Preference for consonant music over dissonant music by an infant chimpanzee

It has been shown that humans prefer consonant sounds from the early stages of development. From a comparative psychological perspective, although previous studies have shown that birds and monkeys can discriminate between consonant and dissonant sounds, it remains unclear whether nonhumans have a spontaneous preference for consonant music over dissonant music as humans do. We report here that a five-month-old human-raised chimpanzee (Pan troglodytes) preferred consonant music. The infant chimpanzee consistently preferred to produce, with the aid of our computerized setup, consonant versions of music for a longer duration than dissonant versions. This result suggests that the preference for consonance is not unique to humans. Further, it supports the hypothesis that one major basis of musical appreciation has some evolutionary origins.     

On the Relevance of Natural Stimuli for the Study of Brainstem Correlates: The Example of Consonance Perception

Some combinations of musical tones sound pleasing to Western listeners, and are termed consonant, while others sound discordant, and are termed dissonant. The perceptual phenomenon of consonance has been traced to the acoustic property of harmonicity. It has been repeatedly shown that neural correlates of consonance can be found as early as the auditory brainstem as reflected in the harmonicity of the scalp-recorded frequency-following response (FFR). “Neural Pitch Salience” (NPS) measured from FFRs—essentially a time-domain equivalent of the classic pattern recognition models of pitch—has been found to correlate with behavioral judgments of consonance for synthetic stimuli. Following the idea that the auditory system has evolved to process behaviorally relevant natural sounds, and in order to test the generalizability of this finding made with synthetic tones, we recorded FFRs for consonant and dissonant intervals composed of synthetic and natural stimuli. We found that NPS correlated with behavioral judgments of consonance and dissonance for synthetic but not for naturalistic sounds. These results suggest that while some form of harmonicity can be computed from the auditory brainstem response, the general percept of consonance and dissonance is not captured by this measure. It might either be represented in the brainstem in a different code (such as place code) or arise at higher levels of the auditory pathway. Our findings further illustrate the importance of using natural sounds, as a complementary tool to fully-controlled synthetic sounds, when probing auditory perception.     

Patterns of Gazing in Orangutans (Pongo pygmaeus)

Eyes play an important role in communication amongst humans and animals. However, relatively little is known about specific differences in eye morphology amongst primates and how these features might be associated with social structure and direction of gaze. We present a detailed study of gazing and eye morphology—exposed sclera and surrounding features—in orangutans. We measured gazing in rehabilitating orangutans in two contexts: interspecific viewing of the experimenter (with video camera) and intraspecific gazing (between subjects). Our findings show that direct staring is avoided and social looking is limited to certain age/social categories: juveniles engage in more looking at other orangutans than do adults or infants. While orangutans use eye movements in social communication, they avoid the more prolonged mutual gaze that is characteristic of humans, and also apparent in chimpanzees and gorillas. Detailed frame-by-frame analysis of videotapes from field and zoo studies of orangutans revealed that they pay visual attention to both human observers and conspecifics by glancing sideways, with the head turned at an angle away from the subject being observed. Mutual gaze was extremely rare, and we have observed only two incidences of gaze following. Orangutans in captivity appear to use a more restricted pattern of gazes compared to free-living, rehabilitating ones, possibly suggesting the presence of a pathological condition (such as depression) in the captive subjects. Our findings have implications for further investigations of social communication and cognition in orangutans.     

Rapid facial mimicry in orangutan play

Emotional contagion enables individuals to experience emotions of others. This important empathic phenomenon is closely linked to facial mimicry, where facial displays evoke the same facial expressions in social partners. In humans, facial mimicry can be voluntary or involuntary, whereby its latter mode can be processed as rapid as within or at 1s. Thus far, studies have not provided evidence of rapid involuntary facial mimicry in animals.This study assessed whether rapid involuntary facial mimicry is present in orangutans (Pongo pygmaeus; N=25) for their open-mouth faces (OMFs) during everyday dyadic play. Results clearly indicated that orangutans rapidly mimicked OMFs of their playmates within or at 1s. Our study revealed the first evidence on rapid involuntary facial mimicry in non-human mammals. This finding suggests that fundamental building blocks of positive emotional contagion and empathy that link to rapid involuntary facial mimicry in humans have homologues in non-human primates.     

How Different Are Our Perceptions of Equal-Tempered and Microtonal Intervals? A Behavioural and EEG Survey

For listeners familiar with Western twelve-tone equal-tempered (12-TET) music, a novel microtonal tuning system is expected to present additional processing challenges. We aimed to determine whether this was the case, focusing on the extent to which our perceptions can be considered bottom-up (psychoacoustic and primarily perceptual) and top-down (dependent on familiarity and cognitive processing). We elicited both overt response ratings, and covert event-related potentials (ERPs), so as to compare subjective impressions of sounds with the neurophysiological processing of the acoustic signal. We hypothesised that microtonal intervals are perceived differently from 12-TET intervals, and that the responses of musicians (n = 10) and non-musicians (n = 10) are distinct. Two-note chords were presented comprising 12-TET intervals (consonant and dissonant) or microtonal (quarter tone) intervals, and ERP, subjective roughness ratings, and liking ratings were recorded successively. Musical experience mediated the perception of differences between dissonant and microtone intervals, with non-musicians giving similar ratings for each, and musicians preferring dissonant over the less commonly used microtonal intervals, rating them as less rough. ERP response amplitude was greater for consonant intervals than other intervals. Musical experience interacted with interval type, suggesting that musical expertise facilitates the sensory and perceptual discrimination of microtonal intervals from 12-TET intervals, and an increased ability to categorize such intervals. Non-musicians appear to have perceived microtonal intervals as instances of neighbouring 12-TET intervals.     

Harmonic calls and indifferent females: no preference for human consonance in an anuran

The human music faculty might have evolved from rudimentary components that occur in non-human animals. The evolutionary history of these rudimentary perceptual features is not well understood and rarely extends beyond a consideration of vertebrates that possess a cochlea. One such antecedent is a preferential response to what humans perceive as consonant harmonic sounds, which are common in many animal vocal repertoires. We tested the phonotactic response of female túngara frogs (Physalaemus pustulosus) to variations in the frequency ratios of their harmonically structured mating call to determine whether frequency ratio influences attraction to acoustic stimuli in this vertebrate that lacks a cochlea. We found that the ratio of frequencies present in acoustic stimuli did not influence female response. Instead, the amount of inner ear stimulation predicted female preference behaviour. We conclude that the harmonic relationships that characterize the vocalizations of these frogs did not evolve in response to a preference for frequency intervals with low-integer ratios. Instead, the presence of harmonics in their mating call, and perhaps in the vocalizations of many other animals, is more likely due to the biomechanics of sound production rather than any preference for ‘more musical’ sounds.     

Evolution of nuclear gene families in primates,Copy-number variation in the argininosuccinate synthetase (ASS) pseudogene family and the anonymous DNA sequence,D1S1

Changes in the copy number of nuclear genes provide the raw material for the creation of new gene functions. To better understand the mechanisms for such events, and their physiologic and evolutionary consequences, it is valuable to study a well characterized and closely related group of species such as primates. Fortuitously, most of the powerful molecular techniques and DNA probes developed for research in humans are equally applicable to non-human primates. We review what is known of copy number variation in primates and describe two informative DNA probes: pAS-1, a cDNA probe to the human urea cycle enzyme argininosuccinate synthetase (ASS), and an anonymous DNA probe, D1S1.In additon to the ASS structural locus on human chromosome 9, pAS-1 detects at least 14 dispersed, processed pseudogenes in humans. The number of pseudogene copies appears to be approximately the same in humans, chimpanzees, gorillas, orangutans and baboons; less in marmosets; and least in some rodents. Chimpanzees and gorillas appear to have all of the human pseudogenes though an Xp copy may be missing from gorillas. The Y pseudogene is apparently absent from orangutans and baboons, and, finally, a comparison of humans and chimpanzees revealed that the number of nucleotide substitutions in the Y chromosome pseudogenes is approximately 1 per 100.D1S1 maps to human chromosome 3 but also detects a high homology copy on chromosome 1. Chimpanzees, gorillas and orangutans all appear to have only the chromosome 3 homolog suggesting that this is the ancestral sequence and that the duplication occurred after separation of humans and the great apes.Both the ASS pseudogene family and the D1S1 system provide valuable information on the evolution of nuclear gene families in primates.     

Auditory processing--speech, space and auditory objects

There have been recent developments in our understanding of the auditory neuroscience of non-human primates that, to a certain extent, can be integrated with findings from human functional neuroimaging studies. This framework can be used to consider the cortical basis of complex sound processing in humans, including implications for speech perception, spatial auditory processing and auditory scene segregation.     

Acoustical expression of arousal in conflict situations in tree shrews (<Emphasis Type="Italic">Tupaia belangeri)</Emphasis>

Empirical research on human and non-human primates suggests that communication sounds express the intensity of an emotional state of a signaller. In the present study, we have examined communication sounds during induced social interactions of a monogamous mammal, the tree shrew. To signal their unwillingness to mate, female tree shrews show defensive threat displays towards unfamiliar males paralleled by acoustically variable squeaks. We assumed that the distance between interacting partners as well as the behavior of the male towards the female indicates the intensity of perceived social threat and thereby the arousal state of a female. To explore this hypothesis we analyzed dynamic changes in communication sounds uttered during induced social interactions between a female and an unfamiliar male. Detailed videographic and sound analyzes revealed that the arousal state predicted variations in communication sound structure reliably. Both, a decrease of distance and a male approaching the female led to an increase in fundamental frequency and repetition rate of syllables. These findings support comparable results in human and non-human primates and suggest that common coding rules in communication sounds govern acoustic conflict regulation in mammals.     

Monkeys,apes, mirrors and minds: The evolution of self-awareness in primates

Almost two decades of research on the self-recognition capacity of non-human primates has produced evidence of intriguing phylogenetic differences. Not a single species of monkey has demonstrated the ability to recognize its own reflection in a mirror, despite some claims to the contrary. To date, only humans, orangutans and chimpanzees have passed objective tests of mirror-recognition. This paper reviews the methodology and evidence for self-recognition in primates along with the assumption that this ability is an indicator of self-awareness. The failure of the gorilla to master the task is discussed in some detail, along with an evaluation of anecdotal evidence of self-recognition by at least one gorilla. Also, the evolutionary backdrop of the primates is considered with reference to this unique behavior. Evidence supporting alternate, non-cognitive interpretations of self-recognition is assessed.     

Economic behaviours among non-human primates

Do we have any valid reasons to affirm that non-human primates display economic behaviour in a sufficiently rich and precise sense of the phrase? To address this question, we have to develop a set of criteria to assess the vast array of experimental studies and field observations on individual cognitive and behavioural competences as well as the collective organization of non-human primates. We review a sample of these studies and assess how they answer to the following four main challenges. (i) Do we see any economic organization or institutions emerge among groups of non-human primates? (ii) Are the cognitive abilities, and often biases, that have been evidenced as underlying typical economic decision-making among humans, also present among non-human primates? (iii) Can we draw positive lessons from performance comparisons among primate species, humans and non-humans but also across non-human primate species, as elicited by canonical game-theoretical experimental paradigms, especially as far as economic cooperation and coordination are concerned? And (iv) in which way should we improve models and paradigms to obtain more ecological data and conclusions? Articles discussed in this paper most often bring about positive answers and promising perspectives to support the existence and prevalence of economic behaviours among non-human primates.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

Dogs Evaluate Threatening Facial Expressions by Their Biological Validity – Evidence from Gazing Patterns

Appropriate response to companions’ emotional signals is important for all social creatures. The emotional expressions of humans and non-human animals have analogies in their form and function, suggesting shared evolutionary roots, but very little is known about how animals other than primates view and process facial expressions. In primates, threat-related facial expressions evoke exceptional viewing patterns compared with neutral or positive stimuli. Here, we explore if domestic dogs (Canis familiaris) have such an attentional bias toward threatening social stimuli and whether observed emotional expressions affect dogs’ gaze fixation distribution among the facial features (eyes, midface and mouth). We recorded the voluntary eye gaze of 31 domestic dogs during viewing of facial photographs of humans and dogs with three emotional expressions (threatening, pleasant and neutral). We found that dogs’ gaze fixations spread systematically among facial features. The distribution of fixations was altered by the seen expression, but eyes were the most probable targets of the first fixations and gathered longer looking durations than mouth regardless of the viewed expression. The examination of the inner facial features as a whole revealed more pronounced scanning differences among expressions. This suggests that dogs do not base their perception of facial expressions on the viewing of single structures, but the interpretation of the composition formed by eyes, midface and mouth. Dogs evaluated social threat rapidly and this evaluation led to attentional bias, which was dependent on the depicted species: threatening conspecifics’ faces evoked heightened attention but threatening human faces instead an avoidance response. We propose that threatening signals carrying differential biological validity are processed via distinctive neurocognitive pathways. Both of these mechanisms may have an adaptive significance for domestic dogs. The findings provide a novel perspective on understanding the processing of emotional expressions and sensitivity to social threat in non-primates.     

Neural Responses to Smoking Stimuli Are Influenced by Smokers' Attitudes towards Their Own Smoking Behaviour

An important feature of addiction is the high drug craving that may promote the continuation of consumption. Environmental stimuli classically conditioned to drug-intake have a strong motivational power for addicts and can elicit craving. However, addicts differ in the attitudes towards their own consumption behavior: some are content with drug taking (consonant users) whereas others are discontent (dissonant users). Such differences may be important for clinical practice because the experience of dissonance might enhance the likelihood to consider treatment. This fMRI study investigated in smokers whether these different attitudes influence subjective and neural responses to smoking stimuli. Based on self-characterization, smokers were divided into consonant and dissonant smokers. These two groups were presented smoking stimuli and neutral stimuli. Former studies have suggested differences in the impact of smoking stimuli depending on the temporal stage of the smoking ritual they are associated with. Therefore, we used stimuli associated with the beginning (BEGIN-smoking-stimuli) and stimuli associated with the terminal stage (END-smoking-stimuli) of the smoking ritual as distinct stimulus categories. Stimulus ratings did not differ between both groups. Brain data showed that BEGIN-smoking-stimuli led to enhanced mesolimbic responses (amygdala, hippocampus, insula) in dissonant compared to consonant smokers. In response to END-smoking-stimuli, dissonant smokers showed reduced mesocortical responses (orbitofrontal cortex, subcallosal cortex) compared to consonant smokers. These results suggest that smoking stimuli with a high incentive value (BEGIN-smoking-stimuli) are more appetitive for dissonant than consonant smokers at least on the neural level. To the contrary, smoking stimuli with low incentive value (END-smoking-stimuli) seem to be less appetitive for dissonant smokers than consonant smokers. These differences might be one reason why dissonant smokers experience difficulties in translating their attitudes into an actual behavior change.     

Neural Correlates of Auditory Perceptual Awareness under Informational Masking

Our ability to detect target sounds in complex acoustic backgrounds is often limited not by the ear's resolution, but by the brain's information-processing capacity. The neural mechanisms and loci of this “informational masking” are unknown. We combined magnetoencephalography with simultaneous behavioral measures in humans to investigate neural correlates of informational masking and auditory perceptual awareness in the auditory cortex. Cortical responses were sorted according to whether or not target sounds were detected by the listener in a complex, randomly varying multi-tone background known to produce informational masking. Detected target sounds elicited a prominent, long-latency response (50–250 ms), whereas undetected targets did not. In contrast, both detected and undetected targets produced equally robust auditory middle-latency, steady-state responses, presumably from the primary auditory cortex. These findings indicate that neural correlates of auditory awareness in informational masking emerge between early and late stages of processing within the auditory cortex.     

Failure to detect simian immunodeficiency virus infection in a large Cameroonian cohort with high non-human primate exposure

Hunting and butchering of wildlife in Central Africa are known risk factors for a variety of human diseases, including HIV/AIDS. Due to the high incidence of human exposure to body fluids of non-human primates, the significant prevalence of simian immunodeficiency virus (SIV) in non-human primates, and hunting/butchering associated cross-species transmission of other retroviruses in Central Africa, it is possible that SIV is actively transmitted to humans from primate species other than mangabeys, chimpanzees, and/or gorillas. We evaluated SIV transmission to humans by screening 2,436 individuals that hunt and butcher non-human primates, a population in which simian foamy virus and simian T-lymphotropic virus were previously detected. We identified 23 individuals with high seroreactivity to SIV. Nucleic acid sequences of SIV genes could not be detected, suggesting that SIV infection in humans could occur at a lower frequency than infections with other retroviruses, including simian foamy virus and simian T-lymphotropic virus. Additional studies on human populations at risk for non-human primate zoonosis are necessary to determine whether these results are due to viral/host characteristics or are indicative of low SIV prevalence in primate species consumed as bushmeat as compared to other retroviruses in Cameroon.     

Neural correlates of auditory perceptual awareness under informational masking

Our ability to detect target sounds in complex acoustic backgrounds is often limited not by the ear's resolution, but by the brain's information-processing capacity. The neural mechanisms and loci of this “informational masking” are unknown. We combined magnetoencephalography with simultaneous behavioral measures in humans to investigate neural correlates of informational masking and auditory perceptual awareness in the auditory cortex. Cortical responses were sorted according to whether or not target sounds were detected by the listener in a complex, randomly varying multi-tone background known to produce informational masking. Detected target sounds elicited a prominent, long-latency response (50–250 ms), whereas undetected targets did not. In contrast, both detected and undetected targets produced equally robust auditory middle-latency, steady-state responses, presumably from the primary auditory cortex. These findings indicate that neural correlates of auditory awareness in informational masking emerge between early and late stages of processing within the auditory cortex.     

Bird speech perception and vocal production: a comparison with humans

Research into speech perception by nonhuman animals can be crucially informative in assessing whether specific perceptual phenomena in humans have evolved to decode speech, or reflect more general traits. Birds share with humans not only the capacity to use complex vocalizations for communication but also many characteristics of its underlying developmental and mechanistic processes; thus, birds are a particularly interesting group for comparative study. This review first discusses commonalities between birds and humans in perception of speech sounds. Several psychoacoustic studies have shown striking parallels in seemingly speech-specific perceptual phenomena, such as categorical perception of voice-onset-time variation, categorization of consonants that lack phonetic invariance, and compensation for coarticulation. Such findings are often regarded as evidence for the idea that the objects of human speech perception are auditory or acoustic events rather than articulations. Next, I highlight recent research on the production side of avian communication that has revealed the existence of vocal tract filtering and articulation in bird species-specific vocalization, which has traditionally been considered a hallmark of human speech production. Together, findings in birds show that many of characteristics of human speech perception are not uniquely human but also that a comparative approach to the question of what are the objects of perception--articulatory or auditory events--requires careful consideration of species-specific vocal production mechanisms.     

Follow my eyes: the gaze of politicians reflexively captures the gaze of ingroup voters

Studies in human and non-human primates indicate that basic socio-cognitive operations are inherently linked to the power of gaze in capturing reflexively the attention of an observer. Although monkey studies indicate that the automatic tendency to follow the gaze of a conspecific is modulated by the leader-follower social status, evidence for such effects in humans is meager. Here, we used a gaze following paradigm where the directional gaze of right- or left-wing Italian political characters could influence the oculomotor behavior of ingroup or outgroup voters. We show that the gaze of Berlusconi, the right-wing leader currently dominating the Italian political landscape, potentiates and inhibits gaze following behavior in ingroup and outgroup voters, respectively. Importantly, the higher the perceived similarity in personality traits between voters and Berlusconi, the stronger the gaze interference effect. Thus, higher-order social variables such as political leadership and affiliation prepotently affect reflexive shifts of attention.     

Social Interactions through the Eyes of Macaques and Humans

Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable resources. Observing such social interactions between group members provides individuals with essential information (e.g. on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners. This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore, the monkeys’ gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions. Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying a homologous cognitive mechanism of social attention between rhesus macaques and humans.     

Cortical mechanisms in hearing

Current understanding of neural processing in the auditory cortex has been shaped by a variety of experimental approaches in animals and humans. It remains a daunting challenge to reconcile data as diverse as synaptic properties recorded in a rodent brain slice and functional images of auditory cortex in a behaving human. Nevertheless, the gaps are narrowing through a renewed focus on humans and other primates, a continuing interest in evidence for functional pathways, a broader application of modern imaging techniques, a growing awareness of cortical sensitivity to dynamic features of sounds, and an improved understanding of auditory cortical circuitry.