August 2, 2011 Features

Stimulating Swallowing: Essential Central and Peripheral Nervous System Targets

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Oropharyngeal swallowing involves preparing or manipulating a bolus (food) in the oral cavity (mastication), propelling it into the pharynx (posterior oral propulsion), and squeezing it through the pharynx to the esophagus (pharyngeal swallow) without compromising the airway.

Despite its ease in healthy adults, swallowing is a complex sensorimotor phenomenon that includes numerous meticulously timed events involving both the peripheral and central nervous systems as well as many paired muscles. For instance, the pharyngeal swallow involves a cascade of neuromuscular and kinematic events that are critical for safe swallowing. Neuromuscular events (central nervous system control of muscles) include elevation of the velum (soft palate) to prevent nasal regurgitation, sequential contraction of the pharyngeal constrictors to engulf and squeeze the bolus downward, contraction of the submental muscle group and thyrohyoid muscle for hyoid bone and laryngeal anterior-superior movement to aid in closure of the laryngeal vestibule, intrinsic laryngeal closure (true and false vocal folds) for additional airway protection, and relaxation of the upper esophageal sphincter (UES) to allow the bolus to pass into the esophagus.

Movement kinematics (movement of structures in terms of timing, displacement, and velocity) include epiglottal inversion to aid in airway protection and further opening of the relaxed UES due to laryngeal elevation. The entire pharyngeal swallow is complete in less than one second, but varies depending on the bolus swallowed and the person's age (Bisch, 1994; Tracey et al., 1989).

Swallowing was once considered a simple reflex involving only the brainstem. Recent evidence, however, shows the importance of higher brain centers in the cortex during swallowing (Humbert et al., 2009; Mistry et al., 2007). This finding has advantageous implications in the treatment of dysphagia because clinicians and patients may more readily access, train, and modify components of oropharyngeal swallowing that are volitionally initiated or modified. Despite this knowledge, many swallowing treatments are more compensatory (e.g., bolus modification, a strategy aimed not at improving the system but rather working around it) and less rehabilitative.

We also do not yet fully understand changes to the underlying system of deglutition that occur due to rehabilitative swallowing strategies. Thus, important scientific and clinical questions remain unanswered.

Motor Control: Sensory Plus Motor 

Motor control is an important part of the field of neuroscience. It is the process of creating movement, including the interaction between the central and peripheral nervous systems (CNS and PNS) for stimulating coordinated and skilled actions. Although "motor" is often emphasized, increasing attention is being paid to the sensory component of producing movements (sensory integration).

The principles of motor control are derived primarily from studies of the limbs and eye movement, and several of these concepts may be applied to swallowing. One important concept is that ease of movement is possible because of the steady stream of sensory information being processed while planning, executing, and evaluating an action. This concept has particular significance for oropharyngeal swallowing because the bolus being swallowed provides constant sensory input, albeit subconscious, for planning (bringing food to mouth), execution (moving food through the oropharyngeal cavity), and evaluation (determining how soon to move to the next mouthful based on the success of the previous swallow). 

Sensory input is the information propagated to the central nervous system following stimulation of a group of sensory receptors. Sensory receptors are modality-specific, so sensory nerve endings are receptive to a specific type of sensory information. The oral, pharyngeal, and laryngeal structures are lined with mucosae (mucous membrane epithelial lining). Sensory receptors within the mucosae and taste buds on the tongue offer a vast array of sensory modalities for a bolus to stimulate, including general sensation (touch/pressure), thermal sensation (temperature), chemical sensitivity (taste), nociception (damaging stimuli, pain), vibrotactile sensation, oral stereognosis (ability to recognize and discriminate forms in mouth), proprioception (awareness of position), and two-point discrimination (ability to detect two distinct points when two nearby objects are touching the skin). Furthermore, periodontium receptors (tissues around the tooth; gum) provide information about the size and hardness of objects between the teeth.

The oral, laryngeal, and pharyngeal cavities together are among the most diverse and rich sensory systems of the body. (See Miller, 1994, chapter 2, for a thorough review of oral, pharyngeal, and laryngeal sensory systems for swallowing.)

Effortless movement occurs when sensory information is processed continually before, during, and after a movement. Given that the goal of swallowing is to move the bolus safely from mouth to stomach, it is no surprise that the oropharynx has a heightened sensory system. The bolus provides sensory input to the CNS while moving through oral and pharyngeal regions and influences many aspects of the swallow. Swallowing research shows that oropharyngeal swallowing is responsive to the properties of the bolus being ingested. A clear example is described in studies of bolus volume, in which swallowing a large amount of liquid (20 ml) involves longer durations and range of motion of the hyoid bone and larynx compared to a very small bolus (1 ml), thus protecting the airway longer (Kahrilas & Logemann, 1993).

Larger bolus volumes also are associated with longer durations of UES opening (Jacob et al., 1989; Hoffman et al., 2010). This bolus-dependent modification likely exists to ensure swallowing safety. If, for instance, a 20-ml liquid bolus is swallowed, yet the timing of hyo-laryngeal excursion and UES opening responded as with a 1-ml bolus, the risk of aspiration could increase. These kinds of errors may be avoided well before the bolus has entered the mouth in healthy adults who determine the size of each bite (e.g., spoon size, straw sip).

Taste offers another example of sensory input on swallowing movement. Healthy adults and those with dysphagia both have shorter swallow onset response times with a sour bolus compared to that of a bolus without taste, eliminating aspiration in many swallows (Logemann et al., 1995). However, a palatable sour plus sucrose mix did not yield the same effects (Pelletier & Lawless, 2003; see Steele & Miller, 2010, pp. 323–333, for a review of many stimulus types). Although the reasons for the different effects are not known, Pelletier & Lawless (2003, p. 7) suggest that the properties of the mixtures themselves might provide some explanation. More research is needed to answer these questions.

Motor Control: Reflex to Volition 

Another significant issue in motor control is categorizing movements as reflexive or volitional. Prochazka and colleagues (2000, pp. 417–432) debate these issues in a review article, "What do reflex and voluntary mean? Modern views on an ancient debate." There is some agreement among the authors that reflexive movements require initiation by a trigger, are difficult to suppress once in motion, and are controlled by lower brain areas (brainstem or spinal cord). Conversely, voluntary movements do not require a trigger, can be interrupted at any time, and are controlled primarily by higher brain areas (cortex).

The work of Prochazka et al. suggests there is likely a continuum on which many sensorimotor tasks can be placed, rather than in two distinct categories of reflex and volition. Oropharyngeal swallowing is unique because its components fall on more than one site on this continuum. For instance, chewing, the oral component, does not need a stimulus to be initiated (that is, one can simulate chewing without a bolus) and it can be interrupted at any time. Initiation of the pharyngeal phase of swallowing, however, does require a sensory trigger (Ertekin et al., 2000; Mansson & Sandberg, 1975) and is likely difficult to suppress or interrupt once triggered.

Although the literature does not offer direct evidence of intentional pharyngeal swallowing suppression or interruption in healthy adults, there is clear evidence of pharyngeal phase modification, such as the Mendelsohn maneuver, in which healthy adults and those with dysphagia can intentionally prolong hyo-laryngeal movement and UES opening (Kahrilas et al., 1991). This ability to modify the pharyngeal phase, once initiated, suggests that the pharyngeal swallow can be modified by input from higher (cortical) centers in the brain. Given this information, oropharyngeal swallowing—although challenging to define—presents a unique model for understanding how a variety of stimuli can affect oral manipulation of a bolus as well as the cascade of events in the pharyngeal swallow.

Stimulating Swallowing 

The many forms of dysphagia vary depending on etiology (e.g., neurological damage, surgery). In addition, two different patients may have experienced a stroke in the same neuroanatomical location, but only one might experience dysphagia. Although the reasons for such discrepancies are not known, most clinicians and scientists agree that the goal in treating any patient with dysphagia is to achieve a functional swallowing status to increase safety, nutrition, and hydration.

Some clinicians may perceive dysphagic swallows as having a high threshold for initiation and completion—that is, a 5-ml teaspoon of thin liquid barium can stimulate a swallow in a healthy person, but a patient with dysphagia may not respond safely or at all with this same stimulus. A goal of dysphagia treatment is to determine what technique can be used to lower the swallowing threshold. Changing bolus properties (temperature, taste, etc.) may help patients. However, probing an injured swallowing system may require a more thoughtful approach, possibly by hypothesizing the level of anatomy or physiology affected by the injury.

Neuroplasticity in Dysphagia 

Neuroplasticity—experience-based structural or functional changes in the CNS—is proving to be a new paradigm for the development of rehabilitative strategies. Both healthy and unhealthy individuals may experience neuroplasticity, although for dysphagia, neuroplasticity in patients who also show improvements in swallowing has great potential (for reviews, see Martin, 2009, and Robbins et al., 2008).

Some critical concepts about neuroplasticity can be applied readily by clinicians treating dysphagia, especially neurogenic dysphagia, because dysphagia treatments can be an important basis for facilitating neuroplasticity in patients. However, many of these treatments (sensory stimulation, strength training, visual bio-feedback) are not applied equally in the clinical setting, perhaps because they are difficult to use. Many dysphagia treatments meant to lower the swallowing threshold (e.g., trigger a faster pharyngeal swallow response or elicit adequate range of motion of particular structures) involve external forms of stimulation, or stimulus-based techniques that can be easily controlled by the clinician or, in research, by the scientist (e.g., sour bolus, cold bolus).

These stimulus-based treatments also may be called "exogenous" or "bottom-up," as peripheral stimulation ascends to the level of the CNS. They have a place in dysphagia treatment and are encouraging because they often show immediate improvement in a system that relies heavily on sensory stimulation. This improvement has been shown with traditional stimuli such as taste (Logemann et al., 1995) as well as with more recently developed swallowing treatment strategies such as sensory-level surface electrical stimulation (Ludlow et al., 2006). However, we do not completely understand their long-term effects. For instance, habituation (reduced sensory perception with repeated exposures) and its effect on the swallowing motor response needs to be fully investigated.

These stimulus-based techniques also are useful for patients with dysphagia and dementia, minimizing the need for active patient participation for the treatment to be effective. Treatments of these forms may be described as non-behavioral: the clinician is actively applying, while the patient is passively receiving. These forms of treatment may facilitate improvement during a critical period of recovery from a stroke, for instance, but the Martin (2009) review of neuroplasticity in swallowing and dysphagia presents a convincing argument for combining both non-behavioral and behavioral treatments to alleviate swallowing impairment.

Behavioral treatments, conversely, require patients to be active participants in the motor task(s). These treatments may be described as "endogenous,"  "intention-based," or "top-down," with the individual initiating a movement (effortful swallow), typically with some instruction from the clinician. These movements can be familiar (press tongue to hard palate) or may require new skill acquisition (Mendelsohn maneuver).

It is important to note that behavioral treatments are not void of sensory input or stimulation. For instance, with visual bio-feedback, patients are expected to use a visual representation of performance, such as electromyography (EMG) of muscle activity, to modify a behavior. In the case of an effortful swallow, more EMG activity is interpreted as more effort. There also is the "feel" of movement, or knowing where the structures are relative to one another or in space (proprioception), which can be fine-tuned. Proprioception is well described in the limbs, but is understudied in structures of the head and neck, especially those related to swallowing.

The potential benefit of combining non-behavioral and behavioral approaches is that improvement comes more quickly and lasts longer. If a large stroke is responsible for delayed onset of the pharyngeal swallow in addition to reduced UES opening and hyo-laryngeal excursion, it might be appropriate for the patient to swallow a small sour bolus (at a safe consistency) during an effortful swallow. This might address the need for immediate sensory input to the brainstem to initiate the swallow earlier and the goal to strengthen over time because of stronger muscle contractions with the effortful swallow. Another example is increasing bolus size during the Mendelsohn to increase movement range and duration in healthy adults (Kahrilas et al., 1991).

Some studies have combined surface electrical stimulation with active swallowing and/or standard swallowing treatment in post-stroke patients (for a review see Ludlow, 2010), under the hypothesis that these approaches might improve muscle strength as well as both top-down and bottom-up connections between and within the PNS and CNS. Obviously, far more research on these approaches is needed to answer more specific questions about which populations, treatment combinations, and dosages are most beneficial for stimulating swallowing.

Swallowing motor control is very complex but critical to understanding how to treat dysphagia. Sensory and motor components for movement need to be considered in tandem, especially because oropharyngeal swallowing relies heavily on sensory information about the properties of the bolus and where the structures (tongue, larynx) are relative to the moving bolus.

Although experts no longer categorize swallowing as a simple reflex, some events within the oropharyngeal swallow are more stereotypical, whereas others are far more volitional. Ideally, each treatment could be tailored to target the specific cause of dysphagia. The complexity of oropharyngeal swallowing, however, suggests that greater overall success might be attained with techniques that access the neuromuscular system in more than one place and in more than one way, but always maintain the safety of the patient as the top priority. These unknowns will continue to stimulate more important research and clinical questions, leading to clear and valid findings about how normal swallowing is controlled and, subsequently, how to improve swallowing in patients with dysphagia. 

Ianessa A. Humbert, PhD, CCC-SLP, is an assistant professor in the Department of Physical Medicine and Rehabilitation at Johns Hopkins University. Her research interests include normal swallowing motor control across the age span and in populations with neurological disorders. She is a member of the Research Committee of Special Interest Group 13, Swallowing and Swallowing Disorders. Contact her at ihumber1@jhmi.edu.

cite as: Humbert, I. A. (2011, August 02). Stimulating Swallowing: Essential Central and Peripheral Nervous System Targets. The ASHA Leader.

References

Bisch, E. M., Logemann, J. A., Rademaker, A. W., Kahrilas, P. J., & Lazarus, C. L. (1994). Pharyngeal effects of bolus volume, viscosity, and temperature in patients with dysphagia resulting from neurologic impairment and in normal subjects. Journal of Speech and Hearing Research, 37, 1041–1059.

Ertekin, C., Kiylioglu, N., Tarlaci, S., Keskin, A., & Aydogdu, I. (2000). Effect of mucosal anaesthesia on oropharyngeal swallowing. Neurogastroenterology & Motility, 12, 567–572.

Hoffman, M. R., Ciucci, M. R., Mielens, J. D., Jiang, J. J., & McCulloch, T.M. (2010). Pharyngeal swallow adaptations to bolus volume measured with high-resolution manometry. Laryngoscope, 120, 2367–2373. 

Humbert, I. A., Fitzgerald, M. E., McLaren, D. G., Johnson, S., Porcaro, E., Kosmatka, K., Hind, J., & Robbins, J. (2009). Neurophysiology of swallowing: Effects of age and bolus type.NeuroImage,44,982–991,

Jacob, P., Kahrilas, P. J., Logemann, J. A., Shah, V., & Ha, T. (1989). Upper esophageal sphincter opening and modulation during swallowing. Gastroenterology, 97, 1469–1478.

Kahrilas, P. J., Logemann, J. A., Krugler, C., & Flanagan, E. (1991). Volitional augmentation of upper esophageal sphincter opening during swallowing. American Journal of Physiology, 260, G450–456.

Kahrilas, P. J., & Logemann, J. A. (1993). Volume accommodation during swallowing. Dysphagia, 8, 259–265.

Logemann, J. A., Pauloski, B. R., Colangelo, L., Lazarus, C., Fujiu, M., & Kahrilas, P.J . (1995). Effects of a sour bolus on oropharyngeal swallowing measures in patients with neurogenic dysphagia. Journal of Speech and Hearing Research, 38, 556–563.

Ludlow, C. L., Humbert, I., Saxon, K., Poletto, C., Sonies, B., & Crujido, L. (2006). Effects of surface electrical stimulation both at rest and during swallowing in chronic pharyngeal dysphagia. Dysphagia, 22, 1–10.

Ludlow, C. L. (2010). Electrical neuromuscular stimulation in dysphagia: Current status. Current Opinion in Otolaryngology & Head and Neck Surgery, 18, 159–164. 

Mansson, I., & Sandberg, N. (1975). Salivary stimulus and swallowing reflex in man.  Acta Oto-laryngologica, 79, 445–450.

Martin, R. E. (2009). Neuroplasticity and swallowing. Dysphagia, 24, 218–229.

Miller, A. J. (1994). Neuroscientific principles of swallowing. Singular Publishing, London.

Mistry, S., Verin, E., Singh, S., Jefferson, S., Rothwell, J. C., Thompson, D. G., & Hamdy, S. (2007). Unilateral suppression of pharyngeal motor cortex to repetitive transcranial magnetic stimulation reveals functional asymmetry in the hemispheric projections to human swallowing. The Journal of Physiology, 585, 525–538.

Pelletier, C. A., & Lawless, H. T. (2003). Effect of citric acid and citric acid-sucrose mixtures on swallowing in neurogenic oropharyngeal dysphagia. Dysphagia, 18, 231–241.

Prochazka, A., Clarac, F., Loeb, G. E., Rothwell, J. C., & Wolpaw, J. R. (2000). What do reflex and voluntary mean? Modern views on an ancient debate. Experimental Brain Research, 130, 417–432.

Robbins, J., Butler, S. G., Daniels, S. K., Diez Gross, R., Langmore, S., Lazarus, C. L., Martin-Harris, B., McCabe, D., Musson, N., & Rosenbek, J. (2008). Swallowing and dysphagia rehabilitation: Translating principles of neural plasticity into clinically oriented evidence. Journal of Speech, Language, and Hearing Research, 51, S276–300.

Steele, C. M., & Miller, A. J. (2010). Sensory input pathways and mechanisms in swallowing: A review. Dysphagia, 25, 323–333.



  

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