Loosening the leash: The unique emotional canvas of human screams.

We use screams to explore ideas presented in the target article. Evolving first in animals as a response to predation, screams reveal more complex social use in nonhuman primates and, in humans, uniquely, are associated with a much greater variety of emotional contexts including fear, anger, surprise, and happiness. This expansion, and the potential for manipulation, promotes listener social vigilance.

Humans read emotional arousal in monkey vocalizations: evidence for evolutionary continuities in communication.

Humans and other mammalian species communicate emotions in ways that reflect evolutionary conservation and continuity, an observation first made by Darwin. One approach to testing this hypothesis has been to assess the capacity to perceive the emotional content of the vocalizations of other species. Using a binary forced choice task, we tested perception of the emotional intensity represented in coos and screams of infant and juvenile female rhesus macaques (Macaca mulatta) by 113 human listeners without, and 12 listeners with, experience (as researchers or care technicians) with this species. Each stimulus pair contained one high- and one low-arousal vocalization, as measured at the time of recording by stress hormone levels for coos and the degree of intensity of aggression for screams. For coos as well as screams, both inexperienced and experienced participants accurately identified the high-arousal vocalization at significantly above-chance rates. Experience was associated with significantly greater accuracy with scream stimuli but not coo stimuli, and with a tendency to indicate screams as reflecting greater emotional intensity than coos. Neither measures of empathy, human emotion recognition, nor attitudes toward animal welfare showed any relationship with responses. Participants were sensitive to the fundamental frequency, noisiness, and duration of vocalizations; some of these tendencies likely facilitated accurate perceptions, perhaps due to evolutionary homologies in the physiology of arousal and vocal production between humans and macaques. Overall, our findings support a view of evolutionary continuity in emotional vocal communication. We discuss hypotheses about how distinctive dimensions of human nonverbal communication, like the expansion of scream usage across a range of contexts, might influence perceptions of other species' vocalizations.

Vocal expression of emotional arousal across two call types in young rhesus macaques.

As Darwin first recognized, the study of emotional communication has the potential to improve scientific understanding of the mechanisms of signal production as well as how signals evolve. We examined the relationships between emotional arousal and selected acoustic characteristics of coo and scream vocalizations produced by female rhesus macaques, Macaca mulatta, during development. For coos, arousal was assessed through measures of stress-induced elevations of plasma cortisol exhibited in response to the human intruder test. In the analysis of screams, arousal was evaluated from the intensity of aggression experienced by the vocalizer during natural social interactions. Both call types showed a positive relationship between arousal and overall fundamental frequency (F0, perceived as pitch in humans). In coos, this association was dampened over development from infancy (6 months) to the juvenile, prepubertal period (16 months) and further to menarche (21.3-31.3 months), perhaps reflecting developmental changes in physiology, anatomy and/or call function. Heightened arousal was also associated in coos with increases in an acoustic dimension related to F0 modulation and noisiness. As monkeys matured, coos showed decreases in overall F0 as well as increased noisiness and F0 modulation, likely reflecting growth of the vocal apparatus and changes in vocal fold oscillation. Within screams, only one acoustic dimension (related to F0 modulation) showed developmental change, and only within one subclass of screams within one behavioural context. Our results regarding the acoustic correlates of arousal in both call types are broadly consistent with findings in other species, supporting the hypothesis of evolutionary continuity in emotion expression. We discuss implications for broader theories of how vocal acoustics respond to selection pressures.

When less is more in the evolution of language.

Did loss of vocal fold membranes typical of nonhuman primates enable human speech?

The emotional canvas of human screams: patterns and acoustic cues in the perceptual categorization of a basic call type.

Screams occur across taxonomically widespread species, typically in antipredator situations, and are strikingly similar acoustically, but in nonhuman primates, they have taken on acoustically varied forms in association with more contextually complex functions related to agonistic recruitment. Humans scream in an even broader range of contexts, but the extent to which acoustic variation allows listeners to perceive different emotional meanings remains unknown. We investigated how listeners responded to 30 contextually diverse human screams on six different emotion prompts as well as how selected acoustic cues predicted these responses. We found that acoustic variation in screams was associated with the perception of different emotions from these calls. Emotion ratings generally fell along two dimensions: one contrasting perceived anger, frustration, and pain with surprise and happiness, roughly associated with call duration and roughness, and one related to perceived fear, associated with call fundamental frequency. Listeners were more likely to rate screams highly in emotion prompts matching the source context, suggesting that some screams conveyed information about emotional context, but it is noteworthy that the analysis of screams from happiness contexts (n = 11 screams) revealed that they more often yielded higher ratings of fear. We discuss the implications of these findings for the role and evolution of nonlinguistic vocalizations in human communication, including consideration of how the expanded diversity in calls such as human screams might represent a derived function of language.

Do human screams permit individual recognition?

The recognition of individuals through vocalizations is a highly adaptive ability in the social behavior of many species, including humans. However, the extent to which nonlinguistic vocalizations such as screams permit individual recognition in humans remains unclear. Using a same-different vocalizer discrimination task, we investigated participants' ability to correctly identify whether pairs of screams were produced by the same person or two different people, a critical prerequisite to individual recognition. Despite prior theory-based contentions that screams are not acoustically well-suited to conveying identity cues, listeners discriminated individuals at above-chance levels by their screams, including both acoustically modified and unmodified exemplars. We found that vocalizer gender explained some variation in participants' discrimination abilities and response times, but participant attributes (gender, experience, empathy) did not. Our findings are consistent with abundant evidence from nonhuman primates, suggesting that both human and nonhuman screams convey cues to caller identity, thus supporting the thesis of evolutionary continuity in at least some aspects of scream function across primate species.

The credibility of acted screams: Implications for emotional communication research.

Researchers have long relied on acted material to study emotional expression and perception in humans. It has been suggested, however, that certain aspects of natural expressions are difficult or impossible to produce voluntarily outside of their associated emotional contexts, and that acted expressions tend to be overly intense caricatures. From an evolutionary perspective, listeners' abilities to distinguish acted from natural expressions likely depend on the type of expression in question, the costs entailed in its production, and elements of receiver psychology. Here, we investigated these issues as they relate to human screams. We also examined whether listeners' abilities to distinguish acted from natural screams might vary as a function of individual differences in emotional processing and empathy. Using a forced-choice categorization task, we found that listeners could not distinguish acted from natural exemplars, suggesting that actors can produce dramatisations of screams resembling natural vocalisations. Intensity ratings did not differ between acted and natural screams, nor did individual differences in emotional processing significantly predict performance. Scream duration predicted both the probability that an exemplar was categorised as acted and the probability that participants classified that scream accurately. These findings are discussed with respect to potential evolutionary implications and their practical relevance to future research using acted screams.

Behavioral and genetic correlates of the neural response to infant crying among human fathers.

Although evolution has shaped human infant crying and the corresponding response from caregivers, there is marked variation in paternal involvement and caretaking behavior, highlighting the importance of understanding the neurobiology supporting optimal paternal responses to cries. We explored the neural response to infant cries in fathers of children aged 1-2, and its relationship with hormone levels, variation in the androgen receptor (AR) gene, parental attitudes and parental behavior. Although number of AR CAG trinucleotide repeats was positively correlated with neural activity in brain regions important for empathy (anterior insula and inferior frontal gyrus), restrictive attitudes were inversely correlated with neural activity in these regions and with regions involved with emotion regulation (orbitofrontal cortex). Anterior insula activity had a non-linear relationship with paternal caregiving, such that fathers with intermediate activation were most involved. These results suggest that restrictive attitudes may be associated with decreased empathy and emotion regulation in response to a child in distress, and that moderate anterior insula activity reflects an optimal level of arousal that supports engaged fathering.

Reading chimpanzee faces: evidence for the role of verbal labels in categorical perception of emotion.

Categorical perception (CP) occurs when continuously varying stimuli are perceived as belonging to discrete categories. Thereby, perceivers are more accurate at discriminating between stimuli of different categories than between stimuli within the same category (Harnad, 1987; Goldstone, 1994). The current experiments investigated whether the structural information in the face is sufficient for CP to occur. Alternatively, a perceiver's conceptual knowledge, by virtue of expertise or verbal labeling, might contribute. In two experiments, people who differed in their conceptual knowledge (in the form of expertise, Experiment 1; or verbal label learning, Experiment 2) categorized chimpanzee facial expressions. Expertise alone did not facilitate CP. Only when perceivers first explicitly learned facial expression categories with a label were they more likely to show CP. Overall, the results suggest that the structural information in the face alone is often insufficient for CP; CP is facilitated by verbal labeling.

Recognition of rhesus macaque (Macaca mulatta) noisy screams: evidence from conspecifics and human listeners.

Vocalizations are among the diverse cues that animals use to recognize individual conspecifics. For some calls, such as noisy screams, there is debate over whether such recognition occurs. To test recognition of rhesus macaque noisy screams, recorded calls were played back to unrelated and related conspecific group members as either single calls or short bouts. Higher-ranking, but not lower-ranking, monkeys looked longer toward the playback speaker in trials containing screams from kin than in those composed of screams from nonkin. In a second study, human listeners performed a "same/different" discrimination task between presentations of rhesus screams from either the same or two different monkeys. Listeners discriminated between "same" and "different" callers above an established empirical threshold, whether screams were presented singly or in short bouts. Together, these results suggest that rhesus monkeys can distinguish noisy screams between kin and nonkin, and humans are able to discriminate different individuals' noisy screams, even when the duration of the bout is short. Whether noisy screams are ideally designed signals for individual recognition is discussed with respect to possible evolutionary origins of the calls.

Sex differences in juvenile rhesus macaque (Macaca mulatta) agonistic screams: life history differences and effects of prenatal androgens.

This study investigated sex differences in juvenile rhesus macaque (Macaca mulatta) vocal behavior during agonistic contexts, and the effects of prenatal androgens on these differences. A total of 59 subjects (5-8 per treatment group) received exogenous androgen (testosterone enanthate), an anti-androgen (flutamide) or vehicle injections (DMSO) for 30 or 35 days during the second (early) or third (late) trimester of pregnancy. An additional 19 unmanipulated controls were included in the analysis. Screams by juvenile males and females between the ages of 1 and 3 years were compared to the screams of adult female exemplars using a discriminant function analysis. Juvenile females produced more adult-female like screams than did juvenile males. Females exposed to androgen treatment late in gestation produced a more masculine pattern of screams. Flutamide treatment in males either early or late in gestation did not significantly affect scream production. Flutamide treatments in females late in gestation, however, masculinized scream production. Androgen treatments administered late in gestation hyper-masculinized male scream production. No sex differences in the contextual usage of screams emerged. These findings suggest that both life history differences and the early hormone environment contribute to sex differences in juvenile rhesus macaque vocal production.

Sex differences in the acquisition of communicative competence by pigtail macaques (Macaca nemestrina).

Previous study of captive pigtail monkeys (Macaca nemestrina) revealed that victims of an attack by a group member employed one of four acoustically different recruitment calls (Gouzoules&Gouzoules: Animal Behaviour 37:383-401, 1989). The calls appear to provide allies with information pertinent to decisions about fight intervention. Each call was associated with an agonistic context distinguished by the relative rank of the opponent and the severity of the attack. Monkeys younger than 3 years of age were significantly less likely to use a contextually appropriate call than were older animals and their calls tended to be acoustically less like the prototype for a given context. Analyses reported on here revealed that, among juveniles, females were more proficient than males in both the proper contextual use and the production of these calls. These findings suggest parallels with human sex differences in the development of communicative competence. The evolutionary origins for these sex differences in macaque vocal development may be based in the different life history patterns males and females exhibit.

Physiological and social influences on mounting behavior of troop-living female monkeys (Macaca fuscata).

Female mounting behavior was studied in a troop of Japanese macaques during one breeding season. Of 79 sexually active females, mounting behavior during consortships was shown by 50 females; 13 only with males, 20 with both males and females, and 17 only with females. Several factors associated with reproductive state influenced the expression of mounting activity. Recency of parturition influenced the mounting by females regardless of the type of partner. Females that had not given birth the previous spring (four to six months prior to the period of observation) were more likely both to mount partners and to produce an infant the following spring. These findings suggest the existence of a common factor, perhaps associated with lactation, inhibitory both to expression of mounting and to female fertility. Additionally, females that mounted were more likely to do so in consortships that followed than in those that preceded conception. This last finding suggests that, in this social context, the endocrine conditions of early pregnancy facilitated mounting to a greater extent than those associated with the cyclic ovary. Separate statistical analyses examined possible influences of age, dominance rank, and kinship on the likelihoods of mounting and being mounted. None of these factors influenced female mounting. Results suggest that the expression of mounting by females was more influenced by reproductive state than by social characteristics of the partner.