One-to-one innervation of vocal muscles allows precise control of birdsong.

The motor control resolution of any animal behavior is limited to the minimal force step available when activating muscles, which is set by the number and size distribution of motor units (MUs) and muscle-specific force. Birdsong is an excellent model system for understanding acquisition and maintenance of complex fine motor skills, but we know surprisingly little about how the motor pool controlling the syrinx is organized and how MU recruitment drives changes in vocal output. Here we developed an experimental paradigm to measure MU size distribution using spatiotemporal imaging of intracellular calcium concentration in cross-sections of living intact syrinx muscles. We combined these measurements with muscle stress and an in vitro syrinx preparation to determine the control resolution of fundamental frequency (fo), a key vocal parameter, in zebra finches. We show that syringeal muscles have extremely small MUs, with 40%-50% innervating ≤3 and 13%-17% innervating a single muscle fiber. Combined with the lowest specific stress (5 mN/mm2) known to skeletal vertebrate muscle, small force steps by the major fo controlling muscle provide control of 50-mHz to 7.3-Hz steps per MU. We show that the song system has the highest motor control resolution possible in the vertebrate nervous system and suggest this evolved due to strong selection on fine gradation of vocal output. Furthermore, we propose that high-resolution motor control was a key feature contributing to the radiation of songbirds that allowed diversification of song and speciation by vocal space expansion.

Syringeal vocal folds do not have a voice in zebra finch vocal development.

Vocal behavior can be dramatically changed by both neural circuit development and postnatal maturation of the body. During song learning in songbirds, both the song system and syringeal muscles are functionally changing, but it is unknown if maturation of sound generators within the syrinx contributes to vocal development. Here we densely sample the respiratory pressure control space of the zebra finch syrinx in vitro. We show that the syrinx produces sound very efficiently and that key acoustic parameters, minimal fundamental frequency, entropy and source level, do not change over development in both sexes. Thus, our data suggest that the observed acoustic changes in vocal development must be attributed to changes in the motor control pathway, from song system circuitry to muscle force, and not by material property changes in the avian analog of the vocal folds. We propose that in songbirds, muscle use and training driven by the sexually dimorphic song system are the crucial drivers that lead to sexual dimorphism of the syringeal skeleton and musculature. The size and properties of the instrument are thus not changing, while its player is.

Great cormorants (Phalacrocorax carbo) can detect auditory cues while diving.

In-air hearing in birds has been thoroughly investigated. Sound provides birds with auditory information for species and individual recognition from their complex vocalizations, as well as cues while foraging and for avoiding predators. Some 10% of existing species of birds obtain their food under the water surface. Whether some of these birds make use of acoustic cues while underwater is unknown. An interesting species in this respect is the great cormorant (Phalacrocorax carbo), being one of the most effective marine predators and relying on the aquatic environment for food year round. Here, its underwater hearing abilities were investigated using psychophysics, where the bird learned to detect the presence or absence of a tone while submerged. The greatest sensitivity was found at 2 kHz, with an underwater hearing threshold of 71 dB re 1 µPa rms. The great cormorant is better at hearing underwater than expected, and the hearing thresholds are comparable to seals and toothed whales in the frequency band 1-4 kHz. This opens up the possibility of cormorants and other aquatic birds having special adaptations for underwater hearing and making use of underwater acoustic cues from, e.g., conspecifics, their surroundings, as well as prey and predators.

In-air hearing of the great cormorant (Phalacrocorax carbo).

Many aquatic birds use sounds extensively for in-air communication. Regardless of this, we know very little about their hearing abilities. The in-air audiogram of a male adult great cormorant (Phalacrocorax carbo) was determined using psychophysical methods (method of constants). Hearing thresholds were derived using pure tones of five different frequencies. The lowest threshold was at 2 kHz: 18 dB re 20 µPa rms. Thresholds derived using signal detection theory were within 2 dB of the ones derived using classical psychophysics. The great cormorant is more sensitive to in-air sounds than previously believed and its hearing abilities are comparable to several other species of birds of similar size. This knowledge is important for our understanding of the hearing abilities of other species of sea birds. It can also be used to develop cormorant deterrent devices for fisheries, as well as to assess the impact of increasing in-air anthropogenic noise levels on cormorants and other aquatic birds.