Individual identity and affective valence in marmoset calls: in vivo brain imaging with vocal sound playback

As with humans, vocal communication is an important social tool for nonhuman primates. Common marmosets (Callithrix jacchus) often produce whistle-like ‘phee’ calls when they are visually separated from conspecifics. The neural processes specific to phee call perception, however, are largely unknown, despite the possibility that these processes involve social information. Here, we examined behavioral and whole-brain mapping evidence regarding the detection of individual conspecific phee calls using an audio playback procedure. Phee calls evoked sound exploratory responses when the caller changed, indicating that marmosets can discriminate between caller identities. Positron emission tomography with [¹⁸F] fluorodeoxyglucose revealed that perception of phee calls from a single subject was associated with activity in the dorsolateral prefrontal, medial prefrontal, orbitofrontal cortices, and the amygdala. These findings suggest that these regions are implicated in cognitive and affective processing of salient social information. However, phee calls from multiple subjects induced brain activation in only some of these regions, such as the dorsolateral prefrontal cortex. We also found distinctive brain deactivation and functional connectivity associated with phee call perception depending on the caller change. According to changes in pupillary size, phee calls from a single subject induced a higher arousal level compared with those from multiple subjects. These results suggest that marmoset phee calls convey information about individual identity and affective valence depending on the consistency or variability of the caller. Based on the flexible perception of the call based on individual recognition, humans and marmosets may share some neural mechanisms underlying conspecific vocal perception.     

Affect intensity in voice recognized by tree shrews (Tupaia belangeri)

Shared acoustic cues in speech, music, and nonverbal emotional expressions were postulated to code for emotion quality and intensity favoring the hypothesis of a prehuman origin of affective prosody in human emotional communication. To explore this hypothesis, we examined in playback experiments using a habituation-dishabituation paradigm whether a solitary foraging, highly vocal mammal, the tree shrew, is able to discriminate two behaviorally defined states of affect intensity (low vs. high) from the voice of conspecifics. Playback experiments with communication calls of two different types (chatter call and scream call) given in the state of low affect intensity revealed that habituated tree shrews dishabituated to one call type (the chatter call) and showed a tendency to do so for the other one (the scream call), both given in the state of high affect intensity. Findings suggest that listeners perceive the acoustic variation linked to defined states of affect intensity as different within the same call type. Our findings in tree shrews provide first evidence that acoustically conveyed affect intensity is biologically relevant without any other sensory cue, even for solitary foragers. Thus, the perception of affect intensity in voice conveyed in stressful contexts represents a shared trait of mammals, independent of the complexity of social systems. Findings support the hypothesis that affective prosody in human emotional communication has deep-reaching phylogenetic roots, deriving from precursors already present and relevant in the vocal communication system of early mammals.     

Perception of individuality in bat vocal communication: discrimination between, or recognition of, interaction partners?

Different cognitive processes underlying voice identity perception in humans may have precursors in mammals. A perception of vocal signatures may govern individualised interactions in bats, which comprise species living in complex social structures and are nocturnal, fast-moving mammals. This paper investigates to what extent bats recognise, and discriminate between, individual voices and discusses acoustic features relevant for accomplishing these tasks. In spontaneous presentation and habituation–dishabituation experiments, we investigated how Megaderma lyra perceives and evaluates stimuli consisting of contact call series with individual-specific signatures from either social partners or unknown individuals. Spontaneous presentations of contact call stimuli from social partners or unknown individuals elicited strong, but comparable reactions. In the habituation–dishabituation experiments, bats dishabituated significantly to any new stimulus. However, reactions were less pronounced to a novel stimulus from the bat used for habituation than to stimuli from other bats, irrespective of familiarity, which provides evidence for identity discrimination. A model separately assessing the dissimilarity of stimuli in syllable frequencies, syllable durations and inter-call intervals relative to learned memory templates accounted for the behaviour of the bats. With respect to identity recognition, the spontaneous presentation experiments were not conclusive. However, the habituation–dishabituation experiments suggested that the bats recognised voices of social partners as the reaction to a re-habituation stimulus differed after a dishabituation stimulus from a social partner and an unknown bat.     

Acoustic variability and individual distinctiveness in the vocal repertoire of red-capped mangabeys (Cercocebus torquatus)

Acoustic variability and individual distinctiveness of vocal signals are expected to vary with both their communicative function and the need for individual recognition during social interactions. So far, few attempts have been made to comparatively study these features across the different call types within a species' vocal repertoire. We collected recordings of the six most common call types from 14 red-capped mangabeys (Cercocebus torquatus) to assess intra- and interindividual acoustic variability, using a range of temporal and frequency parameters. Acoustic variability was highest in contact and threat calls, intermediate in food calls, and lowest in loud and alarm calls. Individual distinctiveness was high in contact, threat, loud and alarm calls, and low in food calls. In sum, calls mediating intragroup social interactions were structurally most variable and individually most distinctive, highlighting the key role that social factors must have played in the evolution of the vocal repertoire in this species. We discuss these findings in light of existing hypotheses of acoustic variability in primate vocal behavior.     

Social processes in communication and cognition in callitrichid monkeys: a review

Studies of vocal development in nonhuman primates have found little evidence for plasticity in vocal production, somewhat more for usage of calls, with the greatest plasticity arising in response to calls of others. Generally, similar results were obtained with callitrichid monkeys, the marmosets and tamarins, but with several interesting exceptions. Infant pygmy marmosets show babbling behavior with improvement in adult call structure related to the amount and diversity of babbling. Adult marmosets alter call structure in response to changes in social partners, and wild marmosets have vocal dialects and modify call structure according to how far they are from other group members, suggesting the potential to modify call structure in different social and environmental contexts, though direct learning of novel vocalizations has not been observed. Infant cotton-top tamarins do not produce adult-like calls in appropriate contexts, at least in the first few months of life, but through food sharing from adults infants learn about appropriate foods and the appropriate contexts for food vocalizations. Tamarins modify call structure and usage with changes in social status. Tamarins, unlike other monkeys tested, can learn to avoid noxious foods through observation of other group members, and can learn about novel food locations. Recent studies provide evidence of contextual imitation in marmosets. The plasticity in vocal communication and evidence of social learning in marmosets and tamarins relative to other monkeys may be related to the cooperative breeding system of marmosets and tamarins. With a high degree of behavioral coordination among group members, there is a priority on monitoring signals and behavior of others and adjusting one's own signals and behavior. This creates the context for vocal plasticity and social learning. Accepted after revision: 23 May 2001 Electronic Publication     

Sex and species recognition by wild male southern white rhinoceros using contact pant calls

Recognition of information from acoustic signals is crucial in many animals, and individuals are under selection pressure to discriminate between the signals of conspecifics and heterospecifics or males and females. Here, we first report that rhinos use information encoded in their calls to assess conspecifics and individuals of closely related species. The southern (Ceratotherium simum) and critically endangered northern (C. cottoni) white rhinos are the most social out of all the rhinoceros species and use a contact call pant. We found that southern white rhino pant calls provide reliable information about the caller’s sex, age class and social situation. Playback experiments on wild territorial southern white rhinoceros males revealed that they responded more strongly to the pant calls of conspecific females compared to the calls of other territorial males. This suggests that pant calls are more important form of communication between males and females than between territorial males. Territorial southern males also discriminated between female and territorial male calls of northern species and reacted more intensively to the calls of northern than southern males. This might be caused by a novelty effect since both species naturally live in allopatry. We conclude that white rhinos can directly benefit from assessing individuals at long distances using vocal cues especially because their eyesight is poor. Pant calls thus likely play a significant role in their social relationships and spatial organization. In addition, better understanding of vocal communication in white rhinos might be helpful in conservation management particularly because of their low reproduction in captivity.     

Is acoustic evaluation in a non-primate mammal,the tree shrew,affected by context?

Sound categorisation plays a crucial role for processing ecological and social stimuli in a species’ natural environment. To explore the discrimination and evaluation of sound stimuli in human babies and nonhuman primates, a reciprocal habituation-dishabituation paradigm has been successfully introduced into auditory research. We applied the reciprocal paradigm for the first time to a non-primate mammal, the tree shrew (Tupaia belangeri), to examine to what extent non-primate mammals share the ability to evaluate communication calls with primates. Playback stimuli were three types of communication calls, differing distinctively in context and acoustic structure, as well as two artificial control sounds, differing solely in frequency. We assessed the attention towards the playback stimuli by the latency to respond to the test stimulus. Subjects evaluated pairs of communication call types as well as the artificial playback stimuli. Attention towards the test stimuli differed significantly in strength for one pair of communication calls, with subjects dishabituating faster to one category than the other. The comparison of a second pair of communication calls did not show significant differences. Interestingly, subjects also evaluated the artificial control sounds. Findings are only partly in line with results on human and non-human primates. They provided first evidence that in non-primate mammals acoustic evaluation is not solely affected by the sound-associated context but is also linked to unusualness and acoustic cues, such as peak frequency.     

Face processing in humans and new world monkeys: the influence of experiential and ecological factors

This study tests whether the face-processing system of humans and a nonhuman primate species share characteristics that would allow for early and quick processing of socially salient stimuli: a sensitivity toward conspecific faces, a sensitivity toward highly practiced face stimuli, and an ability to generalize changes in the face that do not suggest a new identity, such as a face differently oriented. The look rates by adult tamarins and humans toward conspecific and other primate faces were examined to determine if these characteristics are shared. A visual paired comparison (VPC) task presented subjects with either a human face, chimpanzee face, tamarin face, or an object as a sample, and then a pair containing the previous stimulus and a novel stimulus was presented. The stimuli were either presented all in an upright orientation, or all in an inverted orientation. The novel stimulus in the pair was either an orientation change of the same face/object or a new example of the same type of face/object, and the stimuli were shown either in an upright orientation or in an inverted orientation. Preference to novelty scores revealed that humans attended most to novel individual human faces, and this effect decreased significantly if the stimuli were inverted. Tamarins showed preferential looking toward novel orientations of previously seen tamarin faces in the upright orientation, but not in an inverted orientation. Similarly, their preference to look longer at novel tamarin and human faces within the pair was reduced significantly with inverted stimuli. The results confirmed prior findings in humans that novel human faces generate more attention in the upright than in the inverted orientation. The monkeys also attended more to faces of conspecifics, but showed an inversion effect to orientation change in tamarin faces and to identity changes in tamarin and human faces. The results indicate configural processing restricted to particular kinds of primate faces by a New World monkey species, with configural processing influenced by life experience (human faces and tamarin faces) and specialized to process orientation changes specific to conspecific faces.     

Horse (Equus caballus) whinnies: a source of social information

Many animal species that rely mainly on calls to communicate produce individual acoustic structures, but we wondered whether individuals of species better known as visual communicants, with small vocal repertoires, would also exhibit individual distinctiveness in calls. Moreover, theoretical advances concerning the evolution of social intelligence are usually based on primate species data, but relatively little is known about the social cognitive capacities of non-primate mammals. However, some non-primate species demonstrate auditory recognition of social categories and possess mental representation of their social network. Horses (Equus caballus) form stable social networks and although they display a large range of visual signals, they also use long-distance whinny calls to maintain contact. Here, we investigated the potential existence of individual acoustic signatures in whinny calls and the ability of horses to discriminate by ear individuals varying in their degree of familiarity. Our analysis of the acoustic structure of whinnies of 30 adult domestic horses (ten stallions, ten geldings, ten mares) revealed that some of the frequency and temporal parameters carried reliable information about the caller’s sex, body size and identity. However, no correlations with age were found. Playback experiments evaluated the behavioural significance of this variability. Twelve horses heard either control white noise or whinnies emitted by group members, familiar neighbours or unfamiliar horses. While control sounds did not induce any particular response, horses discriminated the social category of the callers and reacted with a sound-specific behaviour (vigilance and attraction varied with familiarity). Our results support the existence of social knowledge in horses and suggest a process of vocal coding/decoding of information.     

Salience of caller identity in rhesus monkey (Macaca mulatta) coos and screams: perceptual experiments with human (Homo sapiens) listeners

Recent evidence from acoustic analysis and playback experiments indicates that adult female rhesus monkey (Macaca mulatta) coos are individually distinctive but their screams are not. In this study, the authors compared discrimination of individual identity in these sounds by naive human listeners who judged whether 2 sounds had been produced by the same monkey or 2 monkeys. Each of 3 experiments using this same-different design showed significantly better discrimination of vocalizer identity from coos than from screams. Experiment 1 demonstrated the basic finding. Experiment 2 also tested the effect of non-identity-related scream variation, and Experiment 3 added a comparison with human vowel sounds. Outcomes suggest that acoustic structural differences in coos and screams influence salience of caller-identity cues, with significant implications for understanding the functions of these calls.     

Face processing in cotton-top tamarins (Saguinus oedipus)

Current research on face processing in primates has focused on a few species, mostly macaques and chimpanzees; to date, only one New World monkey, the squirrel monkey, has been tested. We explored face processing, and the inversion effect in particular, in a New World primate species, the cotton-top tamarin (Saguinus oedipus). In phase 1 of our study, we trained subjects to discriminate between two faces and two scrambled faces; we then presented the tamarins with a series of novel probes in order to determine the features underlying classification. Results showed that the tamarins relied on the external contour of the face for discrimination more than the internal features and their configuration. Statistical analyses revealed no differences in accuracy or response times to upright versus inverted stimuli, and thus no inversion effect. In phase 2, we provided subjects with additional training on the face versus scrambled face discrimination task in order to focus their attention on the configuration of the internal features. Accuracy data revealed individual differences in how tamarins classified these stimuli, even though each subject was trained in the same way. In phase 3, we tested for generalization to a new set of face stimuli, as well as for the capacity to show an inversion effect. For one subject who attended to the configuration of internal features, we found significant evidence of generalization, but no evidence for an inversion effect. Electronic Publication     

Numbers or apologies? Customer reactions to telephone waiting time fillers

The authors examined the effect of time perception and sense of progress in telephone queues on caller reactions to 3 telephone waiting time fillers: music, apologies, and information about location in the queue. In Study 1, conducted on 123 real calls, call abandonment was lowest, and call evaluations were most positive with information about location in the queue as the time filler. In Study 2, conducted with 83 participants who experienced a simulated telephone wait experience, sense of progress in the queue rather than perceived waiting time mediated the relationship between telephone waiting time filler and caller reactions. The findings provide insight for the management and design of telephone queues, as well as theoretical insight into critical cognitive processes that underlie telephone waiting, opening up an important new research agenda.     

Tracking responses related to self-recognition: a frequency comparison of responses to mirrors, photographs, and videotapes by cotton top tamanins (Saguinus oedipus)

The frequency of responses cotton top tamarins (Saguinus oedipus) emitted indicative of self-recognition to a mirror was compared with the frequencies of responses emitted to digitized photographs of tamarins (Experiment 1) and to videotapes of real-time or prior tamarin action (Experiment 2). Results indicated more attentional responses toward the mirror in both studies, but behavioral indices of self-recognition were not consistently generated by the mirror. The 2 experiments confirmed that real-time self-reflection is a condition that generates heightened attention and rare examples of particular mirror-specific behaviors in tamarins.     

Context-related call combinations in female Diana monkeys

Non-human primates possess species-specific repertoires of acoustically distinct call types that can be found in adults in predictable ways. Evidence for vocal flexibility is generally rare and typically restricted to acoustic variants within the main call types or sequential production of multiple calls. So far, evidence for context-specific call sequences has been mainly in relation to external disturbances, particularly predation. In this study, we investigated extensively the vocal behaviour of free-ranging and individually identified Diana monkeys in non-predatory contexts. We found that adult females produced four vocal structures alone (‘H’, ‘L’, ‘R’ and ‘A’ calls, the latter consisting of two subtypes) or combined in non-random ways (‘HA’, ‘LA’ and ‘RA’ call combinations) in relation to ongoing behaviour or external events. Specifically, the concatenation of an introductory call with the most frequently emitted and contextually neutral ‘A’ call seems to function as a contextual refiner of this potential individual identifier. Our results demonstrate that some non-human primates are able to increase the effective size of their small vocal repertoire not only by varying the acoustic structure of basic call types but also by combining them into more complex structures. We have demonstrated this phenomenon for a category of vocalisations with a purely social function and discuss the implications of these findings for evolutionary theories of primate vocal communication.     

What’s in a voice? Dolphins do not use voice cues for individual recognition

Most mammals can accomplish acoustic recognition of other individuals by means of “voice cues,” whereby characteristics of the vocal tract render vocalizations of an individual uniquely identifiable. However, sound production in dolphins takes place in gas-filled nasal sacs that are affected by pressure changes, potentially resulting in a lack of reliable voice cues. It is well known that bottlenose dolphins learn to produce individually distinctive signature whistles for individual recognition, but it is not known whether they may also use voice cues. To investigate this question, we played back non-signature whistles to wild dolphins during brief capture-release events in Sarasota Bay, Florida. We hypothesized that non-signature whistles, which have varied contours that can be shared among individuals, would be recognizable to dolphins only if they contained voice cues. Following established methodology used in two previous sets of playback experiments, we found that dolphins did not respond differentially to non-signature whistles of close relatives versus known unrelated individuals. In contrast, our previous studies showed that in an identical context, dolphins reacted strongly to hearing the signature whistle or even a synthetic version of the signature whistle of a close relative. Thus, we conclude that dolphins likely do not use voice cues to identify individuals. The low reliability of voice cues and the need for individual recognition were likely strong selective forces in the evolution of vocal learning in dolphins.     

Geographic vocal variation and perceptual discrimination abilities in male Australian sea lions

Vocal characteristics can vary among and within populations. In species with geographic variation in the structure of vocalizations, individuals may have the ability to discriminate between calls from local and non-local individuals. The ability to distinguish differences in acoustic signals is likely to have a significant influence on the outcome of social interactions between individuals, including potentially mate selection and breeding success. Pinnipeds (seals, fur seals, sea lions and walruses) are highly vocal yet the Australian sea lion (Neophoca cinerea) is the only eared seal known to show geographic vocal variation in male barks. Barks are produced in many social interactions and encode sufficient information for both individual and colony identity to be discriminable. Yet until now, whether males could themselves discriminate these bark differences was unclear. We performed playback experiments in four breeding colonies to investigate whether males can discriminate local from non-local barks. Overall, males responded more strongly to barks from their own colony compared to barks from other colonies regardless of whether those other colonies were close or distant. Competition for females is high in Australian sea lions, but mating periods are asynchronous across colonies. The ability to correctly assess whether a male is from the same colony, thus representing a potential competitor for mates, or merely a visitor from elsewhere, may influence how males interact with others. Given the high cost of fighting, the ability to discern competitors may influence the nature of male–male interactions and ultimately influence how they allocate reproductive effort.     

Defining Moments: Catalysts for Professional Development

In this series of papers, 17 genetic counselors describe defining moments, that is, personal experiences or events that led to a further realization of themselves as genetic counselors. These experiences, both positive and negative, describe a significant impact on the authors' professional growth and development. A call for papers was issued through the National Society of Genetic Counselors listserv and through the Journal of Genetic Counseling in 2001. This call resulted in the following 15 papers in which the authors were asked to describe the nature of a defining moment and how it affected their professional identity and practice. The authors provided an account of the experience or event, what it was about the experience that made it a defining moment, how it affected them personally and professionally, and if a defining moment was negative, how they were able to derive positive outcomes. Implications of these defining moments for other genetic counselors are discussed in a concluding paper.     

Effect of acoustic cue modifications on evoked vocal response to calls in zebra finches (Taeniopygia guttata)

Besides their song, which is usually a functionally well-defined communication signal with an elaborate acoustic structure, songbirds also produce a variety of shorter vocalizations named calls. While a considerable amount of work has focused on information coding in songs, little is known about how calls' acoustic structure supports communication processes. Because male and female zebra finches use calls during most of their interactions and answer to conspecific calls without visual contact, we aimed at identifying which calls' acoustic cues are necessary to elicit a vocal response. Using synthetic zebra finch calls, we examined evoked vocal response of male and female zebra finches to modified versions of the distance calls. Our results show that the vocal response of zebra finches to female calls requires the full harmonic structure of the call, whereas the frequency downsweep of male calls is necessary to evoke a vocal response. It is likely that both female and male calls require matching a similar frequency bandwidth to trigger a response in conspecific individuals.     

Attention grabbing in red deer sexual calls

Identifying the respective functions of distinct call types is an important step towards understanding the diversification of mammal vocal repertoires. Red deer (Cervus elaphus) stags give two distinct types of roars during the rut, termed ‘common roars’ and ‘harsh roars’. This study tests the hypothesis that harsh roars function to raise and maintain female attention to calling males. To this end, we examined the response of female red deer to playback sequences of common roar bouts including a bout of harsh roars midway through the sequence. We found that females not only substantially increased their attention to the bout of harsh roars but also then maintained overall higher attention levels to subsequent common roar bouts. Our results suggest that the specific acoustic characteristics of male red deer harsh roar bouts may have evolved to engage and maintain the attention of female receivers during the breeding season. More generally, they indicate a possible evolutionary path for the diversification of male sexual vocal repertoires.     

Can music with prosocial lyrics heal the working world? A field intervention in a call center

Music with lyrics about helping is shown to reduce aggression in the laboratory. This paper tests whether the prosocial lyric effect generalizes to reducing customer aggression in the workplace. A field experiment involved changing the hold music played to customers of a call center. The results of a 3 week study suggested that music significantly affected customers, but not in the way suggested by previous laboratory experiments; compared with days when instrumental background music was played, caller anger and employee exhaustion were lower on days when callers were played popular music with neutral, but not prosocial, lyrics. The findings suggest that music influences customer aggression, but that the prosocial lyric effect may not generalize from the laboratory to the call center.