Surface Electrical Stimulation Perturbation Context Determines the Presence of Error Reduction in Swallowing Hyolaryngeal Kinematics

Abstract

Purpose: Error-based learning (EBL) involves gradually reducing movement errors caused by a perturbation. When the perturbation has been unexpectedly removed, exaggerated movements occur in the opposite direction of a perturbation effect, known as aftereffects. Our goal was to determine whether the perturbation type impacts error reduction or aftereffects in swallowing hyolaryngeal kinematics. Method: We perturbed peak hyolaryngeal elevation during swallowing in 16 healthy adults with surface electrical stimulation (SES) in 2 different ways during videofluoroscopy: intermittent SES (I-SES) was applied only during swallowing, and continuous SES (C-SES) was applied during swallowing and during interswallow intervals. In C-SES and I-SES, the onset and offset of the perturbation were unmasked. Results: Only the C-SES perturbation caused error reduction (gradually increasing peak elevation). Aftereffects were absent in both perturbations, unlike findings from our previous study with masked perturbation. Furthermore, the duration of laryngeal vestibule closure (dLVC) increased during the I-SES perturbation but was unchanged during C-SES perturbation. Conclusion: EBL of swallowing airway protection events was strongly influenced by the context of the perturbation. These findings also elucidate how the relationship among critical swallowing airway protection events (hyoid peak, laryngeal peak, and dLVC) can be modified during EBL.

The perturbation paradigm modulates error-based learning in a highly automated task: outcomes in swallowing kinematics

“…Thus far, varied forms of motor perturbation have been tested in a swallowing error-based paradigm in only one study to our knowledge (10). In this study, error-based learning of swallowing hyo-laryngeal movements were only evident in healthy adults who were continuously perturbed (during both swallowing and interswallowing intervals) but not in participants who were intermittently perturbed (during swallowing only, not interswallow intervals).…”

“…As expected, there was no other change in any other timing measurement. Motor adaptation of a swallowing timing measure (duration of laryngeal vestibule closure) has only previously been shown by Humbert et al (10), when the perturbation (also neck surface electrical stimulation) was administered intermittently (only during the perturbation, not during the 10-s interswallow intervals) (10). The current study included a continuous perturbation paradigm (perturbation during both swallowing and the interswallow interval).…”

“…ELECTRICAL STIMULATION. Surface electrical stimulation (Ministim; Life-Tech, Stafford, TX) placement parameters were identical to Humbert et al (10,11) with application on the skin of the anterior neck on either side of the thyroid laminae, overlying infrahyoid muscles bilaterally (omohyoid, sternohyoid, sternothyroid, and thyrohyoid). The Ministim has an output current range of 0 to 50 mA, stimulus pulse of 220 m, square wave monophasic, and participants were stimulated at 100 Hz.…”

“…Thus we compared masked and unmasked onset and offset of both gradual and abrupt perturbations. We hypothesized that, consistent with Humbert et al (10), masking the presence of the perturbation would lead to aftereffects because the stimulation is unexpectedly removed, leading the participant to execute a movement plan that accommodates the perturbation. On the other hand, we predicted that unmasking the presence of the perturbation would not lead to aftereffects due to the perceived sensory discrepancy between the two states and explicit cues of the perturbation removal.…”

“…In Humbert et al (10), it was notable that when initiation and removal of the perturbation were unmasked (i.e., easily identified), aftereffects were not present. Aftereffects are exaggerated movements in the opposite direction of the perturbation effect, exceeding preperturbation levels (1).…”