Abstract
Humans and song-learning birds communicate acoustically using learned vocalizations. The characteristic features of this social communication behavior include vocal control by forebrain motor areas, a direct cortical projection to brainstem vocal motor neurons, and dependence on auditory feedback to develop and maintain learned vocalizations. These features have so far not been found in closely related primate and avian species that do not learn vocalizations. Male mice produce courtship ultrasonic vocalizations with acoustic features similar to songs of song-learning birds. However, it is assumed that mice lack a forebrain system for vocal modification and that their ultrasonic vocalizations are innate. Here we investigated the mouse song system and discovered that it includes a motor cortex region active during singing, that projects directly to brainstem vocal motor neurons and is necessary for keeping song more stereotyped and on pitch. We also discovered that male mice depend on auditory feedback to maintain some ultrasonic song features, and that sub-strains with differences in their songs can match each other's pitch when cross-housed under competitive social conditions. We conclude that male mice have some limited vocal modification abilities with at least some neuroanatomical features thought to be unique to humans and song-learning birds. To explain our findings, we propose a continuum hypothesis of vocal learning.
Highlights
Male mice are known to produce ultrasonic vocalizations (USVs) in a mating context, and these have been assumed to be exclusively innate [1]
Experienced adult males of the same B6D2F1/J strain used by Holy and Guo [2] were isolated overnight and divided into four groups: Non-Singing; Hearing Only; Hearing & Singing; and Deaf-Singing
We performed experiments in mice that tested for the presence of five important features traditionally considered to exist as a package unique to vocal learning species: forebrain activation, direct cortical to vocal motor neuron connectivity, forebrain control, auditory feedback, and vocal imitation
Summary
Male mice are known to produce ultrasonic vocalizations (USVs) in a mating context, and these have been assumed to be exclusively innate [1]. A recent seminal study by Holy and Guo [2] demonstrated that features of male mouse USVs have some characteristics of song behaviors observed in songbirds (Figure 1A; sound recording in Audio S1) These features include the following: melodic structure of the vocalizations; sequential vocal structure unlike ‘calls’ which by definition are isolated or repeated syllables of typically one type; syllables produced in a non-random sequence with repeated motifs; and individual differences in repertoire composition. For these and other reasons, Holy and Guo called these male USVs ‘mouse songs’ [2]. The discovery of USV song in mice opened the question of whether mice share any behavioral and neural mechanisms for song production and learning with the set of rare vocal learning species, which includes three groups of birds (songbirds, parrots, hummingbirds) and several groups of mammals (humans, cetaceans [dolphins and whales], bats, elephants, and pinnipeds [sea lions and seals]) [5,6,7]
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