Swallowing is a complex sequence of movements which we perform voluntarily during eating and drinking but also spontaneously, without awareness between meals, during sleep or in stressful situations (Cuevas, Cook, Richter, McCutcheon, & Taub, 1995; Ertekin, 2011; Fonagy & Calloway, 1986).
The swallowing process consists of three different phases, oral, pharyngeal, and esophageal. It begins with a mainly voluntarily controlled preparatory phase, in which the bolus is prepared for swallowing and tongue movements entrap it between tongue and palate (oral phase). The pharyngeal phase is considered the transfer phase and starts with tip and sides of the tongue pressing against the palate, while the posterior part of it relaxes to allow the bolus to pass into the oropharynx. Contractions of the tongue and pharyngeal wall move the bolus further into the pharynx. To seal the airway during this process, the tongue closes the oral cavity off, the soft palate and proximal wall close the nasopharynx, and vocal cords, arytenoids and epiglottis close the laryngeal opening and vestibule. Next, the larynx positions
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itself outside the path of the bolus and the pharynx starts contracting to move it into the esophagus. The final phase is the esophageal phase, or transport phase. The esophagus relaxes to allow the bolus to pass into the stomach. Fluids are transported mainly through gravity, while peristaltic contractions move solids downwards. Unlike the oral phase, the pharyngeal and esophageal phase are reflexive and involuntary (Ertekin, 2011; Goyal & Mashimo, 2006).
1.2.1 Neuronal Activation of Swallowing
The process of swallowing relies on a large network inside the brain, the exact activation loci depend on the size and properties (consistency, flavor, water or saliva) of the bolus as well as on the type of initiation (voluntary vs. spontaneous) of swallowing (Ertekin, 2011; Humbert & Robbins, 2007; Sorös, Inamoto, & Martin, 2009). The brainstem has been found to play a crucial role in the initiation of the pharyngeal and esophageal phases as well as in swallowing control (Bautista, Sun, & Pilowsky, 2014; Ertekin, 2011; Jean, 2001) and is activated during both voluntary and reflexive swallowing (Ertekin, 2011). Multiple studies found a strong activation of the IFG, which, besides its role in language production, has been linked to the control of non-linguistic mouth and face movements (Kober, Grössinger, et al., 2019; Kober & Wood, 2018; Martin, Goodyear, Gati, & Menon, 2001). The SMA, which plays a role in planning of complex or sequential movements (Satow et al., 2004), has frequently been found to be activated during swallowing (Martin et al., 2001; Sorös et al., 2009). The insula is involved in integrating sensory and gustatory information received from different brain regions, which are active during swallowing (Ertekin, 2011; Hamdy, Mikulis, et al., 1999; Smits, Peeters, Hecke, & Sunaert, 2007; Sorös et al., 2009). The lateral precentral gyrus in M1 is crucial to initiate voluntary swallowing and movements of tongue, jaws and lips, but has also been found to be activated during spontaneous swallowing, whereas the postcentral gyrus in the somatosensory cortex processes sensory inputs in mouth and pharynx (Hamdy, Mikulis, et al., 1999; Hamdy, Rothwell, et al., 1999). The superior temporal gyrus addresses perception of taste sensations and swallowing noises (Martin, 2001).
Compared to other motor actions such as hand movements (Wriessnegger, Kurzmann,
& Neuper, 2008), NIRS signal changes and blood oxygenation dependent (BOLD) signal during active swallowing have been found to be slower and to peak later (Hamdy, Mikulis, et al., 1999; Kober, Bauernfeind, et al., 2015; Kober & Wood, 2014, 2018). During swallowing, peak activation of NIRS signal changes was reported at around 15 seconds after task onset (Kober, Bauernfeind, et al., 2015; Kober & Wood, 2014, 2018), whereas during hand
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movements, the maximum activation of the hemodynamic response was at 5 seconds after task onset (Wriessnegger et al., 2008). As the whole swallowing process takes between 8 and 12 seconds and incorporates secondary motor activity in the esophagus, this prolonged time course could result from sensory and motoric feedback loops leading from cortical to peripheric areas (Hamdy, Mikulis, et al., 1999; Kober & Wood, 2014; Martin et al., 2001).
Regarding different bolus types, several studies showed stronger activation in swallowing related brain areas for saliva than for water swallowing (Humbert & Robbins, 2007; Kober & Wood, 2018). Further, a lateralization effect indicating higher activation during water swallowing in the right inferior parietal lobe, the right postcentral gyrus and the right insula has been found, whereas activation patterns for saliva swallowing were more bilaterally distributed (Sorös et al., 2009). In a NIRS study, signal changes during water swallowing were most pronounced over the right IFG and during saliva swallowing over the left IFG, indicating a similar lateralization effect (Kober & Wood, 2018). Another finding of this study was that compared to water swallowing, oxy hemoglobin (HbO) levels showed a prolonged time course and deoxy hemoglobin (HbR) decreased steady during saliva
swallowing, reflecting a higher task demands of saliva swallowing (Kober & Wood, 2018).
1.2.2 Dysphagia
Dysphagia is a pathological difficulty in swallowing, which can affect all phases of the movement sequence. Dysphagia can result from brain injuries or neurological diseases like Alzheimer’s dementia, Multiple Sclerosis, amyotrophy lateral sclerosis (ALS), strokes or traumatic brain injuries, but it is also present in the healthy aging population. In the normal elderly population, prevalence for suffering from dysphagia is expected between 15 and 23%
while for clinical populations the prevalence can be up to 85.9% (Barczi, Sullivan, &
Robbins, 2000; Eslick & Talley, 2008; Espinosa-Val et al., 2020; Wilkins, Gillies, Thomas, &
Wagner, 2007). Difficulties in the swallowing process are not only troublesome in daily life but can also lead to severe lung damage through choking and inhalation. Patients with
dysphagia are more likely to develop anxiety disorders or depression and often report impacts on their social life. Hence, dysphagia highly affects health and overall quality of life (Eslick &
Talley, 2008).
Conventional therapy methods for dysphagia focus mainly on compensatory strategies or on training of in swallowing involved muscular structures (Langmore & Pisegna, 2015;
Szynkiewicz, Nobriga, & Donoghue, 2018; Vose, Nonnenmacher, Singer, &
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Fernández, 2014). Compensatory strategies are mostly used to prevent health consequences of dysphagia like dehydration, malnutrition or pneumonia and do not lead to any physiological improvements. Examples for such strategies are different postures of head and tongue during swallowing, as well as modification of the texture of fluids and food (Vose et al., 2014).
Contrary, exercises for swallowing related muscle structures aim to improve swallowing function directly and therefore enhance neuroplasticity (Langmore & Pisegna, 2015; Vose et al., 2014). Along those exercises, some can also serve as compensatory strategy (Vose et al., 2014).
Previous research showed that it is possible to enhance neuroplasticity in swallowing related brain areas (Robbins et al., 2008), thus the usage of MI could be a promising tool to support conventional therapy methods in dysphagia patients (Szynkiewicz et al., 2018).
1.2.3 MI of Swallowing
Despite the rapidly increasing number of studies in motor imagery, there is still a shortage of investigations about the imagination of swallowing (for a review, see Szynkiewicz et al., 2018; Yang et al., 2016). For the use in neurorehabilitation, it is important to ensure that MI of swallowing activates similar brain regions as swallowing itself in order to enhance neuroplasticity and thus improve the recovery of patients with dysphagia (Faralli et al., 2013;
Ruffino et al., 2017; Szynkiewicz et al., 2018). The absence of visual cues for swallowing outlines a huge difference to MI of limb movements and forces users to rely on kinesthetic imagery strategies. In addition, various muscle groups have to be imagined. Yet, Yang et al.
(2014) showed in an EEG study that the imagination of swallowing and tongue movements are distinct constructs.
Neuroimaging studies revealed similar brain activation patterns between MIand ME of swallowing, including the IFG, basal ganglia, insula, SMA, bilateral pre- and postcentral gyrus, and the cerebellum (Kober, Bauernfeind, et al., 2015; Kober, Grössinger, et al., 2019;
Kober & Wood, 2014). Previous NIRS studies located strongest signal changes during ME and MI of swallowing above the IFG bilaterally in healthy young adults, healthy elderly and dysphagia patients with brain stem lesions (Kober, Bauernfeind, et al., 2015; Kober & Wood, 2014). For dysphagia patients with cerebral lesions, a more unilateral activation pattern was revealed. (Kober, Bauernfeind, et al., 2015). A recent fMRI study extended those findings for additional activation in deeper brain structures (Kober, Grössinger, et al., 2019). Further, and similar as during ME of swallowing (see section 1.2.1), a prolonged time course of the NIRS
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signal compared to ME and MI of other movements (Wriessnegger et al., 2008) has been found for MI of swallowing (Kober, Bauernfeind, et al., 2015; Kober & Wood, 2014).
Increases in HbR during MI of swallowing were largely comparable to ME, but the tasks differed fundamentally regarding changes in HbO. While a significant increase was observed during ME, HbO levels even decreased during MI (Kober & Wood, 2014). A decrease in HbO has been associated with improved motor inhibition (Gentili, Shewokis, Ayaz, & Contreras-Vidal, 2013), therefore Kober and Wood (2014) interpreted their finding as a sign of movement inhibition. As mentioned before (see section 1.1), MI contains motor plans of the movement, but on some point they have to be stopped to prevent actual
movement (Guillot et al., 2012). However, no such decrease in HbO levels has been observed during MI of other movements (Wriessnegger et al., 2008). As swallowing is partly a
reflexive movement (Ertekin, 2011), more effort could be needed to inhibit active swallowing during MI, leading to a decrease in HbO (Kober & Wood, 2014). Small, but not significant increases in EMG activity during MI support this assumption of increased effort for inhibiting swallowing (Kober & Wood, 2014). In healthy elderly and dysphagia patients with brain stem lesions, increases in HbR were observed during MI of swallowing, but along with a
simultaneous increase in HbO, which could indicate insufficient movement inhibition in this population (Kober, Bauernfeind, et al., 2015).
Neurofeedback studies showed that healthy young adults were able to upregulate HbR but not HbO over the IFG during MI of swallowing (Kober, Gressenberger, et al., 2015;
Kober et al., 2018). Moreover it has been demonstrated that it is possible to voluntary downregulate HbO and upregulate HbR over the IFG during MI of swallowing, but not vice versa (Kober et al., 2018). In contrast, healthy elderly were only able to upregulate HbR (Kober, Spörk, Bauernfeind, & Wood, 2019). MI of swallowing usually leads to a decrease in HbO and an increase in HbR in healthy young adults (Kober & Wood, 2014) and to an
increase in both, HbO and HbR, in healthy elderly (Kober, Bauernfeind, et al., 2015). Hence, the trainability of these parameters during neurofeedback suggests that only this natural course of the NIRS signal can be modulated (Kober et al., 2018).