Elsevier

NeuroImage

Volume 104, 1 January 2015, Pages 117-124
NeuroImage

Pharyngeal electrical stimulation can modulate swallowing in cortical processing and behavior — Magnetoencephalographic evidence

https://doi.org/10.1016/j.neuroimage.2014.10.016Get rights and content

Highlights

  • Modulation of cortical swallowing-associated activation by PES was assessed with MEG.

  • PES induced a right-dominant attenuation of ERD in alpha and beta frequency ranges.

  • Attenuation reflects stimulation-induced increased swallowing processing efficiency.

  • Neuroplastic changes are associated with behavioral gains.

Abstract

Background

The act of swallowing is a complex neuromuscular function that is processed in a distributed network involving cortical, subcortical and brainstem structures. Difficulty in swallowing arises from a variety of neurologic diseases for which therapeutic options are currently limited. Pharyngeal electrical stimulation (PES) is a novel intervention designed to promote plastic changes in the pharyngeal motor cortex to aid dysphagia rehabilitation. In the present study we evaluate the effect of PES on cortical swallowing network activity and associated changes in swallowing performance.

Methods

In a randomized, crossover study design 10 min of real (0.2-ms pulses, 5 Hz, 280 V, stimulation intensity at 75% of maximum tolerated threshold) or sham PES were delivered to 14 healthy volunteers in two separate sessions. Stimulation was delivered via a pair of bipolar ring electrodes mounted on an intraluminal catheter positioned in the pharynx. Before and after each intervention swallowing capacity (ml/s) was tested using a 150 ml-water swallowing stress test. Event-related desynchronization (ERD) of cortical oscillatory activity during volitional swallowing was recorded applying whole-head magnetoencephalography before, immediately after and 45 min past the intervention.

Results

A prominent reduction of ERD in sensorimotor brain areas occurred in the alpha and beta frequency ranges immediately after real PES but not after sham stimulation (p < 0.05) and had faded after 45 min. Volume per swallow and swallowing capacity significantly increased following real stimulation only.

Conclusion

Attenuation of ERD following PES reflects stimulation-induced increased swallowing processing efficiency, which is associated with subtle changes in swallowing function in healthy subjects. Our data contribute evidence that swallowing network organization and behavior can effectively be modulated by PES.

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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