Transcranial direct current stimulation reverses neurophysiological and behavioural effects of focal inhibition of human pharyngeal motor cortex on swallowing

Dipesh H Vasant, Satish Mistry, Emilia Michou, Samantha Jefferson, John C Rothwell, Shaheen Hamdy, Dipesh H Vasant, Satish Mistry, Emilia Michou, Samantha Jefferson, John C Rothwell, Shaheen Hamdy

Abstract

The human cortical swallowing system exhibits bilateral but functionally asymmetric representation in health and disease as evidenced by both focal cortical inhibition (pre-conditioning with 1 Hz repetitive transcranial magnetic stimulation; rTMS) and unilateral stroke, where disruption of the stronger (dominant) pharyngeal projection alters swallowing neurophysiology and behaviour. Moreover, excitatory neurostimulation protocols capable of reversing the disruptive effects of focal cortical inhibition have demonstrated therapeutic promise in post-stroke dysphagia when applied contralaterally. In healthy participants (n = 15, 8 males, mean age (±SEM) 35 ± 9 years), optimal parameters of transcranial direct current stimulation (tDCS) (anodal, 1.5 mA, 10 min) were applied contralaterally after 1 Hz rTMS pre-conditioning to the strongest pharyngeal projection. Swallowing neurophysiology was assessed in both hemispheres by intraluminal recordings of pharyngeal motor-evoked responses (PMEPs) to single-pulse TMS as a measure of cortical excitability. Swallowing behaviour was examined using a pressure-based reaction time protocol. Measurements were made before and for up to 60 min post intervention. Subjects were randomised to active or sham tDCS after 1 Hz rTMS on separate days and data were compared using repeated measures ANOVA. Active tDCS increased PMEPs bilaterally (F1,14 = 7.4, P = 0.017) reversing the inhibitory effects of 1 Hz rTMS in the pre-conditioned hemisphere (F1,14 = 10.1, P = 0.007). Active tDCS also enhanced swallowing behaviour, increasing the number of correctly timed challenge swallows compared to sham (F1,14 = 6.3, P = 0.025). Thus, tDCS to the contralateral pharyngeal motor cortex reverses the neurophysiological and behavioural effects of focal cortical inhibition on swallowing in healthy individuals and has therapeutic potential for dysphagia rehabilitation.

Figures

Figure 1
Figure 1
Abbreviations: PMEPs, pharyngeal motor-evoked potentials; TMEPs, thenar motor-evoked potentials.
Figure 2
Figure 2
A, active tDCS post pre-conditioning with 1 Hz rTMS increased PMEP amplitudes bilaterally. B, sham tDCS post pre-conditioning with 1 Hz rTMS suppressed PMEPs on the conditioned hemisphere. TMEPs were not affected by either tDCS intervention. For visual purposes, responses from the intermediate time points 15 and 45 min post tDCS have been removed. Trace clusters for each recording site are composed of 10 overdrawn responses.
Figure 3
Figure 3
The dashed lines in this figure show the inhibitory changes induced by 1 Hz rTMS after sham tDCS. Active tDCS increases pharyngeal cortical excitability bilaterally (*P = 0.017).
Figure 4
Figure 4
There were no significant effects of interventions on conditioned hemisphere PMEPs latencies (A), unconditioned hemisphere PMEPs latencies (B) or TMEPs latencies (C).
Figure 5
Figure 5
A, mean normal and fast swallowing reaction times (both visits). B, mean number of correctly timed challenge swallows (both visits).
Figure 6
Figure 6
Graphs showing percentage change from baseline in normal swallow reaction times (A), fast swallow reaction times (B) and correctly timed challenge swallows (C) over 60 min post intervention. Active anodal tDCS significantly improved swallowing behaviour (*P = 0.03; **P = 0.025).

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