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The vocal development of the pale spear-nosed bat is dependent on auditory feedback.

ABSTRACT: Human vocal development and speech learning require acoustic feedback, and humans who are born deaf do not acquire a normal adult speech capacity. Most other mammals display a largely innate vocal repertoire. Like humans, bats are thought to be one of the few taxa capable of vocal learning as they can acquire new vocalizations by modifying vocalizations according to auditory experiences. We investigated the effect of acoustic deafening on the vocal development of the pale spear-nosed bat. Three juvenile pale spear-nosed bats were deafened, and their vocal development was studied in comparison with an age-matched, hearing control group. The results show that during development the deafened bats increased their vocal activity, and their vocalizations were substantially altered, being much shorter, higher in pitch, and more aperiodic than the vocalizations of the control animals. The pale spear-nosed bat relies on auditory feedback for vocal development and, in the absence of auditory input, species-atypical vocalizations are acquired. This work serves as a basis for further research using the pale spear-nosed bat as a mammalian model for vocal learning, and contributes to comparative studies on hearing impairment across species. This article is part of the theme issue 'Vocal learning in animals and humans'.

SUBMITTER: Lattenkamp EZ

PROVIDER: S-EPMC8419572 | biostudies-literature | 2021 Oct

REPOSITORIES: biostudies-literature

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The vocal development of the pale spear-nosed bat is dependent on auditory feedback.

Lattenkamp Ella Z EZ Linnenschmidt Meike M Mardus Eva E Vernes Sonja C SC Wiegrebe Lutz L Schutte Michael M

Philosophical transactions of the Royal Society of London. Series B, Biological sciences 20210906 1836

Human vocal development and speech learning require acoustic feedback, and humans who are born deaf do not acquire a normal adult speech capacity. Most other mammals display a largely innate vocal repertoire. Like humans, bats are thought to be one of the few taxa capable of vocal learning as they can acquire new vocalizations by modifying vocalizations according to auditory experiences. We investigated the effect of acoustic deafening on the vocal development of the pale spear-nosed bat. Three ...[more]

PMID: 34482731

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Project description:Vocal control plays a critical role in smooth social communication. Speakers constantly monitor auditory feedback (AF) and make adjustments when their voices deviate from their intentions. Previous studies have shown that when certain acoustic features of the AF are artificially altered, speakers compensate for this alteration in the opposite direction. However, little is known about how the vocal control system implements compensations for alterations of different acoustic features, and associates them with subjective consciousness. The present study investigated whether compensations for the fundamental frequency (F0), which corresponds to perceived pitch, and formants, which contribute to perceived timbre, can be performed unconsciously and independently. Forty native Japanese speakers received two types of altered AF during vowel production that involved shifts of either only the formant frequencies (formant modification; Fm) or both the pitch and formant frequencies (pitch + formant modification; PFm). For each type, three levels of shift (slight, medium, and severe) in both directions (increase or decrease) were used. After the experiment, participants were tested for whether they had perceived a change in the F0 and/or formants. The results showed that (i) only formants were compensated for in the Fm condition, while both the F0 and formants were compensated for in the PFm condition; (ii) the F0 compensation exhibited greater precision than the formant compensation in PFm; and (iii) compensation occurred even when participants misperceived or could not explicitly perceive the alteration in AF. These findings indicate that non-experts can compensate for both formant and F0 modifications in the AF during vocal production, even when the modifications are not explicitly or correctly perceived, which provides further evidence for a dissociation between conscious perception and action in vocal control. We propose that such unconscious control of voice production may enhance rapid adaptation to changing speech environments and facilitate mutual communication.

Project description:BackgroundSuccessful animal communication depends on a receiver's ability to detect a sender's signal. Exemplars of adaptive sender-receiver coupling include acoustic communication, often important in the context of seasonal reproduction. During the reproductive summer season, both male and female midshipman fish (Porichthys notatus) exhibit similar increases in the steroid-dependent frequency sensitivity of the saccule, the main auditory division of the inner ear. This form of auditory plasticity enhances detection of the higher frequency components of the multi-harmonic, long-duration advertisement calls produced repetitively by males during summer nights of peak vocal and spawning activity. The molecular basis of this seasonal auditory plasticity has not been fully resolved. Here, we utilize an unbiased transcriptomic RNA sequencing approach to identify differentially expressed transcripts within the saccule's hair cell epithelium of reproductive summer and non-reproductive winter fish.ResultsWe assembled 74,027 unique transcripts from our saccular epithelial sequence reads. Of these, 6.4 % and 3.0 % were upregulated in the reproductive and non-reproductive saccular epithelium, respectively. Gene ontology (GO) term enrichment analyses of the differentially expressed transcripts showed that the reproductive saccular epithelium was transcriptionally, translationally, and metabolically more active than the non-reproductive epithelium. Furthermore, the expression of a specific suite of candidate genes, including ion channels and components of steroid-signaling pathways, was upregulated in the reproductive compared to the non-reproductive saccular epithelium. We found reported auditory functions for 14 candidate genes upregulated in the reproductive midshipman saccular epithelium, 8 of which are enriched in mouse hair cells, validating their hair cell-specific functions across vertebrates.ConclusionsWe identified a suite of differentially expressed genes belonging to neurotransmission and steroid-signaling pathways, consistent with previous work showing the importance of these characters in regulating hair cell auditory sensitivity in midshipman fish and, more broadly, vertebrates. The results were also consistent with auditory hair cells being generally more physiologically active when animals are in a reproductive state, a time of enhanced sensory-motor coupling between the auditory periphery and the upper harmonics of vocalizations. Together with several new candidate genes, our results identify discrete patterns of gene expression linked to frequency- and steroid-dependent plasticity of hair cell auditory sensitivity.

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The vocal development of the pale spear-nosed bat is dependent on auditory feedback.

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The vocal development of the pale spear-nosed bat is dependent on auditory feedback.

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