conspecifics differently than rhesus monkeys and in a manner similar to humans.
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Parr, L. A. (2004). Perceptual biases for multimodal cues in chimpanzee (Pan troglodytes) affect recognition. Anim. Cogn., 7(3), 171–178.
Abstract: The ability of organisms to discriminate social signals, such as affective displays, using different sensory modalities is important for social communication. However, a major problem for understanding the evolution and integration of multimodal signals is determining how humans and animals attend to different sensory modalities, and these different modalities contribute to the perception and categorization of social signals. Using a matching-to-sample procedure, chimpanzees discriminated videos of conspecifics' facial expressions that contained only auditory or only visual cues by selecting one of two facial expression photographs that matched the expression category represented by the sample. Other videos were edited to contain incongruent sensory cues, i.e., visual features of one expression but auditory features of another. In these cases, subjects were free to select the expression that matched either the auditory or visual modality, whichever was more salient for that expression type. Results showed that chimpanzees were able to discriminate facial expressions using only auditory or visual cues, and when these modalities were mixed. However, in these latter trials, depending on the expression category, clear preferences for either the visual or auditory modality emerged. Pant-hoots and play faces were discriminated preferentially using the auditory modality, while screams were discriminated preferentially using the visual modality. Therefore, depending on the type of expressive display, the auditory and visual modalities were differentially salient in ways that appear consistent with the ethological importance of that display's social function.
Keywords: Acoustic Stimulation; *Animal Communication; Animals; Auditory Perception/physiology; Cues; Discrimination Learning/*physiology; Facial Expression; Female; Male; Pan troglodytes/*psychology; Perceptual Masking/*physiology; Photic Stimulation; Recognition (Psychology)/*physiology; Visual Perception/physiology; *Vocalization, Animal
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Parr, L. A., Hopkins, W. D., & de Waal, F. B. (1997). Haptic discrimination in capuchin monkeys (Cebus apella): evidence of manual specialization. Neuropsychologia, 35(2), 143–152.
Abstract: Two experiments investigated the effects of haptic and visual discrimination on hand preference in 22 brown capuchin monkeys (Cebus apella). The percentage of left-handed subjects in Experiment 1 were 63.6%, 45.5%, and 18.2% for haptic, bipedal, and quadrupedal reaching, respectively. In Experiment 2, the haptic demands of the task were manipulated by using additional food types and another tactile medium. Left-hand preferences were further strengthened when reaching into water compared to pineshavings in Experiment 1. Reaching with no tactile interference resulted in equal numbers of lateralized and nonlateralized subjects. These results show that when reaching demands the use of haptic cues, as opposed to visual ones, monkeys shift towards greater left hand use. This is consistent with what is known about right hemisphere superiority for haptic discrimination in humans.
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Parr, L. A., & de Waal, F. B. (1999). Visual kin recognition in chimpanzees (Vol. 399).
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Parr, L. A., Winslow, J. T., Hopkins, W. D., & de Waal, F. B. (2000). Recognizing facial cues: individual discrimination by chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). J Comp Psychol, 114(1), 47–60.
Abstract: Faces are one of the most salient classes of stimuli involved in social communication. Three experiments compared face-recognition abilities in chimpanzees (Pan troglodytes) and rhesus monkeys (Macaca mulatta). In the face-matching task, the chimpanzees matched identical photographs of conspecifics' faces on Trial 1, and the rhesus monkeys did the same after 4 generalization trials. In the individual-recognition task, the chimpanzees matched 2 different photographs of the same individual after 2 trials, and the rhesus monkeys generalized in fewer than 6 trials. The feature-masking task showed that the eyes were the most important cue for individual recognition. Thus, chimpanzees and rhesus monkeys are able to use facial cues to discriminate unfamiliar conspecifics. Although the rhesus monkeys required many trials to learn the tasks, this is not evidence that faces are not as important social stimuli for them as for the chimpanzees.
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