Learning to cope with degraded sounds: Female zebra finches can improve their expertise at discriminating between male voices at long distance

Abstract

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 degradation. 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 distances, 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 involve not only the emitter's vocal plasticity but also the receptor's decoding process through on-going learning.

Individual recognition of opposite sex vocalizations in the zebra finch

“…The sound level of the experimental signals, measured at a distance of 1 m from the loud speaker (Sound Meter, Model HD600, Extech Instruments, U.S.A), was adjusted to a peak value between 50.03 dB ± 0.87 dB (mean ± SD; minimum for the lowest call type, the tet) and 74.05 dB ± 1.15 dB (corresponding to the loudest call type, the distance call reflecting a typical level of a natural distance call) 39 , and was constant for all three familiarity levels of each call type.…”

Single Neurons in the Avian Auditory Cortex Encode Individual Identity and Propagation Distance in Naturally Degraded Communication Calls

“…Although birds (Klump, 1996; Mathevon et al, 2008; Mouterde et al, 2014a) as well as many other animals (e.g., Mercado and Frazer, 1999) excel at recognizing the information embedded in communication signals degraded by propagation, the neural mechanisms mediating this task remained unexplored. We found neurons in the avian auditory forebrain displaying high discrimination for the identity of unfamiliar vocalizing birds, with remarkable invariance to the sound degradation induced by long-range propagation through the natural environment.…”

“…Wang et al (2007) have shown that behavioral performance for song discrimination is correlated with the performance of the most discriminating higher-level single neurons, which activity might potentially be reflecting the computations performed by the entire network. Using behavioral tests, we had previously found that female zebra finches were able to discriminate between the degraded calls of male zebra finches at up to 128 m without training and up to 256 m with training (Mouterde et al, 2014a). Here we found that single neurons could discriminate among unfamiliar individuals with calls that were degraded up to 256 m. Thus, there is an approximate match between single neuron performance and behavioral performance, with single neurons even outperforming behavioral tests in the sense that recognition at the longest propagation distance in behavioral testing was only achieved after repeated training.…”

“…This short call is emitted by both sexes, bears an individual signature, and pair-bonded adults use it to both identify and locate their partner when a visual connection has been lost (Zann, 1984, 1996; Vignal et al, 2004, 2008). While long-range propagation through the environment induces a profound degradation of the calls' quality (Wiley and Richards, 1982; Mouterde et al, 2014b), previous experiments showed that female zebra finches can still discriminate between the calls of males propagated at distances >100 m (Mouterde et al, 2014a). This impressive perceptual ability must be mediated by auditory neurons whose responses, coding for identity information, are only minimally affected by propagation-induced sound degradations.…”

Sounds of the city: The effects of urbanization and noise on mountain and black-capped chickadee communication.

“…There is some evidence that zebra finches (Taeniopygia guttata) can learn to correctly discriminate among songs that have been degraded by distance (Mouterde et al, 2014).…”