The Effect of Swallowing Cues in Healthy Individuals: An Exploratory Study.

The goal of this study was to determine whether providing verbal and visual cues about swallowing changes the timing of swallowing events, and whether this information interacts with bolus volume. 20 healthy adults swallowed 5 ml and 15 ml liquid barium mixed with orange juice under videofluoroscopy during 2 conditions: one condition absent swallowing-specific cues and one condition with verbal and visual input about the swallowing process. Outcome measures included the timing of 10 swallowing events and the number of swallows per bolus. As expected, volume had a significant effect on all outcome measures (p < 0.05). Three timing events differed by cueing condition: 1. swallowing reaction time was earlier for control (- 9.45 ms vs. - 2.01 ms, p = 0.033); 2. the time between initial hyoid movement and maximum hyoid elevation was longer for control (152.85 ms vs. 143.79 ms; p = 0.015); and 3. the onset of upper esophageal sphincter opening occurred later after bolus entry into the pharynx for the swallowing cues condition (111.9 ms vs. 103.31 ms; p = 0.017); however, effect sizes were small (< 0.2). There was a significant interaction between cue condition and bolus volume on swallowing frequency, such that the mean number of swallows of 15 ml boluses was slightly higher during the control condition than during the swallowing cues condition. There were no significant interactions on measures of timing, suggesting distinct mechanisms for the effect of bolus volume and cues on swallowing kinematics. Further research is needed to investigate the effects of different cue modalities and focus (internal vs. external) on swallowing physiology.

Effects of Submental Surface Electrical Stimulation on Swallowing Kinematics in Healthy Adults: An Error-Based Learning Paradigm.

Purpose: Hyoid bone and laryngeal approximation aid airway protection (laryngeal vestibule closure) while moving toward their peak superior and anterior positions during swallowing. Submental surface electrical stimulation (SES) is a therapeutic technique that targets the muscles that move the hyoid bone during swallowing. It is unknown whether submental SES only increases peak hyoid bone swallowing positions but not peak laryngeal swallowing positions, which could require faster or greater laryngeal movement to achieve adequate laryngeal vestibule closure. Method: We examined the effects of submental SES on hyo-laryngeal kinematics in 30 healthy adults who swallowed 50 times using an error-based learning paradigm. Results: Submental SES did not alter any hyo-laryngeal swallowing kinematic. However, submental SES significantly changed the starting position of the hyoid bone just prior to the swallow onset (more anterior; p = .003). On average, submental SES immediately prior to swallow onset can position the hyoid approximately 20% closer to its peak swallowing point. Conclusions: These findings indicate that electrical stimulation of the agonists for hyoid movement might not alter swallowing outcomes tested in this study. However, submental SES could have clinical utility by minimizing swallowing impairments related to reduced hyoid swallowing range of motion in individuals with dysphagia.

Swallowing Kinematic Differences Across Frozen, Mixed, and Ultrathin Liquid Boluses in Healthy Adults: Age, Sex, and Normal Variability.

Purpose: The aim of this study was to examine the effects of frozen and mixed-consistency boluses on the swallowing physiology of younger and older adults. We also aimed to quantify factors that lead to increased variability in swallowing outcomes (i.e., age, sex, bolus type). Method: Forty-one healthy adults (18-85 years old) swallowed 5 blocks of 5 different boluses: 10-ml ultrathin liquid, a teaspoon of iced barium, a teaspoon of room-temperature pudding, a teaspoon of frozen pudding, and ultrathin barium with chocolate chips. All data were recorded with videofluoroscopy and underwent detailed timing kinematic measurements. Results: Neither barium ice nor frozen pudding sped up swallow responses. Many healthy adults initiated swallowing with the bolus as deep as the pyriform sinuses. Swallowing temporal kinematics for ultrathin liquid consistencies are most different from all others tested, requiring the best possible physiological swallowing performance in younger and older healthy individuals (i.e., faster reaction times, longer durations) compared with other bolus types tested. In each measure, older adults had significantly longer durations compared with the younger adults. More variability in swallowing kinematics were seen with age and laryngeal vestibule kinematics. Conclusion: This study provides important contributions to the literature by clarifying normal variability within a wide range of swallowing behaviors and by providing normative data from which to compare disordered populations.

Elucidating inconsistencies in dysphagia diagnostics: Redefining normal.

Speech-language pathologists (SLPs) are the primary healthcare providers responsible for the evaluation and treatment of dysphagia. Fundamental to this role is the ability to make accurate clinical judgements to distinguish between normal versus disordered swallowing for subsequent treatment planning. In this review, we highlight recent data collected from practising clinicians in the USA that reveal low levels of agreement across clinicians and poor to moderate levels of accuracy for making binary diagnostic ratings (normal vs. disordered). We then propose and discuss barriers that may represent challenges to practising SLP's understanding of normal swallowing physiology. Proposed barriers include: (1) an educational focus on the disordered system; (2) system 1 processing; (3) complexity of the swallowing system; (4) inability to directly visualise the swallowing process; (5) degree of variability of normal swallowing; and (6) high clinical productivity requirements. This article concludes with suggestions for reducing identified educational and clinical barriers to ultimately improve diagnostic decision-making practices and to benefit patient-related outcomes in dysphagia management.

Motor transfer from the corticospinal to the corticobulbar pathway.

There are multiple descending neural pathways, including the corticospinal pathway (CS) and the corticobulbar pathway (CB). The corticospinal pathway has been shown to exhibit within-pathway (CS-to-CS) motor transfer. However, motor transfer across each pathway (CS-to-CB or CB-to-CS) has yet to be studied in depth. The aim of the present study was to examine the effects of cross-pathway motor transfer between the ankle (CS) and tongue (CB) after training with a ballistic goal-directed motor task. Twelve healthy participants were recruited for this two-day experimental study. Six participants performed a ballistic goal-directed task with their ankle on Day 1 (ankle dorsiflexion), then tongue on Day 2 (elevate tongue against IOPI). The other 6 participants performed the same task with their tongue on Day 1, then ankle on Day 2. Both the ankle and tongue tasks (50 trials each) required matching force and time to a visual target. Our findings indicate that participants who underwent ankle training on Day 1 exhibited decreased tongue force error on Day 2 compared with participants who completed the tongue training on Day 1, with no prior ankle training (p = 0.02) (i.e. greater accuracy). This finding suggests that cross-pathway transfer from the corticospinal pathway to the corticobulbar pathway occurred with respect to force error. In other words, training of the ankle (CS) translated to improved training performance of the tongue (CB) through a reduction in force error. However, the reverse was not true - training the tongue did not elicit improved performance of the ankle. Nonetheless, if training with the corticospinal pathway can lead to improved corticobulbar pathway functioning, incorporating multi-pathway rehabilitation techniques might be valuable for clinicians across medical disciplines.

Integration of visual feedback and motor learning: Corticospinal vs. corticobulbar pathway.

Although movement is controlled by different descending pathways, it remains unknown whether the integration of visual feedback and motor learning differs for movements controlled by different descending pathways. Here, we compare motor control and learning of the ankle joint and tongue because they are primarily controlled by the corticospinal and corticobulbar pathways, respectively. Twelve young adults (19.63 ±â€¯2.11 years, 6 females) practiced a tracking task (combination of 0.02, 0.37, 0.5, and 1 Hz) with ankle dorsiflexion and with tongue elevation for 100 trials. The participants practiced each effector (ankle and tongue) in different days and the order of the effector was counterbalanced. Following practice, participants performed the same tracking task with concurrent contractions of the tongue and ankle (dual tracking task; transfer) with three different visual feedback conditions (no visual feedback, visual feedback only for ankle, visual feedback only for tongue). We quantified the force accuracy (RMSE) from each effector during the practice and transfer periods. During practice, the force accuracy and performance improvement to the visuomotor task was greater for the ankle dorsiflexion than tongue elevation. During the transfer task, the ankle dorsiflexion was more accurate than tongue elevation, independent of whether visual feedback was given for the ankle or tongue. The greater performance improvement for the ankle dorsiflexion during practice was related to superior transfer performance. These findings suggest that the corticospinal pathway integrates visual feedback more efficiently than the corticobulbar pathway, which enhances performance and learning of visuomotor tasks.

Taste Perception and Water Swallow Screen Results in Old-Old Women.

Changes in both swallowing and taste commonly occur in advanced age, though the relationship between the two is unknown. This study examined the association between a water swallow screen test and taste identification and intensity rating. Participants included 47 community-dwelling women aged 85-94 years. Participants completed three trials of a water swallow screen and were observed for signs of aspiration, which, if present, indicated failure. Four pure taste stimuli at low and high concentrations and water were presented, and participants selected one of five taste labels and rated their intensity on the generalized Labeled Magnitude Scale. Ratios of intensity ratings were computed for each taste stimulus to compare the perception of low and high concentrations. The association between water swallow screen failure, correct taste identification, and taste intensity ratio was evaluated with logistic regression modeling, with mediating factors of frailty and number of comorbidities. Failure of three water swallow screen trials was associated with a higher taste intensity ratio for caffeine (bitter) and a lower taste intensity ratio for sucrose (sweet). Correct identification of taste, frailty, and number of comorbidities were not associated with failure of any number of water swallow screen trials. Intensity ratings of certain tastes may be associated with swallowing in old-old women. Heightened vigilance in this population may be necessary to prevent complications related to dietary intake.

Examination of swallowing maneuver training and transfer of practiced behaviors to laryngeal vestibule kinematics in functional swallowing of healthy adults.

Swallowing maneuvers are routinely trained in dysphagia rehabilitation with the assumption that practiced behaviors transfer to functional swallowing, however transfer is rarely examined in the deglutition literature. The goal of this study was to train the volitional laryngeal vestibule closure (vLVC) maneuver, which is a swallowing maneuver that targets prolonged laryngeal vestibule closure (LVC). In two different training experiments, 69 healthy adults underwent Long-hold (hold vLVC as long as possible) or Short-hold vLVC training (hold vLVC for 2s). Before and after vLVC training, natural swallows (swallowing without a therapeutic technique) were completed. The outcome variables included laryngeal vestibule closure reaction time and the duration of laryngeal vestibule closure. Results indicate that during both Long-hold and Short-hold vLVC trainings, vLVC swallows had faster laryngeal vestibule closure reaction times and longer durations of laryngeal vestibule closure than in pre-training 5ml liquid swallows. However, only faster laryngeal vestibule closure reaction times transferred to post-training 5ml liquid swallows (20-24% faster), but not prolonged durations of laryngeal vestibule closure. Our findings suggest that swallowing maneuver training has the potential to induce transfer of what was practiced to functional swallowing behavior, although not all practiced behaviors may generalize. These findings are significant for bolstering the effectiveness of dysphagia management in medical settings and should be tested in individuals with dysphagia.

Effects of chin-up posture on the sequence of swallowing events.

BACKGROUND: Chin-up posture is frequently used to manage oral dysphagia after head and neck cancer. This prospective study investigates the effects of chin-ups on the sequence of pharyngeal swallowing events. METHODS: Twelve healthy young adults performed 45 consecutive swallows of 5 mL water across 3 phases on videofluoroscopy: 5 swallows in the neutral head position; 30 swallows during chin-up posture; and 10 swallows in the neutral head position. Swallowing kinematic and bolus flow measures for 9 swallowing events were recorded. Linear trends were analyzed across 30 chin-up swallows; pairwise comparison was used to compare the 3 phases. RESULTS: Time to hyoid peak and laryngeal vestibule closure changed abruptly during chin-up swallowing compared to the initial neutral position. No measure changed across 30 chin-up swallows. Time of hyoid burst decreased upon returning to the neutral position. CONCLUSION: Our findings indicate that chin-up posture challenges the pharyngeal sequence of events for both swallowing kinematics and bolus flow. © 2017 Wiley Periodicals, Inc. Head Neck 39: 947-959, 2017.

Kinematic Visual Biofeedback Improves Accuracy of Learning a Swallowing Maneuver and Accuracy of Clinician Cues During Training.

Submental surface electromyography (ssEMG) visual biofeedback is widely used to train swallowing maneuvers. This study compares the effect of ssEMG and videofluoroscopy (VF) visual biofeedback on hyo-laryngeal accuracy when training a swallowing maneuver. Furthermore, it examines the clinician's ability to provide accurate verbal cues during swallowing maneuver training. Thirty healthy adults performed the volitional laryngeal vestibule closure maneuver (vLVC), which involves swallowing and sustaining closure of the laryngeal vestibule for 2 s. The study included two stages: (1) first accurate demonstration of the vLVC maneuver, followed by (2) training-20 vLVC training swallows. Participants were randomized into three groups: (a) ssEMG biofeedback only, (b) VF biofeedback only, and (c) mixed biofeedback (VF for the first accurate demonstration achieving stage and ssEMG for the training stage). Participants' performances were verbally critiqued or reinforced in real time while both the clinician and participant were observing the assigned visual biofeedback. VF and ssEMG were continuously recorded for all participants. Results show that accuracy of both vLVC performance and clinician cues was greater with VF biofeedback than with either ssEMG or mixed biofeedback (p < 0.001). Using ssEMG for providing real-time biofeedback during training could lead to errors while learning and training a swallowing maneuver.

Respiratory training in an individual with amyotrophic lateral sclerosis.

We examined the impact of expiratory muscle strength training on maximum expiratory pressure, cough spirometry, and disease progression in a 71-year-old male with amyotrophic lateral sclerosis. Maximum expiratory pressure declined 9% over an 8-week sham training period, but subsequently improved by 102% following 8 weeks of expiratory muscle strength training. Improvements in cough spirometry and mitigated disease progression were also observed post expiratory muscle strength training. Improvements in maximum expiratory pressures were maintained 6 months following expiratory muscle strength training and were 79% higher than baseline data obtained 301 days prior. In this spinal-onset amyotrophic lateral sclerosis patient, respiratory training improved subglottic air pressure generation and sequential cough generation.

The Relationship Between Submental Surface Electromyography and Hyo-Laryngeal Kinematic Measures of Mendelsohn Maneuver Duration.

PURPOSE: The Mendelsohn Maneuver (MM) is a commonly prescribed technique that is taught to individuals with dysphagia to improve swallowing ability. Due to cost and safety concerns associated with videofluoroscopy (VFS) use, submental surface electromyography (ssEMG) is commonly used in place of VFS to train the MM in clinical and research settings. However, it is unknown whether ssEMG accurately reflects the prolonged hyo-laryngeal movements required for execution of the MM. The primary goal of this study was to examine the relationship among ssEMG duration, duration of laryngeal vestibule closure, and duration of maximum hyoid elevation during MM performance. METHOD: Participants included healthy adults and patients with dysphagia due to stroke. All performed the MM during synchronous ssEMG and VFS recording. RESULTS: Significant correlations between ssEMG duration and VFS measures of hyo-laryngeal kinematic durations during MM performance ranged from very weak to moderate. None of the correlations in the group of stroke patients reached statistical significance. CONCLUSION: Clinicians and researchers should consider that the MM involves novel hyo-laryngeal kinematics that may be only moderately represented with ssEMG. Thus, there is a risk that these target therapeutic movements are not consistently being trained.

The Sequence of Swallowing Events During the Chin-Down Posture.

PURPOSE: This study investigated the effect of the chin-down posture on the sequence of swallowing events in healthy adults. METHOD: Sixteen healthy participants performed 45 5-ml thin liquid swallows during videofluoroscopy: 5 neutral head position, 30 chin-down posture, and then 10 neutral head position. Eight swallowing events were measured: the time of hyoid burst, bolus head in the pharynx, bolus tail in the pharynx, laryngeal vestibule closure (LVC), upper esophageal sphincter (UES) opening, bolus head in the UES, bolus tail exiting the pharynx, and laryngeal vestibule opening (LVO). RESULTS: Our key finding is that LVC was one of the first 3 swallowing events in 69% of neutral swallows and in 78% of chin-down swallows (p = .006). Also, LVO occurred last in 14% of chin-down swallows but never occurred last in the preceding neutral swallows (p ≤ .001). Thus, in chin-down swallows, LVC occurred earlier and LVO occurred later. CONCLUSIONS: The chin-down posture may be beneficial for individuals with delayed onset of LVC and reduced duration of the LVC. Future studies are needed to examine this effect in individuals with dysphagia.

Surface electrical stimulation perturbation context determines the presence of error reduction in swallowing hyolaryngeal kinematics.

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.

Differential psychophysiological interactions of insular subdivisions during varied oropharyngeal swallowing tasks.

Abstract The insula is a highly integrated cortical region both anatomically and functionally. It has been shown to have cognitive, social-emotional, gustatory, and sensorimotor functions. Insular involvement in both normal and abnormal swallowing behavior is well established, yet its functional connectivity is unclear. Studies of context-dependent connectivity, or the connectivity during different task conditions, have the potential to reveal information about synaptic function of the insula. The goal of this study was to examine the functional connectivity of specific insular regions (ventral anterior, dorsal anterior, and posterior) with distant cortical regions during four swallowing conditions (water, sour, e-stim, and visual biofeedback) using generalized psychophysiological interactions (gPPI). In 19 healthy adults, we found that the visual biofeedback condition was associated with the most and strongest increases in functional connectivity. The posterior insula/rolandic operculum regions had the largest clusters of increases in functional connectivity, but the ventral anterior insula was functionally connected to a more diverse array of cortical regions. Also, laterality assessments showed left lateralized increases in swallowing functional connectivity. Our results are aligned with reports about the insula's interconnectivity and extensive involvement in multisensory and cognitive tasks.

Human hyolaryngeal movements show adaptive motor learning during swallowing.

The hyoid bone and larynx elevate to protect the airway during swallowing. However, it is unknown whether hyolaryngeal movements during swallowing can adjust and adapt to predict the presence of a persistent perturbation in a feed-forward manner (adaptive motor learning). We investigated adaptive motor learning in nine healthy adults. Electrical stimulation was administered to the anterior neck to reduce hyolaryngeal elevation, requiring more strength to swallow during the perturbation period of this study. We assessed peak hyoid bone and laryngeal movements using videofluoroscopy across thirty-five 5-ml water swallows. Evidence of adaptive motor learning of hyolaryngeal movements was found when (1) participants showed systematic gradual increases in elevation against the force of electrical stimulation and (2) hyolaryngeal elevation overshot the baseline (preperturbation) range of motion, showing behavioral aftereffects, when the perturbation was unexpectedly removed. Hyolaryngeal kinematics demonstrates adaptive, error-reducing movements in the presence of changing and unexpected demands. This is significant because individuals with dysphagia often aspirate due to disordered hyolaryngeal movements. Thus, if rapid motor learning is accessible during swallowing in healthy adults, patients may be taught to predict the presence of perturbations and reduce errors in swallowing before they occur.

New directions for understanding neural control in swallowing: the potential and promise of motor learning.

Oropharyngeal swallowing is a complex sensorimotor phenomenon that has had decades of research dedicated to understanding it more thoroughly. However, the underlying neural mechanisms responsible for normal and disordered swallowing remain very vague. We consider this gap in knowledge the result of swallowing research that has been broad (identifying phenomena) but not deep (identifying what controls the phenomena). The goals of this review are to address the complexity of motor control of oropharyngeal swallowing and to review the principles of motor learning based on limb movements as a model system. We compare this literature on limb motor learning to what is known about oropharyngeal function as a first step toward suggesting the use of motor learning principles in swallowing research.

Electrical stimulation and swallowing: how much do we know?

Consequences of dysphagia substantially reduce quality of life, increase the risk of medical complications and mortality, and pose a substantial cost to healthcare systems. As a result, it is of no wonder that the clinical and scientific communities are showing interest in new avenues for dysphagia rehabilitation. Electrical stimulation (e-stim) for the treatment of swallowing impairments is among the most studied swallowing interventions in the published literature, yet many unanswered questions about its efficacy remain. In the meantime, many speech-language pathologists who treat dysphagia are attending educational and training sessions to obtain certifications to use this technique. Here, we review the values and limitations of the published literature on the topic of e-stim for swallowing to assist clinicians in decision making in their clinical practice. The discussion provides a review of swallowing anatomy and physiology, the fundamentals of e-stim, and information essential for the readers' independent critique of these studies--all of which are crucial for evaluating the possible effects of e-stim.

Adaptation of swallowing hyo-laryngeal kinematics is distinct in oral vs. pharyngeal sensory processing.

Before a bolus is pushed into the pharynx, oral sensory processing is critical for planning movements of the subsequent pharyngeal swallow, including hyoid bone and laryngeal (hyo-laryngeal) kinematics. However, oral and pharyngeal sensory processing for hyo-laryngeal kinematics is not fully understood. In 11 healthy adults, we examined changes in kinematics with sensory adaptation, sensitivity shifting, with oropharyngeal swallows vs. pharyngeal swallows (no oral processing), and with various bolus volumes and tastes. Only pharyngeal swallows showed sensory adaptation (gradual changes in kinematics with repeated exposure to the same bolus). Conversely, only oropharyngeal swallows distinguished volume differences, whereas pharyngeal swallows did not. No taste effects were observed for either swallow type. The hyo-laryngeal kinematics were very similar between oropharyngeal swallows and pharyngeal swallows with a comparable bolus. Sensitivity shifting (changing sensory threshold for a small bolus when it immediately follows several very large boluses) was not observed in pharyngeal or oropharyngeal swallowing. These findings indicate that once oral sensory processing has set a motor program for a specific kind of bolus (i.e., 5 ml water), hyo-laryngeal movements are already highly standardized and optimized, showing no shifting or adaptation regardless of repeated exposure (sensory adaptation) or previous sensory experiences (sensitivity shifting). Also, the oral cavity is highly specialized for differentiating certain properties of a bolus (volume) that might require a specific motor plan to ensure swallowing safety, whereas the pharyngeal cavity does not make the same distinctions. Pharyngeal sensory processing might not be able to adjust motor plans created by the oral cavity once the swallow has already been triggered.

Tactile, gustatory, and visual biofeedback stimuli modulate neural substrates of deglutition.

It has been well established that swallowing kinematics are modified with different forms of exogenous and endogenous input, however the underlying neural substrates associated with these effects are largely unknown. Our objective was to determine whether the swallowing BOLD response is modulated with heightened sensory modalities (taste, cutaneous electrical stimulation, and visual biofeedback) compared to water ingestion (control) in healthy adults across the age span. Habituation and sensitization were also examined for each sensory condition. Our principal findings are that each sensory swallowing condition activated components of the swallowing cortical network, plus regions associated with the particular sensory modality (i.e. primarily frontal motor planning and integration areas with visual condition). Overall, the insula was most commonly active among the sensory modalities. We also discuss gradual increases and decreases in BOLD signal with repeated exposures for each condition. We conclude that both stimulus- and intention-based inputs have unique cortical swallowing networks relative to their modality. This scientific contribution advances our understanding of the mechanisms of normal swallowing cortical control and has the potential to impact clinical uses of these modalities in treatments for neurogenic dysphagia.