Sound production in piranhas is associated with modifications of the spinal locomotor pattern.

Marine Banse,Eric Parmentier,Boris P Chagnaud,Loïc Kéver,Alessia Huby

doi:10.1242/jeb.242336

Marine Banse, Eric Parmentier + Show 3 more

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https://doi.org/10.1242/jeb.242336

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Abstract

ABSTRACTIn piranhas, sounds are produced through the vibration of the swim bladder wall caused by the contraction of bilateral sonic muscles. Because they are solely innervated by spinal nerves, these muscles likely evolved from the locomotor hypaxial musculature. The transition from a neuromuscular system initially shaped for slow movements (locomotion) to a system that requires a high contraction rate (sound production) was accompanied with major peripheral structural modifications, yet the associated neural adjustments remain to this date unclear. To close this gap, we investigated the activity of both the locomotor and the sonic musculature using electromyography. The comparison between the activation patterns of both systems highlighted modifications of the neural motor pathway: (1) a transition from a bilateral alternating pattern to a synchronous activation pattern, (2) a switch from a slow- to a high-frequency regime, and (3) an increase in the synchrony of motor neuron activation. Furthermore, our results demonstrate that sound features correspond to the activity of the sonic muscles, as both the variation patterns of periods and amplitudes of sounds highly correspond to those seen in the sonic muscle electromyograms (EMGsonic). Assuming that the premotor network for sound production in piranhas is of spinal origin, our results show that the neural circuit associated with spinal motor neurons transitioned from the slow alternating pattern originally used for locomotion to a much faster simultaneous activation pattern to generate vocal signals.

Highlights

The ability to produce sounds for social communication is widespread across vertebrates, including fishes
While our knowledge about these neuronal circuits is often limited to the location of the motor neurons innervating the sound-producing muscles, with some notable exceptions (Bass et al, 2015), the activation patterns recorded at the muscles or the nerves innervating those muscles allow us to readily identify some shared and divergent properties of the sound-generating circuits
These sonic muscles insert on transverse enlargements at the base of the second ribs articulating on the third vertebrae and are connected with a common broad tendon that surrounds the swim bladder ventrally (Ladich and Bass, 2005)

Summary

Introduction

The ability to produce sounds for social communication (courtship, spawning, agonistic behavior, competitive feeding, etc.) is widespread across vertebrates, including fishes It has evolved independently in many phylogenetically distinct fish taxa, the existence of several types of sound-producing mechanisms (Fine and Parmentier, 2015). One of the mechanisms to produce such acoustic signals originates from contractions of paired muscles associated with the swim bladder (Parmentier and Fine, 2016). In piranhas, these sonic muscles insert on transverse enlargements at the base of the second ribs articulating on the third vertebrae and are connected with a common broad tendon that surrounds the swim bladder ventrally (Ladich and Bass, 2005). In many other sonic teleosts, sonic swim bladder muscles are innervated by occipital nerve roots or by a combination of spinal and occipital nerve roots (for review, see Ladich and Bass, 1998, 2005)

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