Abstract:The anatomical overlap of the pathways for air passage and nutrition necessitate precise coordination between the two vital functions. Neuroanatomic structures in the brainstem for sucking, breathing, and swallowing are also in close proximity and must swiftly coordinate the processes. In a healthy neonate, the oropharyngeal experience and stimulation of early feeding enables respiratory control during suckling to develop. Despite wide variability among the methods used to investigate breathing and swallowing … Show more
“…Therefore, bringing fluid into the mouth to be swallowed is likely the fundamental process common to all developing vertebrates. For example, it is known that fetal swallowing of amniotic fluid emerges right after major organogenesis around 10–14 weeks of gestation in human and is observed in early development of chicks, sheep, rodents, and monkeys ( Ross and Nijland, 1998 ; Delaney and Arvedson, 2008 ; Mashayekhi et al, 2011 ; Gross and Trapani-Hanasewych, 2017 ; Maynard et al, 2020 ). This process of transporting fluid into the body is repeatedly executed and requires coordinated activation of oropharyngeal muscles ( Sherman et al, 1990 ).…”
Section: A Hypothesis: How Conserved Embryonic Hindbrain Generates Circuits For Diverse Modes Of Feeding and Breathingmentioning
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.
“…Therefore, bringing fluid into the mouth to be swallowed is likely the fundamental process common to all developing vertebrates. For example, it is known that fetal swallowing of amniotic fluid emerges right after major organogenesis around 10–14 weeks of gestation in human and is observed in early development of chicks, sheep, rodents, and monkeys ( Ross and Nijland, 1998 ; Delaney and Arvedson, 2008 ; Mashayekhi et al, 2011 ; Gross and Trapani-Hanasewych, 2017 ; Maynard et al, 2020 ). This process of transporting fluid into the body is repeatedly executed and requires coordinated activation of oropharyngeal muscles ( Sherman et al, 1990 ).…”
Section: A Hypothesis: How Conserved Embryonic Hindbrain Generates Circuits For Diverse Modes Of Feeding and Breathingmentioning
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.
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