Multisensory processes in birds: From single neurons to the influence of social interactions and sensory loss.

World experiences involve multisensory stimulation that arises simultaneously from multiple sources. Yet, we experience a coherent and unified world. Many studies have focused on how sensory information from distinct modalities are integrated and showed that numerous behavioural and cognitive benefits are provided by multisensory processes. Much work has been done with mammalian models but research on avian species also expands our knowledge on multisensory processes. Avian species exhibit a great diversity of behaviours and these species have provided evidence that multisensory processes benefit by the learning that occurs in natural situations. Cross-modal influences on the control of sensorimotor processes occur in circumstances of sensory loss. Also, studies suggest pervasive multisensory influences throughout the avian brain. This review summarizes research done on the imprinting behaviour of precocial bird species, on the ability of barn owls to detect prey and on the vocal communication of songbirds.

Distinct timescales for the neuronal encoding of vocal signals in a high-order auditory area.

The ability of the auditory system to selectively recognize natural sound categories while maintaining a certain degree of tolerance towards variations within these categories, which may have functional roles, is thought to be crucial for vocal communication. To date, it is still largely unknown how the balance between tolerance and sensitivity to variations in acoustic signals is coded at a neuronal level. Here, we investigate whether neurons in a high-order auditory area in zebra finches, a songbird species, are sensitive to natural variations in vocal signals by recording their responses to repeated exposures to identical and variant sound sequences. We used the songs of male birds which tend to be highly repetitive with only subtle variations between renditions. When playing these songs to both anesthetized and awake birds, we found that variations between songs did not affect the neuron firing rate but the temporal reliability of responses. This suggests that auditory processing operates on a range of distinct timescales, namely a short one to detect variations in vocal signals, and longer ones that allow the birds to tolerate variations in vocal signal structure and to encode the global context.

Sensory substitution reveals a manipulation bias.

Sensory substitution is a promising therapeutic approach for replacing a missing or diseased sensory organ by translating inaccessible information into another sensory modality. However, many substitution systems are not well accepted by subjects. To explore the effect of sensory substitution on voluntary action repertoires and their associated affective valence, we study deaf songbirds to which we provide visual feedback as a substitute of auditory feedback. Surprisingly, deaf birds respond appetitively to song-contingent binary visual stimuli. They skillfully adapt their songs to increase the rate of visual stimuli, showing that auditory feedback is not required for making targeted changes to vocal repertoires. We find that visually instructed song learning is basal-ganglia dependent. Because hearing birds respond aversively to the same visual stimuli, sensory substitution reveals a preference for actions that elicit sensory feedback over actions that do not, suggesting that substitution systems should be designed to exploit the drive to manipulate.

Undirected singing rate as a non-invasive tool for welfare monitoring in isolated male zebra finches.

Research on the songbird zebra finch (Taeniopygia guttata) has advanced our behavioral, hormonal, neuronal, and genetic understanding of vocal learning. However, little is known about the impact of typical experimental manipulations on the welfare of these birds. Here we explore whether the undirected singing rate can be used as an indicator of welfare. We tested this idea by performing a post hoc analysis of singing behavior in isolated male zebra finches subjected to interactive white noise, to surgery, or to tethering. We find that the latter two experimental manipulations transiently but reliably decreased singing rates. By contraposition, we infer that a high-sustained singing rate is suggestive of successful coping or improved welfare in these experiments. Our analysis across more than 300 days of song data suggests that a singing rate above a threshold of several hundred song motifs per day implies an absence of an acute stressor or a successful coping with stress. Because singing rate can be measured in a completely automatic fashion, its observation can help to reduce experimenter bias in welfare monitoring. Because singing rate measurements are non-invasive, we expect this study to contribute to the refinement of the current welfare monitoring tools in zebra finches.

Neuronal Encoding in a High-Level Auditory Area: From Sequential Order of Elements to Grammatical Structure.

Sensitivity to the sequential structure of communication sounds is fundamental not only for language comprehension in humans but also for song recognition in songbirds. By quantifying single-unit responses, we first assessed whether the sequential order of song elements, called syllables, in conspecific songs is encoded in a secondary auditory cortex-like region of the zebra finch brain. Based on a habituation/dishabituation paradigm, we show that, after multiple repetitions of the same conspecific song, rearranging syllable order reinstated strong responses. A large proportion of neurons showed sensitivity to song context in which syllables occurred providing support for the nonlinear processing of syllable sequences. Sensitivity to the temporal order of items within a sequence should enable learning its underlying structure, an ability considered a core mechanism of the human language faculty. We show that repetitions of songs that were ordered according to a specific grammatical structure (i.e., ABAB or AABB structures; A and B denoting song syllables) led to different responses in both anesthetized and awake birds. Once responses were decreased due to song repetitions, the transition from one structure to the other could affect the firing rates and/or the spike patterns. Our results suggest that detection was based on local differences rather than encoding of the global song structure as a whole. Our study demonstrates that a high-level auditory region provides neuronal mechanisms to help discriminate stimuli that differ in their sequential structure.SIGNIFICANCE STATEMENT Sequence processing has been proposed as a potential precursor of language syntax. As a sequencing operation, the encoding of the temporal order of items within a sequence may help in recognition of relationships between adjacent items and in learning the underlying structure. Taking advantage of the stimulus-specific adaptation phenomenon observed in a high-level auditory region of the zebra finch brain, we addressed this question at the neuronal level. Reordering elements within conspecific songs reinstated robust responses. Neurons also detected changes in the structure of artificial songs, and this detection depended on local transitions between adjacent or nonadjacent syllables. These findings establish the songbird as a model system for deciphering the mechanisms underlying sequence processing at the single-cell level.

Seasonal plasticity of song behavior relies on motor and syntactic variability induced by a basal ganglia-forebrain circuit.

The plasticity of nervous systems allows animals to quickly adapt to a changing environment. In particular, seasonal plasticity of brain structure and behavior is often critical to survival or mating in seasonal climates. Songbirds provide striking examples of seasonal changes in neural circuits and vocal behavior and have emerged as a leading model for adult brain plasticity. While seasonal plasticity and the well-characterized process of juvenile song learning may share common neural mechanisms, the extent of their similarity remains unclear. Especially, it is unknown whether the basal ganglia (BG)-forebrain loop which implements song learning in juveniles by driving vocal exploration participates in seasonal plasticity. To address this issue, we performed bilateral lesions of the output structure of the song-related BG-forebrain circuit (the magnocellular nucleus of the anterior nidopallium) in canaries during the breeding season, when song is most stereotyped, and just after resuming singing in early fall, when canaries sing their most variable songs and may produce new syllable types. Lesions drastically reduced song acoustic variability, increased song and phrase duration, and decreased syntax variability in early fall, reverting at least partially seasonal changes observed between the breeding season and early fall. On the contrary, lesions did not affect singing behavior during the breeding season. Our results therefore indicate that the BG-forebrain pathway introduces acoustic and syntactic variability in song when canaries resume singing in early fall. We propose that BG-forebrain circuits actively participate in seasonal plasticity by injecting variability in behavior during non-breeding season. SIGNIFICANCE STATEMENT: The study of seasonal plasticity in temperate songbirds has provided important insights into the mechanisms of structural and functional plasticity in the central nervous system. The precise function and mechanisms of seasonal song plasticity however remain poorly understood. We show here that a basal ganglia-forebrain circuit involved in the acquisition and maintenance of birdsong is actively inducing song variability outside the breeding season, when singing is most variable, while having little effect on the stereotyped singing during the breeding season. Our results suggest that seasonal plasticity reflects an active song-maintenance process akin to juvenile learning, and that basal ganglia-forebrain circuits can drive plasticity in a learned vocal behavior during the non-injury-induced degeneration and reconstruction of the neural circuit underlying its production.

Neural mechanisms of vocal imitation: The role of sleep replay in shaping mirror neurons.

Learning by imitation involves not only perceiving another individual's action to copy it, but also the formation of a memory trace in order to gradually establish a correspondence between the sensory and motor codes, which represent this action through sensorimotor experience. Memory and sensorimotor processes are closely intertwined. Mirror neurons, which fire both when the same action is performed or perceived, have received considerable attention in the context of imitation. An influential view of memory processes considers that the consolidation of newly acquired information or skills involves an active offline reprocessing of memories during sleep within the neuronal networks that were initially used for encoding. Here, we review the recent advances in the field of mirror neurons and offline processes in the songbird. We further propose a theoretical framework that could establish the neurobiological foundations of sensorimotor learning by imitation. We propose that the reactivation of neuronal assemblies during offline periods contributes to the integration of sensory feedback information and the establishment of sensorimotor mirroring activity at the neuronal level.

Sex differences in the representation of call stimuli in a songbird secondary auditory area.

Understanding how communication sounds are encoded in the central auditory system is critical to deciphering the neural bases of acoustic communication. Songbirds use learned or unlearned vocalizations in a variety of social interactions. They have telencephalic auditory areas specialized for processing natural sounds and considered as playing a critical role in the discrimination of behaviorally relevant vocal sounds. The zebra finch, a highly social songbird species, forms lifelong pair bonds. Only male zebra finches sing. However, both sexes produce the distance call when placed in visual isolation. This call is sexually dimorphic, is learned only in males and provides support for individual recognition in both sexes. Here, we assessed whether auditory processing of distance calls differs between paired males and females by recording spiking activity in a secondary auditory area, the caudolateral mesopallium (CLM), while presenting the distance calls of a variety of individuals, including the bird itself, the mate, familiar and unfamiliar males and females. In males, the CLM is potentially involved in auditory feedback processing important for vocal learning. Based on both the analyses of spike rates and temporal aspects of discharges, our results clearly indicate that call-evoked responses of CLM neurons are sexually dimorphic, being stronger, lasting longer, and conveying more information about calls in males than in females. In addition, how auditory responses vary among call types differ between sexes. In females, response strength differs between familiar male and female calls. In males, temporal features of responses reveal a sensitivity to the bird's own call. These findings provide evidence that sexual dimorphism occurs in higher-order processing areas within the auditory system. They suggest a sexual dimorphism in the function of the CLM, contributing to transmit information about the self-generated calls in males and to storage of information about the bird's auditory experience in females.

Evidence for a causal inverse model in an avian cortico-basal ganglia circuit.

Learning by imitation is fundamental to both communication and social behavior and requires the conversion of complex, nonlinear sensory codes for perception into similarly complex motor codes for generating action. To understand the neural substrates underlying this conversion, we study sensorimotor transformations in songbird cortical output neurons of a basal-ganglia pathway involved in song learning. Despite the complexity of sensory and motor codes, we find a simple, temporally specific, causal correspondence between them. Sensory neural responses to song playback mirror motor-related activity recorded during singing, with a temporal offset of roughly 40 ms, in agreement with short feedback loop delays estimated using electrical and auditory stimulation. Such matching of mirroring offsets and loop delays is consistent with a recent Hebbian theory of motor learning and suggests that cortico-basal ganglia pathways could support motor control via causal inverse models that can invert the rich correspondence between motor exploration and sensory feedback.

Phonological-dependent territorial responses in yellowhammers (Emberiza citrinella).

In songbirds, males sing to attract potential mate and to defend their territory. Information about the sender such as its sex, its motivational state, its strength or identity can be encoded through subtle modifications in songs. In this study, we investigated whether territorial responses of yellowhammer males may be affected by modifications of song syntax and phonology. Yellowhammer song is mainly composed of three elements among which the last one is a long and low frequency note that is supposed to be the main component used by males to assess their potential rival. We carried out field experiments and played back either fully natural songs or partly natural and partly artificial songs to test this hypothesis. We identified that phonology rather than syntax modifications altered territorial responses. Our results also suggest that the phonology of the first song element plays a critical role in driving territorial responses.

Finding good acoustic features for parrot vocalizations: the feature generation approach.

A crucial step in the understanding of vocal behavior of birds is to be able to classify calls in the repertoire into meaningful types. Methods developed to this aim are limited either because of human subjectivity or because of methodological issues. The present study investigated whether a feature generation system could categorize vocalizations of a bird species automatically and effectively. This procedure was applied to vocalizations of African gray parrots, known for their capacity to reproduce almost any sound of their environment. Outcomes of the feature generation approach agreed well with a much more labor-intensive process of a human expert classifying based on spectrographic representation, while clearly out-performing other automated methods. The method brings significant improvements in precision over commonly used bioacoustical analyses. As such, the method enlarges the scope of automated, acoustics-based sound classification.

Referential learning of French and Czech labels in African grey parrots (Psittacus erithacus): different methods yield contrasting results.

Some African grey parrots (Psittacus erithacus), the most famous being Pepperberg's parrot Alex, are able to imitate human speech and produce labels referentially. In this study, the aim was to teach ten African grey parrots from two laboratories to label items. Training three parrots from the first laboratory for several months with the Model/Rival method, developed by Pepperberg, in which two humans interact in front of the subject to demonstrate the use of a label, led to disappointing results. Similarly, seven parrots from the second laboratory, having been trained with several variants of Model/Rival attained little success. After the informal observation of the efficiency of other methods (i.e. learning to imitate labels either spontaneously or with specific learning methods and use of these labels referentially), four different teaching methods were tested with two birds: the Model/Rival; Repetition/Association which consisted of repeating a label and presenting the item only when the parrot produced the label; Intuitive in which the experimenter handled an item and repeated its name in front of the subject; Diffusion in which labels with either variable or flat intonation were played back daily to parrots. One bird learned three labels, one of which was used referentially, with the Repetition/Association method. He learned one label non-referentially with the Model/Rival but no labels were acquired using the other methods. The second bird did not learn any labels. This study demonstrates that different methods can be efficient to teach labels referentially and it suggests that rearing conditions and interindividual variability are important features when assessing learning ability of African grey parrots.

Spontaneous categorization of vocal imitations in African grey parrots (Psittacus erithacus).

The ability to categorize elements of the environment is a fundamental aspect of information processing. Many experiments demonstrate the ability of birds and non-human primates to classify items according to their perceptual similarities. Few data are available regarding spontaneous classification of items according to a non-perceptual account in non-human animals. Here, we report unexpected results obtained with African grey parrots learning the referential use of French labels. Parrots did not learn the correct labels but they spontaneously produced more labels corresponding to food when a food item was presented to them and more labels corresponding to an object when shown an object item, although they were never rewarded for doing so. These results demonstrate a form of spontaneous categorization by using vocal imitation of the human language.

Conspecific discrimination in an object-choice task in African grey parrots (Psittacus erithacus).

Living in social groups presents the opportunity to use information provided by other individuals. Several animal species emit specific vocalizations when they find food. Here, we investigate whether African grey parrots (Psittacus erithacus) use vocal and non-vocal information provided by a conspecific in order to find a hidden food source. One subject was attracted by the presence or the vocalizations of a subordinate conspecific, but not of a dominant, which brings us to hypothesize that parrots could be capable of individual vocal discrimination.

The discrimination of discrete and continuous amounts in African grey parrots (Psittacus erithacus).

A wealth of research in infants and animals demonstrates discrimination of quantities, in some cases nonverbal numerical perception, and even elementary calculation capacities. We investigated the ability of three African grey parrots (Psittacus erithacus) to select the largest amount of food between two sets, either discrete food items (experiment 1) or as volume of a food substance (experiment 2). The two amounts were presented simultaneously and were visible at the time of choice. Parrots were tested several times for all possible combinations between 1 and 5 seeds or 0.2 and 1 ml of food substance. In both conditions, subjects performed above chance for almost all combinations. Accuracy was negatively correlated with the ratio, that is performance improved with greater differences between amounts. Therefore, these results with both individual items and volume discrimination suggest that parrots use an analogue of magnitude, rather than object-file mechanisms to quantify items and substances.

Use of experimenter-given cues by African gray parrots (Psittacus erithacus).

One advantage of living in a social group is the opportunity to use information provided by other individuals. Social information can be based on cues provided by a conspecific or even by a heterospecific individual (e.g., gaze direction, vocalizations, pointing gestures). Although the use of human gaze and gestures has been extensively studied in primates, and is increasingly studied in other mammals, there is no documentation of birds using these cues in a cooperative context. In this study, we tested the ability of three African gray parrots to use different human cues (pointing and/or gazing) in an object-choice task. We found that one subject spontaneously used the most salient pointing gesture (looking and steady pointing with hand at about 20 cm from the baited box). The two others were also able to use this cue after 15 trials. None of the parrots spontaneously used the steady gaze cues (combined head and eye orientation), but one learned to do so effectively after only 15 trials when the distance between the head and the baited box was about 1 m. However, none of the parrots were able to use the momentary pointing nor the distal pointing and gazing cues. These results are discussed in terms of sensitivity to joint attention as a prerequisite to understand pointing gestures as it is to the referential use of labels.