Abstract
Birdsong is a widely used model for vocal learning and human speech, which exhibits high temporal and acoustic diversity. Rapid acoustic modulations are thought to arise from the vocal organ, the syrinx, by passive interactions between the two independent sound generators or intrinsic nonlinear dynamics of sound generating structures. Additionally, direct neuromuscular control could produce such rapid and precisely timed acoustic features if syringeal muscles exhibit rare superfast muscle contractile kinetics. However, no direct evidence exists that avian vocal muscles can produce modulations at such high rates. Here, we show that 1) syringeal muscles are active in phase with sound modulations during song over 200 Hz, 2) direct stimulation of the muscles in situ produces sound modulations at the frequency observed during singing, and that 3) syringeal muscles produce mechanical work at the required frequencies and up to 250 Hz in vitro. The twitch kinematics of these so-called superfast muscles are the fastest measured in any vertebrate muscle. Superfast vocal muscles enable birds to directly control the generation of many observed rapid acoustic changes and to actuate the millisecond precision of neural activity into precise temporal vocal control. Furthermore, birds now join the list of vertebrate classes in which superfast muscle kinetics evolved independently for acoustic communication.
Highlights
Some of the most complex vocal communication signals in the animal kingdom are produced by songbirds [1], whose songs often contain long sequences of rapidly modulated sound elements [2]
Rapid acoustic modulations (,10 ms) during song can arise from passive interactions between the two independent sound generators in the vocal organ – the syrinx [3] and intrinsic nonlinear dynamics of sound generating structures [e.g. 4–7]
We present direct evidence that songbird have superfast syringeal muscles, which can modulate song acoustics up to 250 Hz
Summary
Some of the most complex vocal communication signals in the animal kingdom are produced by songbirds [1], whose songs often contain long sequences of rapidly modulated sound elements [2]. The variation in temporal characteristics of song in zebra finches (Taenopygia guttata) correlates with variation in the spiking patterns of neurons in premotor brain nuclei [8,9,11,12,14], which suggests that the temporal precision of the CNS can be expressed at the behavioral level of song production. Both findings are consistent with very fast muscular control of the vocal production system of songbirds. To our knowledge no direct evidence exists that avian vocal muscles can produce modulations at such high rates
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