Pharyngeal electrical stimulation can modulate swallowing in cortical processing and behavior — Magnetoencephalographic evidence
Introduction
Swallowing is a complex motor task involving a widely distributed neuronal network (Jean, 2001, Michou and Hamdy, 2009). Dysphagia is a symptom of manifold neurologic disorders, which has huge impact on the quality of life and is associated with malnutrition, aspiration pneumonia, care dependency and significant mortality. Efficient treatment options for dysphagia rehabilitation are still limited. Spontaneous compensatory changes in swallowing-related cortical areas have, however, been reported for example after stroke (Hamdy et al., 1998a, Teismann et al., 2011a), in Parkinson's disease (Suntrup et al., 2013b) and motor neuron disorder (Dziewas et al., 2009). This natural ability of the brain to reorganize and functionally adapt to altered requirements is known to be driven by experience. Therefore, application of tactile, thermal (Hamdy et al., 2003, Kaatzke-McDonald et al., 1996, Rosenbek et al., 1996, Sciortino et al., 2003, Teismann et al., 2009b) or gustatory stimuli (Babaei et al., 2010, Logemann et al., 1995, Mistry et al., 2006, Pelletier and Lawless, 2003) to oropharyngeal receptors has been tested in a variety of clinical and neurophysiological studies on swallowing function in health and disease. Hamdy and co-workers developed and evaluated pharyngeal electrical stimulation (PES) as a neuromodulation device to enhance cortical reorganization for the restoration of swallowing function after brain injury. They showed that following electrical stimulation of the base of the tongue and posterior pharyngeal wall via a pair of catheter-mounted electrodes, motor cortex excitability and pharyngeal cortical representation area as mapped with repetitive transcranial magnetic stimulation (TMS) increased for at least 30 min (Hamdy et al., 1998b). Prior to clinical application the same group demonstrated the reversal of a virtual lesion induced by TMS in healthy pharyngeal motor cortex by subsequent PES. Finally, in a sham-controlled clinical pilot study on 50 stroke patients daily PES for three days led to reduced aspiration severity rates, improved feeding status and resulted in a shorter time to discharge from the hospital compared to the control group (Jayasekeran et al., 2010), implying that neuroplastic changes lead to clinically meaningful functional improvement.
Apart from these promising results, the underlying mechanism of action of PES, the neurophysiological correlate of behavioral gains and the temporal dynamics of the effects are not completely understood yet. In previous studies, PES-related excitability changes have predominantly been detected with evoked responses by using TMS. Here we contribute further knowledge on the cortical topography and frequency–specificity of activation pattern changes during the act of swallowing by taking advantage of a different functional neuroimaging modality. Magnetoencephalography (MEG) is capable of detecting and localizing power changes in oscillatory cortex activity (Taniguchi et al., 2000) evoked by a decrease or increase in synchrony of the underlying neuronal populations, otherwise known as event-related desynchronization (ERD) or synchronization (ERS) (Pfurtscheller and Lopes da Silva, 1999, Pfurtscheller, 2001). Voluntary movements are generally accompanied by a modulation in the alpha and beta frequency ranges, which is characterized by a power decrease (ERD) during the task, followed by a power increase (ERS) after movement execution. There is general agreement that ERD reflects cortical activation or arousal while ERS has been associated more with inhibitory activities (Pfurtscheller and Lopes da Silva, 1999). Being able to analyze the complete act of swallowing instead of a pharyngeal evoked potential the method allows for exploring stimulation-induced alterations in the cortical large-scale oscillatory swallowing network beyond the pharyngeal motor cortex.
Section snippets
Subjects
Fourteen healthy volunteers (8 male, 6 female, mean age 30.3 ± 4.7 years) participated in this study. Subjects were free of any neurologic, psychiatric or ear–nose–throat disorder, did not take any medication affecting the central nervous system and were right-handed (mean handedness score 90.0 in the Edinburgh Handedness Inventory (Oldfield, 1971)). The local ethics committee approved the protocol of the study. Informed consent was obtained from each subject after the nature of the study was
Pharyngeal electrical stimulation
Table 1 shows group mean values for perceptual threshold, maximum tolerated threshold and calculated optimal stimulation intensity. The latter is equal to the actually delivered stimulation intensity in the real intervention group. A paired samples t-test did not show any significant differences between both study groups (p > 0.05).
Water swallowing test
Group mean values of the 150 ml-water swallowing stress test pre and post intervention are shown in Table 2. Univariate 2 × 2 ANOVA revealed a significant main effect of
Discussion
This is the first study to investigate the effects of PES on the large-scale oscillatory swallowing network. According to our findings PES induced a transient right-dominant attenuation of cortical swallowing-related desynchronization (ERD) in oscillatory alpha and beta frequency ranges that were associated with subtle improvements of performance in a water swallowing stress test in healthy subjects.
Conclusion
In summary, we were able to show that a single session of pharyngeal electrical stimulation leads to beneficial temporary changes in cortical swallowing processing, which are associated with subtle effects on the swallowing function in healthy subjects. Our data contribute evidence that the swallowing network organization and behavior can effectively be modulated by PES and support further research on this promising tool for future dysphagia therapy.
Funding
This work was supported by the Deutsche Forschungsgemeinschaft (DFG) [grant number TE 840/1-1].
Disclosures
R. Dziewas is a member of the clinical advisory board of Phagenesis Ltd.
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