The return to water in ancestral Xenopus was accompanied by a novel mechanism for producing and shaping vocal signals

Abstract

Listeners locate potential mates using species-specific vocal signals. As tetrapods transitioned from water to land, lungs replaced gills, allowing expiration to drive sound production. Some frogs then returned to water. Here we explore how air-driven sound production changed upon re-entry to preserve essential acoustic information on species identity in the secondarily aquatic frog genus Xenopus. We filmed movements of cartilage and muscles during evoked sound production in isolated larynges. Results refute the current theory for Xenopus vocalization, cavitation, and favor instead sound production by mechanical excitation of laryngeal resonance modes following rapid separation of laryngeal arytenoid discs. Resulting frequency resonance modes (dyads) are intrinsic to the larynx rather than due to neuromuscular control. Dyads are a distinctive acoustic signature. While their component frequencies overlap across species, their ratio is shared within each Xenopus clade providing information on species identity that could facilitate both conspecific localization and ancient species divergence.Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (see decision letter).

Gap junction-mediated glycinergic inhibition ensures precise temporal patterning in vocal behavior

“…A gap junction-mediated, feed-forward glycinergic inhibition could account for temporal patterning in the millisecond time range that characterizes the vocal network and behavior of toadfishes ( Pappas and Bennett, 1966 ; Bass and Baker, 1991 ; Chagnaud et al, 2011 ; Chagnaud et al, 2012 ). A similar mechanism has previously been shown for the Mauthner cell escape circuit ( Furukawa and Furshpan, 1963 ; Diamond and Roper, 1973 ; Diamond et al, 1973 ; Faber et al, 1989 ; Zottoli and Faber, 2000 ; Korn and Faber, 2005 ; Sillar, 2009 ) and may operate in other vocal systems in teleosts and tetrapods that are dependent on comparable levels of temporal precision ( Sturdy et al, 2003 ; Rome, 2006 ; Bass et al, 2015 ; Mead et al, 2017 ; Nelson et al, 2018 ; Kwong-Brown et al, 2019 ).…”

“…Teleost families with evidence for soniferous behavior contain nearly two-thirds of actinopterygian species ( Rice et al, 2020 ). Concurrent activation of neurons required for rapid and precise activation of muscle groups underlying acoustic signaling in different lineages of fishes ( Chagnaud et al, 2012 ; Kéver et al, 2020 ) and in tetrapods ( Mead et al, 2017 ; Kwong-Brown et al, 2019 ) might all benefit from gap junction-mediated glycinergic inhibition.…”

“…Mechanisms known to increase precision at single cell and network levels include, for instance, feed-forward inhibition in auditory circuits ( Grothe, 2003 ), recurrent inhibitory input in cerebral cortex ( Kapfer et al, 2007 ), and neuronal synchrony in cortical and sensory neurons ( Tiesinga and Sejnowski, 2001 ; Uhlhaas et al, 2010 ). Synchronous, concurrent activation of neurons is widely distributed in the brain ( Llinás, 2014 ) and especially important for behaviors requiring both rapid and precise motoneuron activation such as electrogenesis in fishes ( Bennett, 1971 ) and vocalization in fishes ( Chagnaud et al, 2012 ) and tetrapods ( Mead et al, 2017 ; Kwong-Brown et al, 2019 ).…”

“…Unlike motor systems controlling locomotion and respiration ( Ramirez and Baertsch, 2018 ; Grillner and El Manira, 2020 ), in-depth inquiries of cellular and network properties of brainstem neurons influencing acoustic signaling remain relatively unexplored, despite advances in characterizing the musculoskeletal periphery ( Mead et al, 2017 ; Kwong-Brown et al, 2019 ; Riede et al, 2019 ; Bowling et al, 2020 ). A neurobehavioral challenge often facing soniferous species is fine temporal control of rapid modulations of acoustic waveforms.…”

A novel degree of sex difference in laryngeal physiology of Xenopus muelleri: behavioral and evolutionary implications

“…The isolated larynx is physiologically robust for several hours ex vivo (Leininger et al, 2015;Potter et al, 2005;Tobias and Kelley, 1987). Stimulation of the laryngeal nerve is sufficient to elicit laryngeal muscle contraction, which separates cartilage discs necessary for sound pulse production (Kwong-Brown et al, 2019). Thus, the ex vivo larynx is a simple neuromuscular circuit with robust ex vivo activity and straightforward correspondence between physiological mechanisms and behavioral features, described below.…”