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Visually-guided compensation of deafening-induced song deterioration

M Rolland, A Zai, RHR Hahnloser, C Del Negro, N Giret

Posted on: 4 February 2025

Preprint posted on 4 November 2024

Hearing impaired songbirds keep their songs on track using visual cues.

Selected by Maitri Manjunath

Background:

Many vertebrates, especially mammals, learn language and speech by imitating and listening to themselves. However, hearing others talk is also crucial. In humans, post-lingual deafness or the loss of hearing after an individual has learned to hear and speak can lead to gradual deterioration of speech quality (Cowie et al., 1982). This emphasises the importance of auditory feedback on the maintenance of speech in adults. 

Besides humans, songbirds also use such feedback to vocalize sounds. These birds hear each other and learn to use different kinds of sounds to attract mates and defend their territories. Young songbirds begin learning this in their juvenile phase in a series of stages. In the so-called ‘primary sensory phase’, the birds listen to their parents (usually the father) and Remember the song by creating mental templates. This stage is followed by the ‘sensorimotor stage’ during which the birds begin to sing. These first attempts at singing turn into identifiable patterned songs by the end of a week, gradually developing into normal adult songs at the onset of sexual maturity. 

Hearing abilities play a crucial role in how well juvenile birds imitate their parents’ songs. Birds that lose their hearing experience a gradual decline in their ability to produce sounds (Nordeen and Nordeen, 1992). Interestingly, Zai and colleagues (2020) discovered that hearing-impaired adult birds can adapt their songs using non-auditory feedback. Building on these insights, the authors of this preprint sought to explore whether non-auditory cues could delay the onset of song deterioration caused by hearing loss.

To investigate this, the researchers developed a metric to assess syllable acoustic stability and track vocal deterioration in real time. They then refined the operant conditioning paradigm, initially designed by Zai et al. (2020) with pitch-contingent transient light extinction, to deliver visual signals based on the measured syllable acoustic stability.

Key findings:

  • A new metric to measure song stability

To determine if the birds (male zebra finches) can compensate for post-deafening song degradation with the help of visual cues, the authors compared the spectrogram of target signals with a reference. They first created songs with distorted acoustics from songs of 19 hearing intact male birds. While ensuring the amplitude did not exceed the original song, they included white noise with intensities between 0 to 100%. A comparison was then made between the spectrograms of the noisy recording and the reference syllable. Spectrogram divergence scores reliably increased with white noise intensity up to 40%, plateauing beyond this point, and showed minimal overlap between different white noise levels. These scores for individual syllables aligned with those for entire song motifs, indicating that assessing a single target syllable could capture broader song alterations.

Compared to other methods, spectrogram divergence scores were more consistent and less prone to variability or computation errors, particularly at higher white noise levels. The efficiency of spectrogram divergence scores, calculated in under 4 milliseconds, made them suitable for online, syllable-contingent behavioral training. These findings validate the spectrogram divergence score as a robust, efficient tool for assessing and addressing deafening-induced song degradation in zebra finches.

  • Hearing impaired songbirds exposed to visual stimuli exhibited stable song syllables.

The authors next explored whether deaf birds could use visual signals to mitigate the degradation of song syllables induced by deafening. Songs of 40 birds were recorded over seven weeks, including 33 birds that were deafened after baseline recording. Birds were divided into three groups: deaf LO (light extinction contingent on syllable accuracy), deaf random LO (random light extinction), and deaf no LO (no light extinction). Hearing birds served as controls.

Analysis showed that deafening caused a progressive loss of song motif stereotypy and increased spectrogram divergence scores, reflecting song degradation. Exposure to contingent light extinction partially slowed this degradation. Entropy and entropy variance analyses further confirmed that deaf LO birds maintained syllable structure better than deaf no LO birds. However, this effect was restricted to the specific 48-millisecond window used for triggering light extinction.

Figure 1.(modified from source)  B. Songs were recorded online, and a target syllable for each bird was automatically detected. For deaf LO birds (13 birds), if the spectrogram divergence score dropped below a set threshold, the housing light in the sound-proof chamber was briefly turned off for 200 ms; otherwise, the light stayed on. For deaf no-LO birds (15 birds), the light was never turned off, and for deaf random LO birds (5 birds), the light was randomly turned off when the bird produced the target syllable. C. Spectrograms of song motifs from three sibling birds were analyzed before and 1–6 weeks after deafening and starting the LO protocol. Each bird’s target syllable is marked with a dashed orange box, with zoomed-in views of the syllable before deafening and 6 weeks after.

Despite differences in syllable accuracy, all deafened groups showed a gradual decrease in singing activity over time, with no significant variation among the deaf groups. Measures of syllable duration, entropy, and entropy variance indicated increased noise and reduced song stability across all deaf birds. Changes to the overall song structure, including non-target syllables, were not significantly influenced by the light-off protocols.

In summary, visual signals contingent on syllable accuracy slowed, but did not prevent, deafening-induced song degradation. The effect was localized to the specific targeted syllable and limited to the visual signal’s operational timeframe.

What I like about the preprint?

This preprint addresses a critical side effect of hearing loss: speech impairment. The authors have focused on studying measures to delay the onset of degradation by studying  neural network plasticity in the absence of sensory information. The multisensory integration of stimuli in vocal song productions is an exciting discovery that could eventually help us understand the neural mechanisms behind speech impairment in people with hearing loss.

Questions to the authors:

  • What is the maximum time after a bird loses its hearing beyond which song degradation cannot be prevented?
  • Can birds with hearing impairments be trained to vocalize songs that are not innate to them from birth?

Future directions:

This study presents phenomenal data of how degradation of vocalizations can be delayed when hearing is impaired. Further to this study, it would be interesting to see at what life stages the delays can be induced such that they remain long term, thereby negating the effects of hearing loss on song production. 

References:

  • Cowie, R., Douglas-Cowie, E., and Kerr, A. G. (1982). A study of speech deterioration in post- lingually deafened adults. J Laryngol Otol 96, 101–112. doi: 10.1017/s002221510009229x
  • Nordeen, K. W., and Nordeen, E. J. (1992). Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. Behav. Neural Biol. 57, 58–66.

Tags: hearing impairment, song deterioration, syllables, vocalization

doi: https://doi.org/10.1242/prelights.39599

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