Vertebrate Evolution Conserves Hindbrain Circuits despite Diverse Feeding and Breathing Modes

Abstract

Feeding and breathing are two functions vital to the survival of all vertebrate species. Throughout the evolution, vertebrates living in different environments have evolved drastically different modes of feeding and breathing through utilizing diversified orofacial and pharyngeal (oropharyngeal) muscles. The oropharyngeal structures are controlled by hindbrain neural circuits. The developing hindbrain shares strikingly conserved organizations and gene expression patterns across vertebrates, thus begs the question of how a highly conserved hindbrain generates circuits subserving diverse feeding/breathing patterns. In this review, we summarize major modes of feeding and breathing and principles underlying their coordination in many vertebrate species. We provide a hypothesis for the existence of a common hindbrain circuit at the phylotypic embryonic stage controlling oropharyngeal movements that is shared across vertebrate species; and reconfiguration and repurposing of this conserved circuit give rise to more complex behaviors in adult higher vertebrates. SIGNIFICANCE STATEMENT Understanding how a highly conserved hindbrain generates diverse feeding/breathing patterns is important for elucidating neural mechanisms underlying the execution and coordination of these two vital behaviors. Here, we first briefly summarize key modes of vertebrates feeding/breathing, discuss main principles coordinating feeding/breathing, and provide a unifying hypothesis for the existence of a shared oropharyngeal movement control circuit across species. By synthesizing behavior, structural and neural mechanisms for feeding/breathing functions across evolution, we believe that this review and our hypothesis can open new research avenues for elucidating the precise hindbrain circuits controlling feeding, breathing and other oropharyngeal functions.

Early development of respiratory motor circuits in larval zebrafish (Danio rerio)

“…The identities of the premotor neurons in the teleost respiratory motor circuit are not known. Some evidence suggests that there are multiple sources of rhythmic respiratory drive to cranial motor neurons along the rostrocaudal axis of the hindbrain in adult goldfish (Duchcherer et al., 2010), consistent with the distributed rhythmic respiratory network observed in other ectothermic vertebrates (Kinkead, 2009; Li & Wang, 2021; Milsom, 2008; Taylor et al, 2010) and in mammals (Smith et al., 2013). However, the precise architecture of this distributed network in teleosts is unclear.…”

“…For example, vertebrates share mechanisms for the molecular specification of rhombomeres, which generate specific populations of cranial motor neurons at different rostrocaudal levels of the hindbrain (Bass & Baker, 1997; Frank & Sela‐Donenfeld, 2019; Gilland & Baker, 2005; Guthrie, 2007; Moens & Prince, 2002). Furthermore, the physiological functions controlled by circuits in the hindbrain are similar across phylogeny, and include neural circuits for feeding and breathing (Li & Wang, 2021).…”

“…For example, conserved rhythm generating centers in the hindbrain form synaptic connections with cranial and spinal motor neurons to generate coordinated, patterned respiratory behaviors (Bass & Baker, 1997; Kinkead, 2009; Mellen & Thoby‐Brisson, 2012; Milsom, 2008; Taylor et al., 2010). In terrestrial vertebrates, these rhythm‐generating circuits drive coordinated movements of the mouth, nose, and diaphragm to move air into and out of the lungs (reviewed in Li & Wang, 2021). In aquatic vertebrates, these circuits drive coordinated movements of the jaw, buccal cavity, and operculum to move water in through the mouth and out across the gills through the opercular openings.…”

“…In aquatic vertebrates, these circuits drive coordinated movements of the jaw, buccal cavity, and operculum to move water in through the mouth and out across the gills through the opercular openings. Li and Wang (2021) hypothesize that all vertebrates begin life with an ancestral hindbrain rhythmic motor circuit configuration that is then modified during development in different ways, to produce diverse motor outcomes across taxa. Understanding the earliest stages of respiratory motor circuit development in a vertebrate model—specifically, when critical synaptic connections form and how they change over time—will provide a foundation to investigate this possibility.…”