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

Key points Cortical control of swallowing exhibits functional asymmetry with brain lesions involving the strongest projection being implicated in the pathophysiology of dysphagia after unilateral stroke. Swallowing recovery is associated with neuroplastic adaptation in the unlesioned hemisphere, a process which can be facilitated by excitatory neurostimulation techniques including transcranial direct current stimulation (tDCS). Unilateral suppression of the strongest pharyngeal motor projection using 1Hz repetitive transcranial magnetic stimulation (rTMS) can disrupt swallowing neurophysiology and behaviour making it a useful model for trialling novel neurostimulation interventions in healthy subjects. In this healthy participant study we examined the effects of tDCS after unilateral pre-conditioning with 1Hz rTMS to determine its ability to restore swallowing neurophysiology and behaviour. We show that application of optimised parameters of tDCS (anodal stimulation, 1.5mA, 10min) over the unconditioned hemisphere reverses the brain and behavioural consequences of inhibitory pre-conditioning, supporting the use of tDCS in clinical trials. 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 1Hz 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 +/- 9years), optimal parameters of transcranial direct current stimulation (tDCS) (anodal, 1.5mA, 10min) were applied contralaterally after 1Hz 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 60min post intervention. Subjects were randomised to active or sham tDCS after 1Hz rTMS on separate days and data were compared using repeated measures ANOVA. Active tDCS increased PMEPs bilaterally (F-1,F-14=7.4, P=0.017) reversing the inhibitory effects of 1Hz rTMS in the pre-conditioned hemisphere (F-1,F-14=10.1, P=0.007). Active tDCS also enhanced swallowing behaviour, increasing the number of correctly timed challenge swallows compared to sham (F-1,F-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.