Activation of XII motoneurons and premotor neurons during various oropharyngeal behaviors
Introduction
Central mechanisms that drive upper airway motoneurons in response to sensory stimuli are still not sufficiently investigated. In particular, little is known on how the central nervous system generates and coordinates different motor programs involving overlapping groups of muscles. This problem of integrated physiology has been preferentially addressed with cellular analyses of fictive oromotor behavior using various in vivo animal models (Gestreau et al., 1996, Gestreau et al., 2000, Ono et al., 1994, Ono et al., 1998a, Ono et al., 1998b, Peever et al., 2002, Roda et al., 2002, Sahara et al., 1996, Saito et al., 2003, Shannon et al., 2004, Shiba et al., 1999), and studies in humans (for review, see Remmers, 2001).
The rich sensory modalities of the oral cavity are able to trigger a broad range of reflexes that ultimately influence hypoglossal (XII) muscle activity (Miller, 2002). This diversity of oropharyngeal behaviors in which tongue muscles are involved constitutes a good framework to (i) analyze changes in XII motor output, (ii) delineate neural substrates related to these functions, and (iii) improve the understanding of neural mechanisms orchestrating specific motor programs required for the coordination of complex oropharyngeal behaviors. Indeed, motor programs related to breathing, swallowing, licking, mastication, gaping, gagging, coughing, sneezing, vocalization, and vomiting are controlled by brainstem neural networks that all impact on XII motoneurons (Bianchi et al., 1995, Ertekin and Aydogdu, 2003, Jean, 2001, Lund et al., 1998, Travers et al., 1997, Chen et al., 2001, Chen and Travers, 2003).
Excellent reviews exist on the neural control of tongue movements with respect to breathing, swallowing, licking, mastication and/or vomiting (Lowe, 1981, Miller, 2002, Sawczuk and Mosier, 2001, Travers et al., 1997), but new results have been published that highlight our understanding of central organization of oropharyngeal behaviors at the level of XII motor and premotor neurons. Therefore, the aim of this review is to discuss available literature on motor and premotor control of XII activity with a special emphasis on breathing, swallowing and coughing. Data concerning activities of XII premotor neurons during licking, mastication, and rejection (gaping) are also considered.
Section snippets
Tongue muscles, movements, and myotopic organization of XII nucleus
The tongue is composed of longitudinal, transverse, and vertical intrinsic muscles that determine its shape and have no bony attachment. In contrast, the extrinsic muscles have bony attachment and are capable of causing tongue protrusion and retrusion (Lowe, 1981). The genioglossus is the main tongue protrusor while the styloglossus and the hyoglossus are considered as the main retrusors. The thyrohyoid serves as tongue elevator. Contraction of muscles of the buccal floor like the geniohyoid
Activity of XII motoneurons during breathing, swallowing and coughing
Depending on the required movement, extrinsic tongue muscles contract in various combinations, either synergistically or antagonistically. During quiet breathing, the characteristic discharge patterns of XII motoneurons have been described in several studies (Hwang et al., 1983, Withington-Wray et al., 1988; see also references in Peever et al., 2002). The XII motor pattern during inspiration leads to enhanced activity of the genioglossus muscle to increase airway patency, and the
Peripheral and central processing of information
Orofacial and upper airway afferents convey sensory information from the jaws, teeth, lips, tongue and palate, as well as from the nasal, pharyngeal, and laryngeal cavities. This information exerts a powerful effect on XII motoneurons (Lowe, 1981, Miller, 2002). The lingual, trigeminal, glossopharyngeal and in particular the superior laryngeal nerves (SLN) have been shown to play an important role in mediating these information. Most of these peripheral inputs are processed by oligosynaptic
Activity of XII premotor neurons
Several methodological approaches can be used to assign a functional role to XII premotor neurons. A combination of immunohistochemical detection of Fos proteins (an indirect marker of neuronal activation) with retrograde-labeling method has proven to be helpful to gauge the level of activation of premotor neurons during a given behavior (Dinardo and Travers, 1997, Roda et al., 2004). Alternatively, electrophysiological techniques based on extracellular recordings of neurons with antidromic
Summary and conclusions
Schematic diagrams summarizing the findings and hypotheses are depicted in Fig. 8. Motoneurons do not participate to the generation of motor programs but contribute through their endogeneous properties to the patterning of motor outputs during breathing (Berger, 2000) and swallowing (discussed in Roda et al., 2002). They represent the “final common pathway” serving various oropharyngeal behaviors. A single CPG can have divergent synaptic inputs on distinct pools of XII motoneurons. Also, one
Acknowledgments
We are extremely grateful to Laurent Grelot, Fabrice Roda, and Yu Zheng for their respective contributions to part of the experiments and interpretation of data. This work was supported by grants from CNRS (UMR 6153) and INRA (USC 1147).
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