Human cerebral response to animal affective vocalizations

It is presently unknown whether our response to affective vocalizations is specific to those generated by humans or more universal, triggered by emotionally matched vocalizations generated by other species. Here, we used functional magnetic resonance imaging in normal participants to measure cerebral activity during auditory stimulation with affectively valenced animal vocalizations, some familiar (cats) and others not (rhesus monkeys). Positively versus negatively valenced vocalizations from cats and monkeys elicited different cerebral responses despite the participants' inability to differentiate the valence of these animal vocalizations by overt behavioural responses. Moreover, the comparison with human non-speech affective vocalizations revealed a common response to the valence in orbitofrontal cortex, a key component on the limbic system. These findings suggest that the neural mechanisms involved in processing human affective vocalizations may be recruited by heterospecific affective vocalizations at an unconscious level, supporting claims of shared emotional systems across species.     

REPRODUCTIVE BEHAVIOR OF FEMALE BUNTINGS: ISOLATING MECHANISMS IN A HYBRIDIZING PAIR OF SPECIES

The plumage characteristics of male Indigo and Lazuli Buntings are distinct, but the two species can learn each other's songs. Populations comprising Indigo, Lazuli and hybrid individuals occur in the Great Plains of North America, and assortative mating has been inferred from morphometric data. We devised a laboratory assay for determining female preferences for visual and vocal characteristics of conspecific and heterospecific males and for mixtures of these characteristics, such as might be encountered in an overlap population. Females of both species gave more copulation-solicitation displays when exposed to conspecific plumage and vocalizations than when exposed to heterospecific plumage and vocalizations. Females gave intermediate and similar responses to the combinations of conspecific plumage with heterospecific vocalizations and heterospecific plumage with conspecific vocalizations. Thus, in the absence of other potentially important variables, female reproductive behavior is consistent with the hypothesis of assortative mating, based upon both vocal and visual traits of the males and caused by female choice in this semispecies pair.     

Reading faces: differential lateral gaze bias in processing canine and human facial expressions in dogs and 4-year-old children

Sensitivity to the emotions of others provides clear biological advantages. However, in the case of heterospecific relationships, such as that existing between dogs and humans, there are additional challenges since some elements of the expression of emotions are species-specific. Given that faces provide important visual cues for communicating emotional state in both humans and dogs, and that processing of emotions is subject to brain lateralisation, we investigated lateral gaze bias in adult dogs when presented with pictures of expressive human and dog faces. Our analysis revealed clear differences in laterality of eye movements in dogs towards conspecific faces according to the emotional valence of the expressions. Differences were also found towards human faces, but to a lesser extent. For comparative purpose, a similar experiment was also run with 4-year-old children and it was observed that they showed differential processing of facial expressions compared to dogs, suggesting a species-dependent engagement of the right or left hemisphere in processing emotions.     

Territorial vocalization in sympatric damselfish: acoustic characteristics and intruder discrimination

Damselfishes are well known for their aggressive, territorial behaviour during which the use of vocalization behaviour has been well documented. However, agonistic acoustic signalling has been understudied in particular when the vocalizations are interspecific. In this study, we characterize and compare the previously undescribed vocalization behaviour of longfin damselfish (Stegastes diencaeus), in an agonistic context, with the closely related and sympatric dusky damselfish (Stegastes adustus). Next, we examined if these congeneric species modulate their vocalizations in a similar pattern to previously described aggressive behaviour patterns. Audio field recordings of territorial males were obtained in response to three separate stimuli: (1) conspecific male damselfish, (2) heterospecific male damselfish and (3) a common intruder, the slippery dick wrasse (Halichoeres bivittatus). The vocal repertoires of both longfin and dusky damselfish comprised the same three distinct call types: chirps, pops and pulse trains. However, temporal measures of the calls showed significant differences between species. Additionally, dusky damselfish were more vocal overall, producing more calls and spending more time calling than longfin damselfish. These responses were stimulus and species dependent, as the two species modulated acoustic response by modulating pulse number based on intruder species. These results suggest that these closely related species of damselfish use vocalization behaviours that are both unique and context dependent.     

An Automated Procedure for Evaluating Song Imitation

Songbirds have emerged as an excellent model system to understand the neural basis of vocal and motor learning. Like humans, songbirds learn to imitate the vocalizations of their parents or other conspecific “tutors.” Young songbirds learn by comparing their own vocalizations to the memory of their tutor song, slowly improving until over the course of several weeks they can achieve an excellent imitation of the tutor. Because of the slow progression of vocal learning, and the large amounts of singing generated, automated algorithms for quantifying vocal imitation have become increasingly important for studying the mechanisms underlying this process. However, methodologies for quantifying song imitation are complicated by the highly variable songs of either juvenile birds or those that learn poorly because of experimental manipulations. Here we present a method for the evaluation of song imitation that incorporates two innovations: First, an automated procedure for selecting pupil song segments, and, second, a new algorithm, implemented in Matlab, for computing both song acoustic and sequence similarity. We tested our procedure using zebra finch song and determined a set of acoustic features for which the algorithm optimally differentiates between similar and non-similar songs.     

Differential Response to Interspecific and Intraspecific Signals Amongst Chickadees

Black‐capped chickadees (Poecile atricapillus) and mountain chickadees (P. gambeli) have a similar vocal repertoire and share many other life history traits; yet, black‐capped chickadees are socially dominant to mountain chickadees where populations overlap. Previous research suggested that in contact zones, both species respond weakly to heterospecific songs during the breeding season, and have suggested minimal interspecific competition. However, both black‐capped and mountain chickadees discriminate between conspecific and heterospecific chick‐a‐dee calls, suggesting attention is paid to interspecific signals. We compared the responses of both black‐capped and mountain chickadees to conspecific and heterospecific chick‐a‐dee calls during the winter, when both species compete for the same food resources. We conducted an aviary playback experiment exposing both species to playback composed of heterospecific and conspecific chick‐a‐dee calls, which had been recorded in the context of finding food sources. Responses from the tested birds were measured by recording vocalizations and behaviour. Black‐capped chickadees responded significantly more to conspecific than to heterospecific stimuli, whereas the subordinate mountain chickadees responded to both mountain and black‐capped chickadee calls. Based upon the reactions to playbacks, our results suggest these two closely related species may differ in their perception of the relative threat associated with intra‐ versus interspecific competitors.     

Neural mechanisms of auditory species recognition in birds

Auditory communication in humans and other animals frequently takes place in noisy environments with many co‐occurring signallers. Receivers are thus challenged to rapidly recognize salient auditory signals and filter out irrelevant sounds. Most bird species produce a variety of complex vocalizations that function to communicate with other members of their own species and behavioural evidence broadly supports preferences for conspecific over heterospecific sounds (auditory species recognition). However, it remains unclear whether such auditory signals are categorically recognized by the sensory and central nervous system. Here, we review 53 published studies that compare avian neural responses between conspecific versus heterospecific vocalizations. Irrespective of the techniques used to characterize neural activity, distinct nuclei of the auditory forebrain are consistently shown to be repeatedly conspecific selective across taxa, even in response to unfamiliar individuals with distinct acoustic properties. Yet, species‐specific neural discrimination is not a stereotyped auditory response, but is modulated according to its salience depending, for example, on ontogenetic exposure to conspecific versus heterospecific stimuli. Neuromodulators, in particular norepinephrine, may mediate species recognition by regulating the accuracy of neuronal coding for salient conspecific stimuli. Our review lends strong support for neural structures that categorically recognize conspecific signals despite the highly variable physical properties of the stimulus. The available data are in support of a ‘perceptual filter’‐based mechanism to determine the saliency of the signal, in that species identity and social experience combine to influence the neural processing of species‐specific auditory stimuli. Finally, we present hypotheses and their testable predictions, to propose next steps in species‐recognition research into the emerging model of the neural conceptual construct in avian auditory recognition.     

Perceptual salience of acoustic differences between conspecific and allospecific vocalizations in African collared-doves

In speciation events, species-distinct vocal signals can diverge acoustically in many ways. Signal receivers have to be able to distinguish conspecific from allospecific vocalizations, and the perceptual salience of acoustic features is therefore expected to be an important factor in the evolution of such vocalizations. We tested how dissimilar the species-identifying perch-coos of 12 closely related turtle-dove species (genus Streptopelia) are, as perceived by one of its members, S. roseogrisea. With operant, psychoacoustic methods we trained six doves to respond only to their conspecific coo. Responses to the perch-coos of the 12 other dove species were used as a measure of their perceptual similarity to conspecific perch-coos. Turtle-doves differentiated between the allospecific coos: some were perceived as more similar to their own species' coo than others. With multiple regression analysis we identified three acoustic features that correlated with these differences in perceptual similarity: coo duration, minimum frequency and Wiener entropy. In contrast to findings in other bird species, duration was by far the most important feature in the discrimination between conspecific and allospecific vocalizations for S. roseogrisea. The results suggest that this is due not only to the coos of the various species differing in duration but also to a comparatively high perceptibility of the differences in duration. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Cues for Early Discrimination of Conspecific Song in the White-Crowned Sparrow (Zonotrichia leucophrys)

In song learning, white-crowned sparrows ( Zonotrichia leucophrys ) begin memorizing conspecific song models at around 20 d of age. Even prior to song memorization, however, between 10 and 20 d of age, these birds respond differently to playbacks of conspecific and heterospecific songs. To investigate the acoustic cues underlying this early song discrimination, we measured the vocal responses of newly fledged young to playbacks of modified conspecific and heterospecific songs. Fledgling white-crowned sparrows responded more strongly to songs containing conspecific notes than to songs containing notes from other species. In contrast, the presence or placement of an introductory whistle, present in all white-crowned sparrow songs, did not affect response levels. A whistle has previously been shown to serve as an acoustic cue for song memorization and production in this species. Such different responses to the species-typical introductory whistle at different stages suggests that developmental changes occur in the template system underlying song learning, the factors governing song recognition, or both.     

Red deer stags use formants as assessment cues during intrasexual agonistic interactions

While vocal tract resonances or formants are key acoustic parameters that define differences between phonemes in human speech, little is known about their function in animal communication. Here, we used playback experiments to present red deer stags with re-synthesized vocalizations in which formant frequencies were systematically altered to simulate callers of different body sizes. In response to stimuli where lower formants indicated callers with longer vocal tracts, stags were more attentive, replied with more roars and extended their vocal tracts further in these replies. Our results indicate that mammals other than humans use formants in vital vocal exchanges and can adjust their own formant frequencies in relation to those that they hear.     

Developmental experience alters information coding in auditory midbrain and forebrain neurons

In songbirds, species identity and developmental experience shape vocal behavior and behavioral responses to vocalizations. The interaction of species identity and developmental experience may also shape the coding properties of sensory neurons. We tested whether responses of auditory midbrain and forebrain neurons to songs differed between species and between groups of conspecific birds with different developmental exposure to song. We also compared responses of individual neurons to conspecific and heterospecific songs. Zebra and Bengalese finches that were raised and tutored by conspecific birds, and zebra finches that were cross‐tutored by Bengalese finches were studied. Single‐unit responses to zebra and Bengalese finch songs were recorded and analyzed by calculating mutual information (MI), response reliability, mean spike rate, fluctuations in time‐varying spike rate, distributions of time‐varying spike rates, and neural discrimination of individual songs. MI quantifies a response's capacity to encode information about a stimulus. In midbrain and forebrain neurons, MI was significantly higher in normal zebra finch neurons than in Bengalese finch and cross‐tutored zebra finch neurons, but not between Bengalese finch and cross‐tutored zebra finch neurons. Information rate differences were largely due to spike rate differences. MI did not differ between responses to conspecific and heterospecific songs. Therefore, neurons from normal zebra finches encoded more information about songs than did neurons from other birds, but conspecific and heterospecific songs were encoded equally. Neural discrimination of songs and MI were highly correlated. Results demonstrate that developmental exposure to vocalizations shapes the information coding properties of songbird auditory neurons. © 2009 Wiley Periodicals, Inc. Develop Neurobiol 70: 235–252, 2010.     

Acoustic parameters of dog barks carry emotional information for humans

In an earlier study, we found that humans were able to categorize dog barks correctly, which were recorded in various situations. The acoustic parameters, like tonality, pitch and inter-bark time intervals, seemed to have a strong effect on how human listeners described the emotionality of these dog vocalisations. In this study, we investigated if the effect of the acoustic parameters of the dog bark is the same on the human listeners as we would expect it from studies in other mammalian species (for example, low, hoarse sounds indicating aggression; high pitched, tonal sounds indicating subordinance/fear). People with different experience with dogs were asked to describe the emotional content of several artificially assembled bark sequences on the basis of five emotional states (aggressiveness, fear, despair, playfulness, happiness). The selection of the barks was based on low, medium and high values of tonality and peak frequency. For assembling artificial bark sequences, we used short, middle or long inter-bark intervals. We found that humans with different levels of experience with dogs described the emotional content of the bark sequences quite similarly, and the extent of previous experience with the given breed (Mudi), or with dogs in general, did not cause characteristic differences in the emotionality scores. The scoring of the emotional content of the bark sequences was in accordance with the so-called Morton's structural–acoustic rules. Thus, low pitched barks were described as aggressive, and tonal and high pitched barks were scored as either fearful or desperate, but always without aggressiveness. In general, tonality of the bark sequence had much less effect than the pitch of the sounds. We found also that the inter-bark intervals had a strong effect on the emotionality of dog barks for the human listeners: bark sequences with short inter-bark intervals were scored as aggressive, but bark sequences with longer inter-bark intervals were scored with low values of aggression. High pitched bark sequences with long inter-bark intervals were considered happy and playful, independently from their tonality. These findings show that dog barks function as predicted by the structural–motivational rules developed for acoustic signals in other species, suggesting that dog barks may present a functional system for communication at least in the dog–human relationship. In sum it seems that many types of different emotions can be expressed with the variation of at least three acoustic parameters.     

Of Mice,Birds, and Men: The Mouse Ultrasonic Song System Has Some Features Similar to Humans and Song-Learning Birds

Humans and song-learning birds communicate acoustically using learned vocalizations. The characteristic features of this social communication behavior include vocal control by forebrain motor areas, a direct cortical projection to brainstem vocal motor neurons, and dependence on auditory feedback to develop and maintain learned vocalizations. These features have so far not been found in closely related primate and avian species that do not learn vocalizations. Male mice produce courtship ultrasonic vocalizations with acoustic features similar to songs of song-learning birds. However, it is assumed that mice lack a forebrain system for vocal modification and that their ultrasonic vocalizations are innate. Here we investigated the mouse song system and discovered that it includes a motor cortex region active during singing, that projects directly to brainstem vocal motor neurons and is necessary for keeping song more stereotyped and on pitch. We also discovered that male mice depend on auditory feedback to maintain some ultrasonic song features, and that sub-strains with differences in their songs can match each other''s pitch when cross-housed under competitive social conditions. We conclude that male mice have some limited vocal modification abilities with at least some neuroanatomical features thought to be unique to humans and song-learning birds. To explain our findings, we propose a continuum hypothesis of vocal learning.     

Eavesdropping on the Neighbourhood: Collared Pika (Ochotona collaris) Responses to Playback Calls of Conspecifics and Heterospecifics

The acoustic environment, composed in part by the vocalizations of sympatric animals, is a major source of information and can be used to fine-tune behavioural decisions. Active assessment of alarm calls within and between mammal species is not fully understood. We explored the behavioural responses of collared pikas to con- and heterospecific vocalizations, in order to determine whether they selectively attend to these calls. Pikas increased their vigilance after playback of alarm calls of heterospecific mammals (marmots and ground squirrels), but responded most strongly to conspecific calls. While responses to playback calls of their own, of neighbours and of a stranger did not differ, pikas did discriminate between individual callers in a habituation-discrimination experiment. The ability to make use of information from different sources in their acoustic environment likely facilitates pikas' behavioural decisions that affect foraging, predator avoidance and nepotism.     

Comparison of Neural Responses to Cat Meows and Human Vowels in the Anterior and Posterior Auditory Field of Awake Cats

For humans and animals, the ability to discriminate speech and conspecific vocalizations is an important physiological assignment of the auditory system. To reveal the underlying neural mechanism, many electrophysiological studies have investigated the neural responses of the auditory cortex to conspecific vocalizations in monkeys. The data suggest that vocalizations may be hierarchically processed along an anterior/ventral stream from the primary auditory cortex (A1) to the ventral prefrontal cortex. To date, the organization of vocalization processing has not been well investigated in the auditory cortex of other mammals. In this study, we examined the spike activities of single neurons in two early auditory cortical regions with different anteroposterior locations: anterior auditory field (AAF) and posterior auditory field (PAF) in awake cats, as the animals were passively listening to forward and backward conspecific calls (meows) and human vowels. We found that the neural response patterns in PAF were more complex and had longer latency than those in AAF. The selectivity for different vocalizations based on the mean firing rate was low in both AAF and PAF, and not significantly different between them; however, more vocalization information was transmitted when the temporal response profiles were considered, and the maximum transmitted information by PAF neurons was higher than that by AAF neurons. Discrimination accuracy based on the activities of an ensemble of PAF neurons was also better than that of AAF neurons. Our results suggest that AAF and PAF are similar with regard to which vocalizations they represent but differ in the way they represent these vocalizations, and there may be a complex processing stream between them.     

Two organizing principles of vocal production: Implications for nonhuman and human primates

Vocal communication in nonhuman primates receives considerable research attention, with many investigators arguing for similarities between this calling and speech in humans. Data from development and neural organization show a central role of affect in monkey and ape sounds, however, suggesting that their calls are homologous to spontaneous human emotional vocalizations while having little relation to spoken language. Based on this evidence, we propose two principles that can be useful in evaluating the many and disparate empirical findings that bear on the nature of vocal production in nonhuman and human primates. One principle distinguishes production-first from reception-first vocal development, referring to the markedly different role of auditory-motor experience in each case. The second highlights a phenomenon dubbed dual neural pathways, specifically that when a species with an existing vocal system evolves a new functionally distinct vocalization capability, it occurs through emergence of a second parallel neural pathway rather than through expansion of the extant circuitry. With these principles as a backdrop, we review evidence of acoustic modification of calling associated with background noise, conditioning effects, audience composition, and vocal convergence and divergence in nonhuman primates. Although each kind of evidence has been interpreted to show flexible cognitively mediated control over vocal production, we suggest that most are more consistent with affectively grounded mechanisms. The lone exception is production of simple, novel sounds in great apes, which is argued to reveal at least some degree of volitional vocal control. If also present in early hominins, the cortically based circuitry surmised to be associated with these rudimentary capabilities likely also provided the substrate for later emergence of the neural pathway allowing volitional production in modern humans.     

Affective responses in tamarins elicited by species-specific music

Theories of music evolution agree that human music has an affective influence on listeners. Tests of non-humans provided little evidence of preferences for human music. However, prosodic features of speech (‘motherese’) influence affective behaviour of non-verbal infants as well as domestic animals, suggesting that features of music can influence the behaviour of non-human species. We incorporated acoustical characteristics of tamarin affiliation vocalizations and tamarin threat vocalizations into corresponding pieces of music. We compared music composed for tamarins with that composed for humans. Tamarins were generally indifferent to playbacks of human music, but responded with increased arousal to tamarin threat vocalization based music, and with decreased activity and increased calm behaviour to tamarin affective vocalization based music. Affective components in human music may have evolutionary origins in the structure of calls of non-human animals. In addition, animal signals may have evolved to manage the behaviour of listeners by influencing their affective state.     

Stimulatory effects on the reproductive axis in female songbirds by conspecific and heterospecific male song

Courtship vocalizations of male songbirds can profoundly enhance the reproductive physiology and behavior of conspecific females. However, no study has fully investigated the selectivity of conspecific song effects on reproductive development in birds. We studied the effects of conspecific and heterospecific song on reproductive development in domesticated (canaries) and wild songbirds (song sparrows). As expected, conspecific song enhanced follicular development. Unexpectedly, however, birds exposed to heterospecific song also underwent enhanced follicular development (compared to birds exposed to no song); conspecific and heterospecific songs were equally effective in enhancing ovarian development. In canaries exposed to 18L:6D, conspecific song induced oviposition earlier and at a greater frequency than in heterospecific and no song groups, with the fewest eggs being laid in the no song group. These results indicate that conspecific and heterospecific male song can enhance reproductive activity in female songbirds. Whether or not activation of the reproductive axis in female songbirds by heterospecific song occurs in the wild remains unclear. It is also unclear as to whether the ability of the reproductive axis to respond to heterospecific song performs a specific function, or whether it is simply a consequence of greater selection pressure acting upon behavioral responses to song.     

Vocal convergence in a multi-level primate society: insights into the evolution of vocal learning

The extent to which nonhuman primate vocalizations are amenable to modification through experience is relevant for understanding the substrate from which human speech evolved. We examined the vocal behaviour of Guinea baboons, Papio papio, ranging in the Niokolo Koba National Park in Senegal. Guinea baboons live in a multi-level society, with units nested within parties nested within gangs. We investigated whether the acoustic structure of grunts of 27 male baboons of two gangs varied with party/gang membership and genetic relatedness. Males in this species are philopatric, resulting in increased male relatedness within gangs and parties. Grunts of males that were members of the same social levels were more similar than those of males in different social levels (N = 351 dyads for comparison within and between gangs, and N = 169 dyads within and between parties), but the effect sizes were small. Yet, acoustic similarity did not correlate with genetic relatedness, suggesting that higher amounts of social interactions rather than genetic relatedness promote the observed vocal convergence. We consider this convergence a result of sensory–motor integration and suggest this to be an implicit form of vocal learning shared with humans, in contrast to the goal-directed and intentional explicit form of vocal learning unique to human speech acquisition.     

Representation of complex vocalizations in the Lusitanian toadfish auditory system: evidence of fine temporal,frequency and amplitude discrimination

Many fishes rely on their auditory skills to interpret crucial information about predators and prey, and to communicate intraspecifically. Few studies, however, have examined how complex natural sounds are perceived in fishes. We investigated the representation of conspecific mating and agonistic calls in the auditory system of the Lusitanian toadfish Halobatrachus didactylus, and analysed auditory responses to heterospecific signals from ecologically relevant species: a sympatric vocal fish (meagre Argyrosomus regius) and a potential predator (dolphin Tursiops truncatus). Using auditory evoked potential (AEP) recordings, we showed that both sexes can resolve fine features of conspecific calls. The toadfish auditory system was most sensitive to frequencies well represented in the conspecific vocalizations (namely the mating boatwhistle), and revealed a fine representation of duration and pulsed structure of agonistic and mating calls. Stimuli and corresponding AEP amplitudes were highly correlated, indicating an accurate encoding of amplitude modulation. Moreover, Lusitanian toadfish were able to detect T. truncatus foraging sounds and A. regius calls, although at higher amplitudes. We provide strong evidence that the auditory system of a vocal fish, lacking accessory hearing structures, is capable of resolving fine features of complex vocalizations that are probably important for intraspecific communication and other relevant stimuli from the auditory scene.