Courtship behaviour reveals temporal regularity is a critical social cue in mouse communication

Abstract

While animals navigating the real world face a barrage of complex sensory input, their brains have evolved to perceptually compress multidimensional information by selectively extracting the features relevant for survival. For instance, communication signals supporting social interactions in several mammalian species consist of acoustically complex sequences of vocalizations, however little is known about what information listeners extract from such timevarying sensory streams. Here, we utilize female mice's natural behavioural response to male courtship songs to evaluate the relevant acoustic dimensions used in their social decisions. We found that females were highly sensitive to disruptions of song temporal regularity, and preferentially approached playbacks of intact male songs over rhythmically irregular versions of the songs. In contrast, female behaviour was invariant to manipulations affecting the songs' sequential organization, or the spectrotemporal structure of individual syllables. The results reveal temporal regularity as a key acoustic cue extracted by mammalian listeners from complex vocal sequences during goal-directed social behaviour.

Vocalization categorization behavior explained by a feature-based auditory categorization model

“…The tempo manipulations lengthened or shortened both syllables and inter-syllable intervals (ISIs). Because a recent study in mice ( Perrodin et al, 2020 ) suggested that the regularity of ISI values might be crucial for the detection of male courtship songs by female mice, we next asked whether GPs used individual syllables or temporal patterns of calls for call categorization. First, as a low-level control, we replaced the ISIs of calls with silence instead of the low level of background noise present in recordings to ensure that GPs were not depending on any residual ISI information (silent ISI).…”

“…Whereas the specific parameters of a given call utterance might carry rich information about the identity ( Boinski and Mitchell, 1997 ; Miller et al, 2010 ; Gamba et al, 2012 ; Fukushima et al, 2015 ) and internal state of the caller as well as social context ( Seyfarth and Cheney, 2003 ; Coye et al, 2016 ), call category identity encompasses all these variations. In some behavioral situations, listeners might need to be sensitive to these specific parameter variations—for example, for courtship, female mice have been shown to exhibit a high preference for temporal regularity of male calls ( Perrodin et al, 2020 ). But in other situations, animals must and do generalize over this variability to extract call category identity, which is critical for providing an appropriate behavioral response.…”

Vocalization categorization behavior explained by a feature-based auditory categorization model

“…The tempo manipulations lengthened or shortened both syllables and inter-syllable intervals (ISIs). Because a recent study in mice (Perrodin et al, 2020) suggested that regularity of ISI values might be crucial for detection of male courtship songs by female mice, we next asked whether GPs used individual syllables or temporal patterns of calls for call categorization. First, as a low-level control, we replaced the ISIs of calls with silence instead of the low level of 13 background noise present in recordings to ensure that GPs were not depending on any residual ISI information (silent ISI).…”

“…Whereas the specific parameters of a given call utterance might carry rich information about the identity (Boinski and Mitchell, 1997; Miller et al, 2010; Gamba et al, 2012; Fukushima et al, 2015) and internal state of the caller as well as social context (Seyfarth and Cheney, 2006; Coye et al, 2016), call category identity encompasses all these variations. In some behavioral situations, listeners might need to be sensitive to these specific parameter variations - for example, for courtship, female mice have been shown to exhibit a high preference for temporal regularity of male calls (Perrodin et al, 2020). But in other situations, animals must and do generalize over this variability to extract call identity, which is critical for providing an appropriate behavioral response.…”

Analysis of Mouse Vocal Communication (AMVOC): A deep, unsupervised method for rapid detection, analysis, and classification of ultrasonic vocalizations

“…Over the past two decades there has been a growing interest in the usage and signaling of vocalizations in mice, with large efforts going into studying the underlying neurobiological mechanisms for auditory processing (Pomerantz et al, 1983;Liu et al, 2003;Neilans et al, 2014;Perrodin et al, 2020;Holy and Guo, 2005), and the production of vocalizations (Arriaga et al, 2012;Chabout et al, 2016;Okobi et al, 2019;Zimmer et al, 2019;Gao et al, 2019;Tschida et al, 2019;Michael et al, 2020). The tools available for experiments in mice provide a promising model for studying the neural basis of vocalizations, as well as the effects of genes on the origin and development of vocal and neural anatomy (Grimsley et al, 2011;Bowers et al, 2013;Chabout et al, 2016;Tabler et al, The copyright holder for this preprint this version posted August 13, 2021. ; https://doi.org/10.1101/2021.08.13.456283 doi: bioRxiv preprint (Steinfath et al, 2021).…”