Engineered Deafness Reveals That Mouse Courtship Vocalizations Do Not Require Auditory Experience

Abstract

Auditory experience during development is necessary for normal language acquisition in humans. Although songbirds, some cetaceans, and maybe bats may also be vocal learners, vocal learning has yet to be well established for a laboratory mammal. Mice are potentially an excellent model organism for studying mechanisms underlying vocal communication. Mice vocalize in different social contexts, yet whether they learn their vocalizations remains unresolved. To address this question, we compared ultrasonic courtship vocalizations emitted by chronically deaf and normal hearing adult male mice. We deafened CBA/CaJ male mice, engineered to express diphtheria toxin (DT) receptors in hair cells, by systemic injection of DT at postnatal day 2 (P2). By P9, almost all inner hair cells were absent and by P16 all inner and outer hair cells were absent in DTR mice. These mice did not show any auditory brainstem responses as adults. Wild-type littermates, also treated with DT at P2, had normal hair cells and normal auditory brainstem responses. We compared the temporal structure of vocalization bouts, the types of vocalizations, the patterns of syllables, and the acoustic features of each syllable type emitted by hearing and deaf males in the presence of a female. We found that almost all of the vocalization features we examined were similar in hearing and deaf animals. These findings indicate that mice do not need auditory experience during development to produce normal ultrasonic vocalizations in adulthood. We conclude that mouse courtship vocalizations are not acquired through auditory feedback-dependent learning.

Spontaneous hair cell regeneration in the neonatal mouse cochlea in vivo

“…Progressive HC death was observed in Pou4f3 DTR/+ mice after DT injection at P1 (Fig. 1), consistent with previous reports (Golub et al, 2012;Mahrt et al, 2013;Tong et al, 2011).…”

“…S4). Prior work on HC ablation (at P2) using the Pou4f3 DTR/+ allele similarly found elevated auditory thresholds in adult animals (Mahrt et al, 2013). In summary, the absence of Pou4f3 in HCs and/or the degeneration of surrounding SCs might have contributed to the poor survival of regenerating HCs and, consequently, to hearing loss.…”

“…To circumvent this limitation, we developed two genetic methods to damage neonatal HCs in vivo. First, we used a knock-in mouse in which expression of the human diphtheria toxin receptor (DTR) is driven by the Pou4f3 promoter (Pou4f3 DTR/+ ) (Golub et al, 2012;Mahrt et al, 2013;Tong et al, 2011) and selective HC death is induced by injection of diphtheria toxin (DT), as Pou4f3 is exclusively expressed by HCs in the inner ear (Erkman et al, 1996;Xiang et al, 1998). Progressive HC death was observed in Pou4f3 DTR/+ mice after DT injection at P1 (Fig.…”

Evidence for an audience effect in mice: male social partners alter the male vocal response to female cues

“…We categorized vocalizations as simple (1 frequency-modulated segment) or complex (>1 frequency-modulated segment), and then further divided simple vocalizations into upsweep (>5 kHz change), downsweep (<−5 kHz change) and flat (≤|5| kHz change) syllable types based on their frequency bandwidth and modulation slope (Mahrt et al, 2013;Panksepp et al, 2007;Scattoni et al, 2008). The proportions of complex vocalizations, upsweeps, downsweeps and flats were compared between individual experiments from the Summed-solo-female-odor (N=16) and Paired-female-odor (N=16) conditions (Wilcoxon signed rank test), the Male-body-odor (N=18) and Male-body-odor-control (N=18) conditions (Wilcoxon signed rank test), the Male-body-odor (N=18) and Paired-female-odor (N=20) conditions (Wilcoxon rank sum test), the Anesthetized-male (N=15) and Solo-female-odor (N=22) conditions (Wilcoxon rank sum test), and the Anesthetized-male (N=15) and Paired-femaleodor (N=20) conditions (Wilcoxon rank sum test).…”

Expression analysis of the speech-related genes FoxP1 and FoxP2 and their relation to singing behavior in two songbird species

“…Besides humans (Homo sapiens), no taxon of primates is capable of substantially modifying its vocal repertoire in response to experience. Moreover, most laboratory animals, including rodents, do not learn a substantial portion of their vocalizations (Kikusui et al, 2011;Arriaga et al, 2012;Mahrt et al, 2013). In striking contrast, thousands of songbird species share the trait of vocal learning with humans, enabling comparison of brain-behavior relationships among these taxa.…”