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.     

Vocal coordination of troop movement among white-faced capuchin monkeys,Cebus capucinus

Coordinated travel by social groups is well documented, often with evidence that cognitive spatial maps are employed. Yet the mechanisms by which movement decisions are made and implemented within social groups are poorly known. In a field study of white-faced capuchin monkeys in Costa Rica it was demonstrated that a specific call, the “trill,” is used by adults in the initiation and directing of troop movement. The trills of subadults were restricted to vocal exchanges with other subadults. Continuous vocal recordings were collected of the vocalizations of the 14 members of the study troop. A cumulative 33.7 h of continuous samples and 1,892 sonagrams were analyzed. In addition to vocalizations clearly associated with alarm, distress, or agonistic contexts, two distinct call types were identified, trills and huhs. Age-sex classes differed in the rate at which both types of calls were produced in different spatial positions within the troop. Adult females and males produced higher rates of trills when in the leading edge compared to all other spatial positions in a traveling troop. Trills at the edge of a stationary troop represented 36 “successful” and 3 “unsuccessful” start attempts; the troop usually moved in the trajectory predicted by a trilling adult's location on the troop periphery within 10 min of the initiation of trilling. Adults also altered the trajectory of traveling troops by trilling at the side and back of the troop (10 “successful” and 4 “unsuccessful” attempts). Huh vocalizations were most predictably produced when a capuchin is in a dense fruit patch. These results emphasize the role vocalizations serve in the coordination and trajectory of group movement in nonhuman primates, especially those populations that are arboreal or in which visual contact is otherwise impeded. © 1993 Wiley-Liss, Inc.

1 This article is a US Government work and, as such, is in the public domain in the United States of America.

     

The influence of stationary auditory fields on postural sway behaviour in man

Postural sway behaviour was investigated in 30 young subjects (15 male and 15 female) during 60 s of erect standing, under various combinations of auditory and visual input. Sway was assessed using a standard biomechanical measuring platform, the output of which led directly to an online computer from which the following parameters were determined: mean lateral and antero-posterior sway, velocity and radius of sway, length of the sway path and area within the sway profile. A marked difference in sway behaviour between the sexes was observed, with women showing increased magnitudes of some sway parameters. Postural sway was significantly increased in conditions without visual feedback. The presence of an auditory field tends to have a destabilising influence on sway behaviour, with both the direction of the sound source and the type of auditory input being important variables. Nevertheless there appears to be no interaction between the visual and the auditory environment in the control of posture.     

The importance of surface-based cues for face discrimination in non-human primates

Understanding how individual identity is processed from faces remains a complex problem. Contrast reversal, showing faces in photographic negative, impairs face recognition in humans and demonstrates the importance of surface-based information (shading and pigmentation) in face recognition. We tested the importance of contrast information for face encoding in chimpanzees and rhesus monkeys using a computerized face-matching task. Results showed that contrast reversal (positive to negative) selectively impaired face processing in these two species, although the impairment was greater for chimpanzees. Unlike chimpanzees, however, monkeys performed just as well matching negative to positive faces, suggesting that they retained some ability to extract identity information from negative faces. A control task showed that chimpanzees, but not rhesus monkeys, performed significantly better matching face parts compared with whole faces after a contrast reversal, suggesting that contrast reversal acts selectively on face processing, rather than general visual-processing mechanisms. These results confirm the importance of surface-based cues for face processing in chimpanzees and humans, while the results were less salient for rhesus monkeys. These findings make a significant contribution to understanding the evolution of cognitive specializations for face processing among primates, and suggest potential differences between monkeys and apes.     

Ocean acidification erodes crucial auditory behaviour in a marine fish

Ocean acidification is predicted to affect marine ecosystems in many ways, including modification of fish behaviour. Previous studies have identified effects of CO(2)-enriched conditions on the sensory behaviour of fishes, including the loss of natural responses to odours resulting in ecologically deleterious decisions. Many fishes also rely on hearing for orientation, habitat selection, predator avoidance and communication. We used an auditory choice chamber to study the influence of CO(2)-enriched conditions on directional responses of juvenile clownfish (Amphiprion percula) to daytime reef noise. Rearing and test conditions were based on Intergovernmental Panel on Climate Change predictions for the twenty-first century: current-day ambient, 600, 700 and 900 μatm pCO(2). Juveniles from ambient CO(2)-conditions significantly avoided the reef noise, as expected, but this behaviour was absent in juveniles from CO(2)-enriched conditions. This study provides, to our knowledge, the first evidence that ocean acidification affects the auditory response of fishes, with potentially detrimental impacts on early survival.     

Agonistic behaviour of juvenile gulls,a neuroethological study

The results relating to agonistic behaviour obtained during an exploration of the brain of juvenile herring and lesser black-backed gulls (Larus argentatus and fuscus) with electrical stimulation are reported. As an introduction the normal agonistic behaviour of immature gulls is described. While the flight and aggressive behaviour is largely unritualized the threat behaviour is more stereotyped. Three basic threat patterns are distinguished: the arched, hunched, and squat postures. The relationship of these juvenile agonistic patterns with adult courtship is considered. A large number of sites evoking fear behaviour were found, anatomically widely and incoherently distributed. It is demonstrated that the spontaneous fearfulness levels of individual subjects influences the likelihood of obtaining escape eliciting loci. Stimulation of a nubmer of these sites had an after-effect: a persistent, increased probability of escape behaviour. It seems likely that a proportion of the fear sequences elicited were secondary responses to evoked sensory hallucinations and forced small movements. None of the sites explored yielded outright attack behaviour. Thirteen sites yielded characteristic threat sequences. About half of them produced changes in ‘mood’ persisting for some 15 min. The sites were clustered in a paleostriatal-septal periventricular and an infundibular area. Histological differentiation of the neuroventricular interface at these areas is noted. Based on these it is argued that the secretion of ‘liquormones’ is responsible for the changes in ‘mood’ that followed stimulation.     

A blueprint for vocal learning: auditory predispositions from brains to genomes

Memorizing and producing complex strings of sound are requirements for spoken human language. We share these behaviours with likely more than 4000 species of songbirds, making birds our primary model for studying the cognitive basis of vocal learning and, more generally, an important model for how memories are encoded in the brain. In songbirds, as in humans, the sounds that a juvenile learns later in life depend on auditory memories formed early in development. Experiments on a wide variety of songbird species suggest that the formation and lability of these auditory memories, in turn, depend on auditory predispositions that stimulate learning when a juvenile hears relevant, species-typical sounds. We review evidence that variation in key features of these auditory predispositions are determined by variation in genes underlying the development of the auditory system. We argue that increased investigation of the neuronal basis of auditory predispositions expressed early in life in combination with modern comparative genomic approaches may provide insights into the evolution of vocal learning.     

Calbindin‐positive neurons reveal a sexual dimorphism within the songbird analogue of the mammalian auditory cortex

The oscine song system, a set of interconnected brain nuclei involved in song production and learning, is one of the first and clearest examples of brain sexual dimorphism in a vertebrate, being typically well‐developed in males, but not females. Here we present evidence for a sexual dimorphism in the caudomedial nidopallidum (NCM), an auditory area outside of the song system. NCM is thought to correspond to a portion of the auditory cortex of mammals and is involved in the perceptual processing of birdsong. We show that cells immunolabeled for the calcium‐binding protein calbindin are primarily localized to caudal NCM and are almost twice as numerous in males as in females. We demonstrate that calbindin‐positive cells constitute a subset of GABAergic cells in NCM, and show that the sex dimorphism in this cell population does not result from local gender differences in the overall density of neuronal or GABAergic cells. In addition, we demonstrate that calbindin‐positive cells lack song‐induced expression of the activity‐dependent gene ZENK, and that song stimulation does not change the density or distribution of these cells in NCM. Finally, we show that the distribution of calbindin‐positive cells in NCM is strikingly similar to the mRNA expression for the estrogen‐generating enzyme aromatase. Together these results suggest that NCM is likely composed of neurochemically‐distinct domains and presents a marked sex dimorphism in a specific subset of GABAergic neurons, which may confer sex‐specific sensory processing capabilities to this auditory area. Our results also suggest that local sex steroid hormones may play a local role in auditory processing in the songbird telencephalon. © 2005 Wiley Periodicals, Inc. J Neurobiol, 2005     

Automated auditory detection of a rare,secretive marsh bird with infrequent and acoustically indistinct vocalizations

Autonomous recording units (ARUs) provide a non-invasive and efficient method for acoustic detection of elusive species across large temporal and spatial scales. However, species with indistinct vocalization structures can be a considerable challenge for automated signal recognizers. We investigated the performance of ARUs and signal recognizers in identifying the broadband, short-syllable, pulsed calls of a secretive, threatened marsh bird, the King Rail Rallus elegans. Other sympatric species in the same habitat also have repetitive calls within the same frequency range that can be difficult to distinguish. Following serial ARU deployments at specified sites in known breeding habitat, we conducted standardized callback surveys and nest searches to provide an independent measure of breeder density. To analyse recordings, we developed a signal recognizer based on user-input training files to detect two common call types, kek and grunt. Detections that remained following manual review of recognizer output revealed a previously undescribed seasonal decline and crepuscular diel pattern in calling rate. The rate of the grunt call also predicted density. These patterns emerged despite the recognizer's low precision and high false-positive rate, which were largely due to misclassification of other species' calls, although ambient noise and effective detection radius also limited the detectability of King Rail calls. We demonstrate that with informed ARU scheduling, improved ability to manipulate user-specified parameters within signal detection software, and attention to quality control, even the simplest call structures can be located consistently in a diverse acoustic landscape. Our behavioural findings will inform improvements to auditory surveys and to management of King Rails across their range.     

A songbird forebrain area potentially involved in auditory discrimination and memory formation

Songbirds rely on auditory processing of natural communication signals for a number of social behaviors,including mate selection,individual recognition and the rare behavior of vocal learning - the ability to learn vocalizations through imitation of an adult model,rather than by instinct.Like mammals,songbirds possess a set of interconnected ascending and descending auditory brain pathways that process acoustic information and that are presumably involved in the perceptual processing of vocal communication signals.Most auditory areas studied to date are located in the caudomedial forebrain of the songbird and include the thalamo-recipient field L (sub fields L1,L2 and L3),the caudomedial and caudolateral mesopallium (CMM and CLM,respectively) and the caudomedial nidopallium (NCM). This review focuses on NCM,an auditory area previously proposed to be analogous to parts of the primary auditory cortex in mammals.Stimulation of songbirds with auditory stimuli drives vigorous electrophysiological responses and the expression of several activity-regulated genes in NCM.Interestingly,NCM neurons are tuned to species-specific songs and undergo some forms of experience-dependent plasticity in-vivo .These activity-dependent changes may underlie long-term modifications in the functional performance of NCM and constitute a potential neural substrate for auditory discrimination.We end this review by discussing evidence that suggests that NCM may be a site of auditory memory formation and/or storage.     

The function and mechanism of vocal accommodation in humans and other primates

The study of non‐human animals, in particular primates, can provide essential insights into language evolution. A critical element of language is vocal production learning, i.e. learning how to produce calls. In contrast to other lineages such as songbirds, vocal production learning of completely new signals is strikingly rare in non‐human primates. An increasing body of research, however, suggests that various species of non‐human primates engage in vocal accommodation and adjust the structure of their calls in response to environmental noise or conspecific vocalizations. To date it is unclear what role vocal accommodation may have played in language evolution, in particular because it summarizes a variety of heterogeneous phenomena which are potentially achieved by different mechanisms. In contrast to non‐human primates, accommodation research in humans has a long tradition in psychology and linguistics. Based on theoretical models from these research traditions, we provide a new framework which allows comparing instances of accommodation across species, and studying them according to their underlying mechanism and ultimate biological function. We found that at the mechanistic level, many cases of accommodation can be explained with an automatic perception–production link, but some instances arguably require higher levels of vocal control. Functionally, both human and non‐human primates use social accommodation to signal social closeness or social distance to a partner or social group. Together, this indicates that not only some vocal control, but also the communicative function of vocal accommodation to signal social closeness and distance must have evolved prior to the emergence of language, rather than being the result of it. Vocal accommodation as found in other primates has thus endowed our ancestors with pre‐adaptations that may have paved the way for language evolution.     

Development in the Usage and Comprehension of Greeting Calls in a Free‐Ranging Group of Japanese Macaques (Macaca fuscata)

The main objective of this study is to clarify the developmental process involved in both the usage of greeting calls and the response to greeting calls by Japanese macaques. These greeting calls facilitate affiliative interactions by communicating benign intent. Specifically, individuals frequently emit greeting calls when interacting with less‐predictable individuals. Here, we examined whether the targets at which greeting calls are directed, along with associated behavioral responses, differed among the age classes, by conducting a cross‐sectional observation of females aged 0–5 yr and their mothers. We found that infant females showed a weak tendency to emit greeting calls at no specific receivers, unlike that by older females. Adult females emitted greeting calls more frequently when approaching unrelated females than related females. In contrast, young adult or juvenile females exhibited no significant difference in the proportion of the calls with related and unrelated conspecifics. Adult and young adult females were more likely to respond affiliatively to other individuals that approached using greeting calls compared with silent approaches, whereas juveniles did not exhibit different responses to the two types of approaches. This study showed that the target‐specific usage and affiliative response to greeting calls emerge with changes in the developmental stage. Furthermore, the fact that even young adults did not use greeting calls as adults indicates that the usage of greeting calls is modified in conjunction with the expansion of social relationships.     

Vocal behavior of Great Curassows,a vulnerable Neotropical bird

ABSTRACT The Cracidae rank among the most threatened families of Neotropical birds, and studies of their vocal behavior may help guide conservation and monitoring efforts. We describe the vocal behavior of Great Curassows (Crax rubra), a little‐studied Cracid species currently listed as vulnerable. From 2008 to 2010, we recorded curassows in northwest Costa Rica using both handheld and automated digital recorders. Analysis of recordings revealed that Great Curassows had a vocal repertoire of five call types. Yip and bark calls are sex‐specific alarm calls of short duration (0.12 and 0.08 s, respectively). The descending whistle is a longer duration alarm call (2.18 s) produced primarily by males. The snarl is a short call (0.67 s) associated with a threat display produced by adults with dependent young. The boom call was the most common Great Curassow vocalization, and was given only by males. Boom calls are long (8.86 s), low‐frequency (<150 Hz), multisyllable calls comprised of four stereotyped phrases. Great Curassows often uttered boom calls well before dawn, with a peak in activity at dawn and the hours following. Males produced bouts of repeated boom calls that lasted an average of 35 min, but sometimes continued for more than 5 h. Boom calls were given from February to June, with a peak in late April and early May when breeding begins. Discriminant analysis of boom calls of birds from 10 different locations revealed interindividual variation in call structure that may be useful for bioacoustic monitoring of individuals. Our results suggest that automated recorders might provide a way to monitor the abundance of male curassows because their boom calls are given frequently during the period from February to June and can be detected at distances up to 250 m.     

Correlations between auditory structures and hearing sensitivity in non‐human primates

Primates show distinctions in hearing sensitivity and auditory morphology that generally follow phylogenetic patterns. However, few previous studies have attempted to investigate how differences in primate hearing are directly related to differences in ear morphology. This research helps fill this void by exploring the form‐to‐function relationships of the auditory system in a phylogenetically broad sample of non‐human primates. Numerous structures from the outer, middle, and inner ears were measured in taxa with known hearing capabilities. The structures investigated include the overall size and shape of the pinna, the areas of the tympanic membrane and stapedial footplate, the masses and lever arm lengths of the ossicles, the volumes of the middle ear cavities, and the length of the cochlea. The results demonstrate that a variety of auditory structures show significant correlations with certain aspects of hearing (particularly low‐frequency sensitivity). Although the majority of these relationships agree with expectations from auditory theory, some traditional (and possibly outdated) ideas were not supported. For example, the common misconception that higher middle ear transformer ratios (e.g., impedance transformer ratio) result in increased hearing sensitivity was not supported. Although simple correlations between form and function do not necessarily imply causality, the relationships defined in this study not only increase our understanding of auditory patterns in extant taxa but also lay the foundation to begin investigating the hearing in fossil primates. J. Morphol., 2010. © 2009 Wiley‐Liss, Inc.     

Adult bengalese finches (Lonchura striata var. domestica) require real-time auditory feedback to produce normal song syntax

Songbirds develop their songs by imitating songs of adults. For song learning to proceed normally, the bird's hearing must remain intact throughout the song development process. In many species, song learning takes place during one period early in life, and no more new song elements are learned thereafter. In these so-called close-ended learners, it has long been assumed that once song development is complete, audition is no longer necessary to maintain the motor patterns of full song. However, many of these close-ended learners maintain plasticity in overall song organization; the number and the sequence of song elements included in a song of an individual vary from one utterance to another, although no new song elements are added or lost in adulthood. It is conceivable that these species rely on continued auditory feedback to produce normal song syntax. The Bengalese finch is a close-ended learner that produces considerably variable songs as an adult. In the present study, we found that Bengalese finches require real-time auditory feedback for motor control even after song learning is complete; deafening adult finches resulted in development of abnormal song syntax in as little as 5 days. We also found that there was considerable individual variation in the degree of song deterioration after deafening. The neural mechanisms underlying adult song production in different species of songbirds may be more diverse than has been traditionally considered. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 343–356, 1997