The Medullary Audio-Vocal Network in the Toad Bombina orientalis.

Abstract

Anurans are an established paradigm to study vocal mechanisms in vertebrates. Regarding the motor patterns, airborne vocalization of most evolutionarily old anurans (Archaeobatrachia) resembles breathing-that is, lung inflation is used to generate sound. Vocal behavior and call timing can be rapidly elicited or modulated by auditory stimulation so that, for example, calls are uttered antiphonally in a chorus to avoid acoustic overlap. Accordingly, in an in vitro preparation of the isolated whole brain of the Chinese fire-bellied toad, Bombina orientalis, motor patterns similar to those of respiration and vocalization can be elicited reliably by stimulation of the posterior (auditory) branchlet of the statoacoustic nerve (N. VIII). Here, we show that audio-vocal integration does not exclusively involve higher brain centers such as mesencephalic torus semicircularis (colliculus inferior) but is in parallel and more rapidly accomplished within the medulla oblongata. We recorded 228 neurons in the areas of motor nuclei of Nn. V, X, and XII. Hypoglossal motor neurons showed fast activation (latency of the first action potential: 9.9 ± 2.3 ms), exceeded by the very fast activation of interneurons within the hypoglossal area (minimum latency of action potential peak 2.9 ms) after N. VIII stimulation. These data support the idea that the area between the roots of the vagal (N. X) and hypoglossal (N. XII) nerves may be a crucial part of the breathing rhythm generator. It suggests that the hypoglossal area plays an important role in controlling the other motor nuclei involved in vocalization. Thus, this post-vagal area may be an important supplementary interface of audio-vocal integration to initiate and coordinate vocal motor patterns and probably inhibit buccal respiration. With this information, a hypothetical motor network of buccal and lung ventilation, as well as vocalization, was constructed.