Evolution of Vertebrate Motor Systems for Acoustic and Electric Communication: Peripheral and Central Elements

Abstract

Among vertebrates, there are a number of different neuromuscular systems specialized for the production of acoustic and electric social communication signals. Each system involves distinct sets of striated muscles that are derived from paraxial mesodermal somites and are components of a peripheral effector or 'communication organ': the larynx and syrinx of tetrapods, the sonic swim bladder and electric organ of fishes. Each of these systems further exhibits species-typical characters ranging from the number of muscles involved to myofibrillar architecture. Given that communication uses striated muscle, its circuitry is seen to represent a modification of existing motor systems. Thus, it is not surprising that these systems share several features suggesting that common mechanical or developmental factors influence their evolution. Of prime importance in comparing central communication circuitry between fishes and tetrapods is that among tetrapods the sound-generating organs are a part of the ventilatory system and so their activity must be coordinated with other sets of neuromuscular units. Differences in the central pattern of circuitry are thus expected between fishes and tetrapods, as well as among tetrapods themselves, since ventilation mechanisms differ between taxa. Moreover, birds have independently evolved a vocal syrinx which is distinctly separate from their larynx.

Sound production to electric discharge: sonic muscle evolution in progress inSynodontisspp. catfishes (Mochokidae)

“…), it is possible that large evolutionary variation exists in protractor muscle specialization for sound production or EOD. The myogenic electrocytes of other electric fishes have evolved independently from a variety of non-sonic muscular precursors [8,13,48,49]. Synodontis protractor muscle, however, presents a unique example in which an electrocyte evolved from a fastcontracting sonic muscle that, in some species, retains the ability to contract in order to produce sounds.…”

Central pattern generators for social vocalization: Androgen-dependent neurophysiological mechanisms

“…The term 'vocal' is appropriate here, as the major groups of vocal vertebrates (frogs, birds, fish, mammals) share common embryonic origins for both the motoneurons and skeletal muscles involved in sound production, i.e., vocalization (Bass, 1989;Bass et al, 1994Bass et al, , 2005aBass and Baker, 1997). Two broad categories of acoustic communication signals that are also observed in fictive preparations (see later sections) are advertisement and agonistic calls that are mainly related to, respectively, mating and territoriality (inclusive of aggressive interactions).…”

“…We provide an extended discussion of batrachoidids for three main reasons. The first is the relative simplicity of the vocal CPG of batrachoidids that controls a single set of muscles, whereas vocalization in most other vertebrates involves multiple sets of vocal and respiratory muscles (Bass, 1989;Bass and Baker, 1997). Second, the studies of batrachoidids illustrate how the oscillatory-like activity of individual premotor and motor neurons is translated into the temporal attributes of vocalizations such as fundamental frequency and duration (Bass and Baker, 1990).…”

“…Anuran amphibians-For terrestrial amphibians (frogs and toads), like other terrestrial vertebrates, vocalization depends upon its coordination with respiration (Gans, 1974;Bass, 1989;Nowicki et al, 1992). Schmidt mapped out a "mating calling pattern generator" in Northern leopard frogs (Lithobates pipiens; formerly Rana pipiens, see Frost, 2006), mainly by using a combination of brain transections with local electrical microstimulation and evoked potential recordings in an isolated brain preparation from males (e.g., see Schmidt, 1976Schmidt, , 1992).…”

The Foam Production System of the Male Japanese Quail: Characterization of Structure and Function

“…The hormone sensitive neuromuscular systems involved in sexually dimorphic reproductive and communicative behaviors, in particular, have been exploited with great success. Examples of such systems include the song control system of oscine birds [Nottebohm and Arnold, 1976;Nottebohm, 1980;DeVoogd, 1986;Konishi, 1994], the vocal control systems of sonic fish [Bass, 1989] and Xenopus frogs [Kelly, 1988], and the system controlling penile reflexes in rats [Holmes et al, 1981;Sengelaub, 1989;Breedlove, 1992].…”