Opinion
How the brainstem controls orofacial behaviors comprised of rhythmic actions

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Highlights

  • Mammalian face and mouth contain sophisticated motor plants that produce diverse orofacial behaviors.

  • Brainstem contains key neural circuits that drive and coordinate different cranial motoneurons to produce various orofacial actions.

  • All orofacial actions are coordinated with breathing.

  • Three major neural computational mechanisms coordinating orofacial actions are discussed.

Mammals perform a multitude of well-coordinated orofacial behaviors such as breathing, sniffing, chewing, licking, swallowing, vocalizing, and in rodents, whisking. The coordination of these actions must occur without fault to prevent fatal blockages of the airway. Deciphering the neuronal circuitry that controls even a single action requires understanding the integration of sensory feedback and executive commands. A far greater challenge is to understand the coordination of multiple actions. Here, we focus on brainstem circuits that drive rhythmic orofacial actions. We discuss three neural computational mechanisms that may enable circuits for different actions to operate without interfering with each other. We conclude with proposed experimental programs for delineating the neural control principles that have evolved to coordinate orofacial behaviors.

Section snippets

Neural control of the mammalian face and mouth

It has long been postulated that there is a hierarchical control structure for motor acts in the nervous system 1, 2. Individual motor actions or primitives [3] can be executed singly or arranged in nested groups to form more complex behaviors. The nature of the interactions among the neural circuits that generate these actions and behaviors has been a topic of long-standing interest to neuroscientists. Interactions between different actions are unavoidable in the mammalian face and mouth,

Coordination of orofacial behaviors with breathing

Orofacial behaviors typically involve functions that affect the upper airway and therefore must be coordinated with breathing. The nature of this coordination constrains the organization of the neural circuits that control these behaviors. Rhythmic ingestive behaviors occur at frequencies that are faster than the 1–2 Hz frequency of basal respiration in rats. Chewing and mature suckling movements occur at ∼4 Hz [12], and rhythmic licking at 5–7 Hz [13]. Rhythmic activities in the trigeminal (V),

CPGs for breathing, chewing, licking, and swallowing in the brainstem

A CPG is operationally defined as a small network of neurons, or even a single neuron, whose activity can generate specific movements with correct timing and sequences in the absence of sensory feedback 26, 27. Various studies have suggested brainstem central origins for rhythmic whisking, chewing, and licking. Whisking, for example, can be generated in the absence of olfactory or trigeminal sensory input, and also after removal of the cortex 5, 18, 28, 29. Similarly, chewing 30, 31, licking 32

The ‘breathing primacy’ hypothesis for coordinating multiple orofacial actions

It is likely, as noted above, that there is a hierarchical control structure that ensures that orofacial behaviors do not interfere with each other. One possibility is that many of these actions are paced by the breathing CPG. Indeed, the whisking [20] and licking rhythms 14, 15 appear to be similarly reset by the breathing rhythm (Figure 2A–C); however, the case of chewing remains equivocal in this respect [25]. What is the neural circuit basis for such interactions between rhythmic actions?

Interactions among nonrespiratory CPGs and multifunctional neurons

Taking a page from the vertebrate and invertebrate locomotion CPGs, in which the left and right CPGs of the same segment, as well as the CPGs between different segments, have reciprocal connections and thus interact to coordinate different muscles during locomotion, it is conceivable that the different nonrespiratory orofacial CPGs also interact to coordinate oromotor activities. The simplest form of interaction is bilateral synchrony as seen in chewing, which is known to be dependent on

Top-down activation of orofacial actions

Although the pattern-generating circuits for chewing, licking, sniffing, and whisking are located in the brainstem, their activity is most likely gated by higher-order brain regions, including the cortex, cerebellum, basal ganglia, and superior colliculus. In support of this idea, stimulation of a region now called the cortical masticatory area produces rhythmic, coordinated jaw–tongue movements that occur at a fixed frequency of 4 Hz irrespective of the stimulation frequency [85]. These fictive

Role of sensation in orofacial actions

Although basic rhythmic motor patterns are controlled by CPGs, they can be modulated or even initiated by external stimuli. Sensory inputs can mediate reflexive motor outputs. More than 20 types of monosynaptic and oligosynaptic orofacial reflexes have been identified and studied [108]. These hard-wired circuits allow sensory inputs to coordinate the actions of multiple muscles to produce stereotyped behaviors, and thus constitute the lowest level of orofacial control.

Let us first consider

Concluding remarks and future directions

Orofacial actions and behaviors are mediated by several specific circuits in the brainstem. The common features of these circuits suggest some tantalizing organizational principles of the brainstem jungle of neural networks. Specifically, the brainstem reticular formation, and in particular the IRt, appears to contain CPGs and multifunctional neurons for various orofacial movements. Nonetheless, conclusive evidence for the exact locations and cell types comprising CPGs and CRGs and for most of

Acknowledgments

We thank Harvey J. Karten for the anatomical dataset used in the brainstem reconstruction (Figure 3), as well as Lauren McElvain, Martin Deschênes, and Winfred Denk for discussions. This work was supported by grants from the National Institute of Health, (NS077986 and DE019440 to F.W. and NS058668 to D.K.) and the US–Israeli Binational Foundation (grant 2011432 to DK).

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