Evolutionary Origins for Social Vocalization in a Vertebrate Hindbrain–Spinal Compartment

Abstract

The macroevolutionary events leading to neural innovations for social communication, such as vocalization, are essentially unexplored. Many fish vocalize during female courtship and territorial defense, as do amphibians, birds, and mammals. Here, we map the neural circuitry for vocalization in larval fish and show that the vocal network develops in a segment-like region across the most caudal hindbrain and rostral spinal cord. Taxonomic analysis demonstrates a highly conserved pattern between fish and all major lineages of vocal tetrapods. We propose that the vocal basis for acoustic communication among vertebrates evolved from an ancestrally shared developmental compartment already present in the early fishes.Although the genetic basis for human speech receives much attention [e.g., (1,2)], the fundamental issue of the ancestral origins of neural networks for vocal signaling is essentially unexplored. Social, context-dependent acoustic communication occurs in most of the major vertebrate lineages, including fishes (Fig. 1A). Teleost fish, the most species-rich of all vertebrate groups (3), have a simple repertoire of vocalizations complemented by vocal and auditory pathways that are organized similarly to those of amphibians, reptiles, birds, and mammals (4). Batrachoidid fish (midshipman and toadfish), in particular, have an expansive vocal-acoustic network, including a rhythmically firing, pacemaker-motor neuron circuit that directly determines the contraction rate of vocal muscles attached to the swim bladder and, in turn, the temporal properties of calls (5,6) ( Fig. 1B and fig. S1; movies S1 to S3). Because batrachoidids also have readily studied larval stages (7), they were chosen to investigate the hypothesis that fish and terrestrial vertebrates share an ancestral origin of their vocal motor networks. Here, we show that the vocal systems of fishes and tetrapods develop very similarly in a segment-like region that forms a transitional compartment between the caudal hindbrain and rostral spinal cord.

The von Economo neurons in frontoinsular and anterior cingulate cortex in great apes and humans

“…Craig (2005) suggests that sympathetic activation on the right side and consequent energy expenditure by the organism, and parasympathetic activation on the left and energy conservation together function to serve as a balancing mechanism for managing the organism's energy resources. These mechanisms involve in part highly conserved circuits in the vagal complex that regulate respiration and the production of vocalizations throughout vertebrates (Bass et al 2008).…”

Functional morphology of theAlligator mississippiensislarynx with implications for vocal production

“…Unifying control and design principles among the ancestral, derived and more distantly related groups (mammals) indicate functional constraints that may make it possible to discern vocal capabilities in extinct groups (e.g. Bass et al, 2008). This study contributes to these efforts because birds and crocodilians are sister taxa that bracket pterosaurs and non-avian dinosaurs, and thus these results shed some light on possible vocal fold morphology and function in the ancestral archosaur.…”

Coding Rate and Duration of Vocalizations of the Frog,Xenopus laevis

“…Despite this difference, it is noteworthy that rate and duration in both species appear to be regulated by the same cellular mechanisms, STOs and LLDs, respectively. Hindbrain circuits controlling vocal production in fishes, frogs, birds, and mammals may have derived from a common ancestor (Bass et al, 2008). Although intracellular recordings of hindbrain neurons have not been obtained in mammals or birds during vocalizations, it is possible that similar cellular mechanisms are involved in temporal coding.…”