Probing forebrain to hindbrain circuit functions in Xenopus

Abstract

The vertebrate hindbrain includes neural circuits that govern essential functions including breathing, blood pressure and heart rate. Hindbrain circuits also participate in generating rhythmic motor patterns for vocalization. In most tetrapods, sound production is powered by expiration and the circuitry underlying vocalization and respiration must be linked. Perception and arousal are also linked; acoustic features of social communication sounds – e.g. a baby’s cry - can drive autonomic responses. The close links between autonomic functions that are essential for life and vocal expression have been a major in vivo experimental challenge. Xenopus provides an opportunity to address this challenge using an ex vivo preparation: an isolated brain that generates vocal and breathing patterns. The isolated brain allows identification and manipulation of hindbrain vocal circuits as well as their activation by forebrain circuits that receive sensory input, initiate motor patterns and control arousal. Advances in imaging technologies, coupled to the production of Xenopus lines expressing genetically encoded calcium sensors, provide powerful tools for imaging neuronal patterns in the entire fictively behaving brain, a goal of the BRAIN Initiative. Comparisons of neural circuit activity across species with distinctive vocal patterns (comparative neuromics) can identify conserved features, and thereby reveal essential functional components.

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

“…In Xenopus , social communication is dominated by vocal signaling (Kelley et al, 2017). Males in each species produce distinctive advertisement calls underwater whose acoustic features inform species identity (Evans et al, 2015).…”

Inhibitory and modulatory inputs to the vocal central pattern generator of a teleost fish

“…Evidence from electrophysiological studies in bats and monkeys, for instance, show the contribution of hindbrain neurons to the determination of the amplitude, duration, and frequency of vocal signals (Jürgens & Hage, ; Rübsamen & Betz, ; Schuller & Rübsamen, ; Suthers & Goller, ; Vicario, ). The most comprehensive investigations of vocal CPGs, however, originate from studies of amphibians (Kelley et al, ; Schmidt, ; Yamaguchi, Kaczmarek, & Kelley, ; Zornik & Yamaguchi, ) and fish (Bass, ; Bass & Baker, ; Bass, Chagnaud, & Feng, ).…”

“…The most comprehensive investigations of vocal CPGs, however, originate from studies of amphibians (Kelley et al, 2017;Schmidt, 1992;Yamaguchi, Kaczmarek, & Kelley, 2000;Zornik & Yamaguchi, 2012) and fish (Bass, 2014;Bass & Baker, 1990;Bass, Chagnaud, & Feng, 2015).…”

“…While the organization of vocal CPGs has been investigated at network and single neuron levels for toadfishes and the African clawed frog Xenopus laevis (e.g., Bass & Baker, 1990;Chagnaud et al, 2011;Chagnaud et al, 2012;Kelley et al, 2017;Yamaguchi et al, 2000;Zornik & Yamaguchi, 2012), less is known about the neurochemicals that modulate their activity (e.g., Forlano, Kim, Krzyminska, and Sisneros, 2014;Yu & Yamaguchi, 2010;Zornik, Katzen, Rhodes, and Yamaguchi, 2010). The well-established neuroanatomical and neurophysiological characterization of the vocal CPG in species such as the Gulf toadfish, Opsanus beta, together with the ability to unambiguously identify each vocal CPG nucleus via transneuronal neurobiotin labeling, present a distinct opportunity to investigate the neurochemical profile of each component of an evolutionarily conserved vertebrate vocal CPG (Bass et al, 2008;Chagnaud & Bass, 2014).…”

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

“…In Xenopus, social communication is dominated by vocal signaling. 5 Males in each species produce distinctive advertisement calls underwater whose acoustic features inform species identity. 4 These calls consist of a series of sound pulses that form species-typical temporal patterns and characteristically include two dominant frequencies (DFs).…”