Auditory–vocal mirroring in songbirds

Mirror neurons are theorized to serve as a neural substrate for spoken language in humans, but the existence and functions of auditory–vocal mirror neurons in the human brain remain largely matters of speculation. Songbirds resemble humans in their capacity for vocal learning and depend on their learned songs to facilitate courtship and individual recognition. Recent neurophysiological studies have detected putative auditory–vocal mirror neurons in a sensorimotor region of the songbird''s brain that plays an important role in expressive and receptive aspects of vocal communication. This review discusses the auditory and motor-related properties of these cells, considers their potential role on song learning and communication in relation to classical studies of birdsong, and points to the circuit and developmental mechanisms that may give rise to auditory–vocal mirroring in the songbird''s brain.     

Individual vocal signatures in barn owl nestlings: does individual recognition have an adaptive role in sibling vocal competition?

To compete over limited parental resources, young animals communicate with their parents and siblings by producing honest vocal signals of need. Components of begging calls that are sensitive to food deprivation may honestly signal need, whereas other components may be associated with individual‐specific attributes that do not change with time such as identity, sex, absolute age and hierarchy. In a sib–sib communication system where barn owl (Tyto alba) nestlings vocally negotiate priority access to food resources, we show that calls have individual signatures that are used by nestlings to recognize which siblings are motivated to compete, even if most vocalization features vary with hunger level. Nestlings were more identifiable when food‐deprived than food‐satiated, suggesting that vocal identity is emphasized when the benefit of winning a vocal contest is higher. In broods where siblings interact iteratively, we speculate that individual‐specific signature permits siblings to verify that the most vocal individual in the absence of parents is the one that indeed perceived the food brought by parents. Individual recognition may also allow nestlings to associate identity with individual‐specific characteristics such as position in the within‐brood dominance hierarchy. Calls indeed revealed age hierarchy and to a lower extent sex and absolute age. Using a cross‐fostering experimental design, we show that most acoustic features were related to the nest of origin (but not the nest of rearing), suggesting a genetic or an early developmental effect on the ontogeny of vocal signatures. To conclude, our study suggests that sibling competition has promoted the evolution of vocal behaviours that signal not only hunger level but also intrinsic individual characteristics such as identity, family, sex and age.     

Quantitative assessment of song-selectivity in the zebra finch “high vocal center”

1. Auditory responses in the zebra finch (Taenopygia guttata) song-system nucleus HVc were assessed at 54 recording sites by 3 different methods: discriminated action potentials; excitatory summed responses; and excitatory minus inhibitory summed responses. Four standard stimuli were presented at each site: the bird's own song; this song reversed; a conspecific song; and a noise burst. Responses were quantified by calculating a relative response index that partitioned the response, to provide a response profile, across the stimuli.
2. Regardless of analysis method, the strongest response was most often to the bird's own song (78–82%, depending on method). The predominant rank order of response strength across the remaining three stimuli was conspecific song > reversed song > noise.
3. The distribution of relative response magnitude was sensitive to analysis method. Discriminated spikes captured the heterogeneity of HVc neurons, whereas the excitatory summed responses reflected the overall trends more consistently. When inhibition was subtracted from excitation in the summed responses, the variance of the relative responses increased, but this method presented some problems for statistical analysis.
4. A small sample of neurons in other forebrain auditory areas was used for comparative analyses. At these recording sites, the bird's own song did not consistently elicit the best response and there were generally smaller differences in the relative responses to the four stimuli. The smaller degree of stimulus selectivity among these cells resulted in less sensitivity to differences in the assessment methods.

     

Does vocal learning accelerate acoustic diversification? Evolution of contact calls in Neotropical parrots

Learning has been traditionally thought to accelerate the evolutionary change of behavioural traits. We evaluated the evolutionary rate of learned vocalizations and the interplay of morphology and ecology in the evolution of these signals. We examined contact calls of 51 species of Neotropical parrots from the tribe Arini. Parrots are ideal subjects due to their wide range of body sizes and habitats, and their open‐ended vocal learning that allows them to modify their calls throughout life. We estimated the evolutionary rate of acoustic parameters of parrot contact calls and compared them to those of morphological traits and habitat. We also evaluated the effect of body mass, bill length, vegetation density and species interactions on acoustic parameters of contact calls while controlling for phylogeny. Evolutionary rates of acoustic parameters did not differ from those of our predictor variables except for spectral entropy, which had a significantly slower rate of evolution. We found support for correlated evolution of call duration, and fundamental and peak frequencies with body mass, and of fundamental frequency with bill length. The degree of sympatry between species did not have a significant effect on acoustic parameters. Our results suggest that parrot contact calls, which are learned acoustic signals, show evolutionary rates similar to those of morphological traits. This is the first study to our knowledge to provide evidence that change through cultural evolution does not necessarily accelerate the evolutionary rate of traits acquired through life‐long vocal learning.     

Does age matter in song bird vocal interactions? Results from interactive playback experiments

The song of oscines provides an extensively studied model of age-dependent behaviour changes. Male and female receivers might use song characteristics to obtain information about the age of a signaller, which is often related to its quality. Whereas most of the age-dependent song changes have been studied in solo singing, the role of age in vocal interactions is less well understood. We addressed this issue in a playback study with common nightingales (Luscinia megarhynchos). Previous studies showed that male nightingales had smaller repertoires in their first year than older males and males adjusted their repertoire towards the most common songs in the breeding population. We now compared vocal interaction patterns in a playback study in 12 one year old and 12 older nightingales (cross-sectional approach). Five of these males were tested both in their first and second breeding season (longitudinal approach). Song duration and latency to respond did not differ between males of different ages in either approach. In the cross-sectional approach, one year old nightingales matched song types twice as often as did older birds. Similarly, in the longitudinal approach all except one bird reduced the number of song type matches in their second season. Individuals tended to overlap songs at higher rates in their second breeding season than in their first. The higher levels of song type matches in the first year and song overlapping by birds in their second year suggest that these are communicative strategies to establish relationships with competing males and/or choosy females.     

Are vocal characteristics related to leadership patterns in mixed‐species bird flocks?

What structures the organization of mixed‐species bird flocks, so that some ‘nuclear’ species lead the flocks, and others follow? Previous research has shown that species actively listen to each other, and that leaders are gregarious; such gregarious species tend to make contact calls and hence may be vocally conspicuous. Here we investigated whether vocal characteristics are associated with leadership, using a global dataset of mixed‐species flock studies and recordings from sound archives. We first asked whether leaders are different from following or occasional species in flocks in the proportion of the recordings that contain calls (n = 58 flock studies, 145 species), and especially alarm calls (n = 111 species). We found that leaders tended to have a higher proportion of their vocalizations that were classified as calls than occasional species, and both leaders and following species had a significantly higher proportion of their calls rated as alarms compared to occasional species. Next, we investigated the acoustic characteristics of flock participants’ calls, hypothesizing that leaders would make more calls, and have less silence on the recordings. We also hypothesized that leaders’ calls would be simple acoustically, as contact calls tend to be, and thus similar to each other, as well as being detectable, in being low frequency and with high frequence bandwidth. The analysis (n = 45 species, 169 recordings) found that only one of these predictions was supported: leading species were less often silent than following or occasional species. Unexpectedly, leaders’ calls were less similar to each other than occasional species. The greater amount of information available and the greater variety of that information support the hypothesis that leadership in flocks is related to vocal communication. We highlight the use of sound archives to ask questions about behavioral and community ecology, while acknowledging some limitations of such studies.     

Primate vocal communication: a useful tool for understanding human speech and language evolution?

Language is a uniquely human trait, and questions of how and why it evolved have been intriguing scientists for years. Nonhuman primates (primates) are our closest living relatives, and their behavior can be used to estimate the capacities of our extinct ancestors. As humans and many primate species rely on vocalizations as their primary mode of communication, the vocal behavior of primates has been an obvious target for studies investigating the evolutionary roots of human speech and language. By studying the similarities and differences between human and primate vocalizations, comparative research has the potential to clarify the evolutionary processes that shaped human speech and language. This review examines some of the seminal and recent studies that contribute to our knowledge regarding the link between primate calls and human language and speech. We focus on three main aspects of primate vocal behavior: functional reference, call combinations, and vocal learning. Studies in these areas indicate that despite important differences, primate vocal communication exhibits some key features characterizing human language. They also indicate, however, that some critical aspects of speech, such as vocal plasticity, are not shared with our primate cousins. We conclude that comparative research on primate vocal behavior is a very promising tool for deepening our understanding of the evolution of human speech and language, but much is still to be done as many aspects of monkey and ape vocalizations remain largely unexplored.     

Are there vocal cues to human developmental stability? Relationships between facial fluctuating asymmetry and voice attractiveness

Fluctuating asymmetry (FA), deviation from perfect bilateral symmetry, is thought to reflect an organism's relative inability to maintain stable morphological development in the face of environmental and genetic stressors. Previous research has documented negative relationships between FA and attractiveness judgments in humans, but scant research has explored relationships between the human voice and this putative marker of genetic quality in either sex. Only one study (and in women only) has explored relationships between vocal attractiveness and asymmetry of the face, a feature-rich trait space central in prior work on human genetic quality and mate choice. We therefore examined this relationship in three studies comprising 231 men and 240 women from two Western samples as well as Hadza hunter–gatherers of Tanzania. Voice recordings were collected and rated for attractiveness, and FA was computed from two-dimensional facial images as well as, for a subset of men, three-dimensional facial scans. Through meta-analysis of our results and those of prior studies, we found a negative association between FA and vocal attractiveness that was highly robust and statistically significant whether we included effect sizes from previously published work, or only those from the present research, and regardless of the inclusion of any individual sample or method of assessing FA (e.g., facial or limb FA). Weighted mean correlations between FA and vocal attractiveness across studies were ?.23 for men and ?.29 for women. This research thus offers strong support for the hypothesis that voices provide cues to genetic quality in humans.     

Midbrain auditory sensitivity in toads of the genus Bufo (amphibia — bufonidae) with different vocal repertoires

Summary South American male toads Bufo chilensis emit a release call in contact with other individuals and a soft amplectic call, B. spinulosus males emit a release call while isolated in breeding areas, and B. arenarum produces a release call plus an intense mating call. Release calls of the 3 species measure 72–86 dB SPL RMS at 20 cm in front of the animal and the mating call of B. arenarum is 84–87 dB SPL at 4 m.Audiograms obtained with multiunit recordings in the torus semicircularis (TS) show a low frequency region (LFR), centered at 352, 356 and 491 Hz, and a high frequency region (HFR), centered at 1199, 1161 and 1423 Hz, in B. chilensis, B. spinulosus and B. arenarum, respectively. Center frequencies (CFs) in the HFR are in gross correspondence with average dominant frequencies (DFs) of the vocalizations of these species. Best thresholds (BTs) in the HFR are similar between B. chilensis and B. arenarum while in B. spinulosus average BTs are 10.8 and 13.5 dB higher, respectively. The similar auditory thresholds between B. chilensis and B. arenarum denote a conservative nature of auditory sensitivity among these anura.Abbreviations AP amphibian papilla - BP basilar papilla - BT best threshold - CF center frequency - DF dominant frequency - HFR high frequency region - LFR low frequency region - TS torus semi-circularis - SPL sound pressure level     

La parole à la portée du conduit vocal de l'homme de Neandertal. Nouvelles recherches,nouvelles perspectives

Investigations about the origin of articulated language result in different interpretations dealing with the phonetic capacity of our ancestors, namely after the discovery of the Neandertals. According to anatomic arguments now called to question, principally the position of the larynx as regard to the basis of skull, some authors claimed that these fossil humans could not be endowed with speech. From a new reconstruction of the estimated position of the larynx and the vocal tract, articulatory simulations were undertaken in order to propose some potential vocalic [i a u] prototypes for Neandertals. And we can show Neandertals could pronounce vowels as differentiated as those of modern humans. To cite this article: J.-L. Heim et al., C. R. Palevol 1 (2002) 129–134.     

Is the nominate subspecies of the common crossbill Loxia c. curvirostra polytypic? II. Differentiation among vocal types in functional traits

Vocally differentiated common crossbill Loxia curvirostra populations ('vocal types') in North America show a high degree of morphological and ecological specialization coupled with significant genetic differentiation and appreciable levels of assortative mating in sympatry. Similar vocally differentiated common crossbill vocal types have recently also been uncovered in Europe. These vocal types frequently overlap in space and time, and preliminary data indicate strong assortatively mating in sympatry. These observations suggest that the European nominate subspecies also consists of several independent evolutionary lineages, but so far morphological and ecological support for this view has been lacking. Bill morphology of crossbills is tightly linked to resource use, and we earlier showed that average morphology (of birds of unknown vocal type) indeed differed among years, consistent with the possibility that vocal types are morphologically differentiated if the proportion of each type caught varies among years. Here we test specifically for morphological differences between birds assigned to vocal type, at two sites and during two independent influxes. Differentiation between the two vocal types studied is highly significant, with the same pattern uncovered at each site and for each influx. Of eight traits investigated, in both univariate and multivariate analyses, the trait that differs most between the two types is the ecologically important bill depth. The difference in average bill depth between these two European vocal types (0.26 mm) is equivalent to the difference between some ecologically specialised North American vocal types. These results provide further evidence that the nominate subspecies of the common crossbill consists of several ecologically distinct populations, if not cryptic species.     

Call types of Bigg’s killer whales (Orcinus orca) in western Alaska: using vocal dialects to assess population structure

Bigg’s killer whales (Orcinus orca; i.e. ‘transient’ ecotype), as apex predators, are important to the dynamics of marine ecosystems, but little is known about their population structure in western Alaska. Currently, all Bigg’s killer whales in western Alaska are ascribed to a single broad stock for management under the US Marine Mammal Protection Act. However, recent nuclear microsatellite and mitochondrial DNA analyses indicate that this stock is likely comprised of genetically distinct sub-populations. In accordance with what is known about killer whale vocal dialects in other locations, we used the spatial distribution of group-specific call types to investigate the population structure of Bigg’s killer whales in this part of Alaska. Digital audio recordings were collected from 33 Bigg’s killer whale encounters throughout the Aleutian and Pribilof Islands in the summers of 2001–2007 and 2009–2010. Recorded calls were qualitatively classified into discrete types and then quantitatively described using 12 structural and time-frequency measures. Resulting call categories were validated using a random forest approach. A total of 36 call types and subtypes were identified across the entire study area, and regional patterns of call type use revealed three distinct dialects which correspond to proposed genetic delineations. Our results suggest that there are at least three acoustically and genetically distinct sub-populations in western Alaska, and we present an initial catalogue for this area describing the regional vocal repertoires of Bigg’s killer whale call types.