Determinants of the mouse ultrasonic vocal structure and repertoire

Heckman, J.; McGuinness, Brigit; Celikel, Tansu; Englitz, Bernhard

doi:10.1016/j.neubiorev.2016.03.029

Cited by 77 publications

(83 citation statements)

References 93 publications

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“…Mouse USVs are known to be highly variable (Heckman et al, 2016), and it was unclear a priori what features of vocalizations might be modified, therefore in addition to measures of basic acoustic properties, we used an analysis method that takes into account the entire structure of the vocal repertoire to ask if subtler differences in vocal phenotype might be present in our mutant mice. From our 9000+ calls, we constructed a map of the vocal repertoire space in which vocalizations with similar frequency contours occupy adjacent regions in the map (Figure 9A–C; see Materials and methods for details).…”

Section: Resultsmentioning

confidence: 99%

“…The ultrasonic calls of rodents have emerged as a useful model for studies of mammalian vocalization (Arriaga et al, 2012; Fischer and Hammerschmidt, 2011) (Heckman et al, 2016; Portfors and Perkel, 2014). Unlike the audible vocalizations generated by vibrations due to the pressure differential across the apposed vocal folds, rodent USVs are generated by a planar impinging air jet (Mahrt et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

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Cilia-mediated Hedgehog signaling controls form and function in the mammalian larynx

Tabler

Rigney

Berman

et al. 2017

eLife

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Acoustic communication is fundamental to social interactions among animals, including humans. In fact, deficits in voice impair the quality of life for a large and diverse population of patients. Understanding the molecular genetic mechanisms of development and function in the vocal apparatus is thus an important challenge with relevance both to the basic biology of animal communication and to biomedicine. However, surprisingly little is known about the developmental biology of the mammalian larynx. Here, we used genetic fate mapping to chart the embryological origins of the tissues in the mouse larynx, and we describe the developmental etiology of laryngeal defects in mice with disruptions in cilia-mediated Hedgehog signaling. In addition, we show that mild laryngeal defects correlate with changes in the acoustic structure of vocalizations. Together, these data provide key new insights into the molecular genetics of form and function in the mammalian vocal apparatus.DOI: http://dx.doi.org/10.7554/eLife.19153.001

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Cilia-mediated Hedgehog signaling controls form and function in the mammalian larynx

Tabler

Rigney

Berman

et al. 2017

eLife

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“…These vocalizations are strongly modulated on different levels by a variety of contextual determinants, such as age, genetic background, behavioural state and to a lesser extent by sex 5 . Mice utilize these USVs during social interactions and in distress to mediate essential behaviours 6–12 .…”

Section: Introductionmentioning

confidence: 99%

High-precision spatial localization of mouse vocalizations during social interaction

Heckman

Proville

Heckman

et al. 2017

Sci Rep

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Mice display a wide repertoire of vocalizations that varies with age, sex, and context. Especially during courtship, mice emit ultrasonic vocalizations (USVs) of high complexity, whose detailed structure is poorly understood. As animals of both sexes vocalize, the study of social vocalizations requires attributing single USVs to individuals. The state-of-the-art in sound localization for USVs allows spatial localization at centimeter resolution, however, animals interact at closer ranges, involving tactile, snout-snout exploration. Hence, improved algorithms are required to reliably assign USVs. We develop multiple solutions to USV localization, and derive an analytical solution for arbitrary vertical microphone positions. The algorithms are compared on wideband acoustic noise and single mouse vocalizations, and applied to social interactions with optically tracked mouse positions. A novel, (frequency) envelope weighted generalised cross-correlation outperforms classical cross-correlation techniques. It achieves a median error of ~1.4 mm for noise and ~4–8.5 mm for vocalizations. Using this algorithms in combination with a level criterion, we can improve the assignment for interacting mice. We report significant differences in mean USV properties between CBA mice of different sexes during social interaction. Hence, the improved USV attribution to individuals lays the basis for a deeper understanding of social vocalizations, in particular sequences of USVs.

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“…Mice were previously shown to change their vocalization pattern in different contexts (Chabout et al, 2012, 2015; Yang et al, 2013; Mun et al, 2015; Srivastava et al, 2015; Gaub et al, 2016; Grimsley et al, 2016; Heckman et al, 2016; Hoier et al, 2016; Seagraves et al, 2016). We therefore hypothesized that head-fixation likely modulates USVs in comparison to non-restrained sessions.…”

Section: Resultsmentioning

confidence: 99%

“…Because not all mice vocalized, we tested several strategies to increase the probability of head-fixed vocalizations but none of these manipulations seemed to be effective. Several manipulations have been used in the past to increase vocalization performance including extended habituation and overnight female experience (Grimsley et al, 2011; Hanson and Hurley, 2012; Chabout et al, 2015; Ferhat et al, 2015; Heckman et al, 2016). In our hands, however, using these and additional methods on non-vocalizers produced little change.…”

Section: Discussionmentioning

confidence: 99%

Social Ultrasonic Vocalization in Awake Head-Restrained Mouse

Weiner

Hertz

Perets

et al. 2016

Front. Behav. Neurosci.

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Numerous animal species emit vocalizations in response to various social stimuli. The neural basis of vocal communication has been investigated in monkeys, songbirds, rats, bats, and invertebrates resulting in deep insights into motor control, neural coding, and learning. Mice, which recently became very popular as a model system for mammalian neuroscience, also utilize ultrasonic vocalizations (USVs) during mating behavior. However, our knowledge is lacking of both the behavior and its underlying neural mechanism. We developed a novel method for head-restrained male mice (HRMM) to interact with non-restrained female mice (NRFM) and show that mice can emit USVs in this context. We first recorded USVs in a free arena with non-restrained male mice (NRMM) and NRFM. Of the NRMM, which vocalized in the free arena, the majority could be habituated to also vocalize while head-restrained but only when a female mouse was present in proximity. The USVs emitted by HRMM are similar to the USVs of NRMM in the presence of a female mouse in their spectral structure, inter-syllable interval distribution, and USV sequence length, and therefore are interpreted as social USVs. By analyzing the vocalizations of NRMM, we established criteria to predict which individuals are likely to vocalize while head fixed based on the USV rate and average syllable duration. To characterize the USVs emitted by HRMM, we analyzed the syllable composition of HRMM and NRMM and found that USVs emitted by HRMM have a higher proportion of USVs with complex spectral representation, supporting previous studies showing that mice social USVs are context dependent. Our results suggest a way to study the neural mechanisms of production and control of social vocalization in mice using advanced methods requiring head fixation.

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Determinants of the mouse ultrasonic vocal structure and repertoire

Cited by 77 publications

References 93 publications

Cilia-mediated Hedgehog signaling controls form and function in the mammalian larynx

Cilia-mediated Hedgehog signaling controls form and function in the mammalian larynx

High-precision spatial localization of mouse vocalizations during social interaction

Social Ultrasonic Vocalization in Awake Head-Restrained Mouse

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