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Acoustic communication in the natural world requires both emitter and receiver to adapt to the loss of information due to the transmission of sound in the environment. At the emitter’s end, encoding information into propagation-resistant features may ensure its transmission on ecologically relevant distances. At the receiver’s end, making sense of the degraded signal merged with added noise enables animals to produce behaviorally relevant responses. In this chapter, I use a songbird model to investigate both sides of the transmission chain, examining how individual vocal signatures are encoded, degraded and finally discriminated, with a particular emphasis on the receiver’s neural encoding of degraded information. The cornerstone of this focal study is the use of naturally degraded vocalizations, combining various aspects of the challenges faced by animals performing auditory scene analysis, in order to address the complexity of real-life ecological constraints. While the individual signature of our songbird model, the zebra finch, is very resistant to propagation-induced degradation, single neurons in the avian auditory cortex have the ability to discriminate highly degraded individual vocal signatures, without prior familiarization or training. In the light of past and recent findings in birds and mammals, I delve further into significant insights uncovered by the research on neural processing and ensemble coding, and discuss the roles of perceptual plasticity and learning in the neural interface between brain and behavior.

One of the most complex tasks performed by sensory systems is “scene analysis”: the interpretation of complex signals as behaviorally relevant objects. The study of this problem, universal to species and sensory modalities, is particularly challenging in audition, where sounds from various sources and localizations, degraded by propagation through the environment, sum to form a single acoustical signal. Here we investigated in a songbird model, the zebra finch, the neural substrate for ranging and identifying a single source. We relied on ecologically and behaviorally relevant stimuli, contact calls, to investigate the neural discrimination of individual vocal signature as well as sound source distance when calls have been degraded through propagation in a natural environment. Performing electrophysiological recordings in anesthetized birds, we found neurons in the auditory forebrain that discriminate individual vocal signatures despite long-range degradation, as well as neurons discriminating propagation distance, with varying degrees of multiplexing between both information types. Moreover, the neural discrimination performance of individual identity was not affected by propagation-induced degradation beyond what was induced by the decreased intensity. For the first time, neurons with distance-invariant identity discrimination properties as well as distance-discriminant neurons are revealed in the avian auditory cortex. Because these neurons were recorded in animals that had prior experience neither with the vocalizers of the stimuli nor with long-range propagation of calls, we suggest that this neural population is part of a general-purpose system for vocalizer discrimination and ranging.SIGNIFICANCE STATEMENTUnderstanding how the brain makes sense of the multitude of stimuli that it continually receives in natural conditions is a challenge for scientists. Here we provide a new understanding of how the auditory system extracts behaviorally relevant information, the vocalizer identity and its distance to the listener, from acoustic signals that have been degraded by long-range propagation in natural conditions. We show, for the first time, that single neurons, in the auditory cortex of zebra finches, are capable of discriminating the individual identity and sound source distance in conspecific communication calls. The discrimination of identity in propagated calls relies on a neural coding that is robust to intensity changes, signals' quality, and decreases in the signal-to-noise ratio.

Agonistic signals used during contests over important resources have been extensively studied; postconflict signals have received comparatively little attention. While ‘triumph displays’, performed by winners following fights, have been described for many species, no experiment has yet assessed one of the main hypotheses explaining their existence: advertising victory to social eavesdroppers. Our experiments evaluated the impact of triumph calls on the behaviour and stress responses of surrounding penguins. We found that territorial male little blue penguins, Eudyptula minor, having previously been exposed to playback of a vocal exchange between conspecifics followed by the sounds of a fight, had higher heart rates in response to the winner’s call than that of the loser; females had high rates in response to both winners and losers. Males were also less likely to threaten winners than losers vocally during a simulated approach of their burrow, while females remained silent in both contexts. Our findings support the hypothesis that triumph calls facilitate an association of winners’ distinctive vocalizations with stress generated by nearby overt aggression. By advertising their victories, males may establish a ‘reputation’ for winning fights within the social group, potentially reducing the likelihood of being challenged by eavesdroppers in future contests.

Reliable transmission of acoustic information about individual identity is of critical importance for pair bond maintenance in numerous monogamous songbirds. However, information transfer can be impaired by environmental constraints such as external noise or propagation-induced degradations. Birds have been shown to use several adaptive strategies to deal with difficult signal transmission contexts. Specifically, a number of studies have suggested that vocal plasticity at the emitter's level allows birds to counteract the deleterious effects of sound degradation. Although the communication process involves both the emitter and the receiver, perceptual plasticity at the receiver's level has received little attention. Here, we explored the reliability of individual recognition by female zebra finches (Taeniopygia guttata), testing whether perceptual training can improve discrimination of degraded individual vocal signatures. We found that female zebra finches are proficient in discriminating between calls of individual males at long distance, and even more so when they can train themselves with increasingly degraded signals over time. In this latter context, females succeed in discriminating between males as far as 250 m. This result emphasizes that adaptation to adverse communication conditions may not only involve the emitters' vocal plasticity, but also the receptors' decoding process through on-going learning.

Background Assessing the active space of the various types of information encoded by songbirds' vocalizations is important to address questions related to species ecology (e.g. spacing of individuals), as well as social behavior (e.g. territorial and/or mating strategies). Up to now, most of the previous studies have investigated the degradation of species-specific related information (species identity), and there is a gap of knowledge of how finer-grained information (e.g. individual identity) can transmit through the environment. Here we studied how the individual signature coded in the zebra finch long distance contact call degrades with propagation. Methodology We performed sound transmission experiments of zebra finches' distance calls at various propagation distances. The propagated calls were analyzed using discriminant function analyses on a set of analytical parameters describing separately the spectral and temporal envelopes, as well as on a complete spectrographic representation of the signals. Results/Conclusion We found that individual signature is remarkably resistant to propagation as caller identity can be recovered even at distances greater than a hundred meters. Male calls show stronger discriminability at long distances than female calls, and this difference can be explained by the more pronounced frequency modulation found in their calls. In both sexes, individual information is carried redundantly using multiple acoustical features. Interestingly, features providing the highest discrimination at short distances are not the same ones that provide the highest discrimination at long distances.

The detection and recognition of communication signals in natural soundscapes is a difficult task that animals and birds in particular excel at. We have used a neuroethological approach to quantify the recognition performance for propagated communication signals in the zebra finch, specifically regarding the information about individual identity. The propagated signals were analyzed using a regularized discriminant function analyses on a complete spectrographic representation of the signals. We found 1) a reduction in the informative frequency range a long distances yielding a frequency band sweet-spot, 2) that call duration and pitch are important parameters at short distances and 3) that frequency modulation gains are important parameters at longer distances. Operant conditioning experiments showed that female songbirds were able to discriminate male calls at up to 128m but not at 256m. Finally, neurophysiological recordings showed a similar pattern in that high neural discrimination for calls was observed at 16 m and that this information degraded as a function of distance. We are currently analyzing the tuning properties of neurons that showed the most invariant responses to propagated sounds and hypothesized that these will be tuned to the parameters that we found were the most informative in the discriminant function analysis.