Tongue Force Training Induces Plasticity of the Lingual Motor Cortex in Young Adult and Aged Rats

Abstract

Tongue exercise programs are used clinically for dysphagia in aged individuals and have been shown to improve lingual strength. However, the neural mechanisms of age-related decline in swallowing function and its association with lingual strength are not well understood. Using an established rat model of aging and tongue exercise, we hypothesized that the motor cortex of aged rats would have a smaller lingual motor map area than young adult rats and would increase in size as a function of tongue exercise. Over 8 weeks, rats either underwent a progressive resistance tongue exercise program (TE), learned the task but did not exercise (trained controls, TC), or were naïve untrained controls (UC). Cortical motor map areas for tongue and jaw were determined using intracortical microstimulation (ICMS). Rats in the TE and TC groups had a significantly larger motor cortex region for the tongue than the UC group. Lingual cortical motor area was not correlated with protrusive tongue force gains and did not differ significantly with age. These results suggest that learning a novel tongue force skill was sufficient to induce plasticity of the lingual motor cortex yet increasing tongue strength with progressive resistance exercise did not significantly expand the lingual motor area beyond the gains that occurred through the skilled learning component.

Tongue Strength Training Increases Daytime Upper Airway Stability in Rats

“…12 As a form of exercise training, tongue training could also induce lingual motor cortex plasticity. 20 We further demonstrated that TST could induce the facilitation of the corticomotor and muscle activity of genioglossus. In addition, the intensity and duration of such excitability gradually increased with prolonged training time, which could be caused by the gradual increase in exercise intensity and difficulty over the course of training.…”

“… 19 Then, do oropharyngeal exercises also improve upper airway collapsibility in this way? Cullins et al 20 found that tongue exercise enlarged the lingual cortical motor area of rats, indicating that tongue training could induce motor cortex plasticity. However, they only assessed it at the end of the 8-week training.…”

A Strength Endurance Exercise Paradigm Mitigates Deficits in Hypoglossal-Tongue Axis Function, Strength, and Structure in a Rodent Model of Hypoglossal Motor Neuron Degeneration

“…Moreover, this 50% > MVLF target is well below the reported 100-150% increase in tongue force (during voluntary drinking) achieved by rats following an 8-week tongue resistance exercise program ( Ma et al, 2017 ; Cullins et al, 2019 ; Glass et al, 2021 ). An important distinction here is that our approach is based on percent effort above natural drinking behavior , whereas most other research groups utilized force lickometer systems that permit estimation of maximum lick force capability ( Connor et al, 2009 ; Behan et al, 2012 ; Cullins et al, 2019 ; Krekeler et al, 2020 ; Glass et al, 2021 ), thereby allowing the exercise target intensity level to be set to a percentage below maximum effort (i.e ., 50–80% of maximum effort) , similar to the maximum bench press test to estimate training intensity percentages for weight-lifting ( Grgic et al, 2020 ). Here, we were interested in the effect of low intensity exercise; therefore, as a starting point, we chose a relatively low effort requirement above MVLF (i.e., 50% > MVLF) as our target for low intensity tongue resistance exercise.…”

“…Data on tongue exercise in MNDs are limited to only a few case studies ( Dworkin and Hartman, 1979 ; Watts and Vanryckeghem, 2001 ) and animal model investigations ( Ma et al, 2017 ) with variable findings, providing insufficient evidence to conclude whether tongue exercise is beneficial or harmful to MND patients ( Plowman, 2015 ; Sheikh and Vissing, 2019 ). However, research outside the MND field has shown that tongue exercise improves upper airway/swallowing deficits caused by stroke ( Robbins et al, 2007 ; Cullins et al, 2019 ), traumatic brain injury ( Steele et al, 2013 ), Parkinson’s disease ( Argolo et al, 2013 ; Ciucci et al, 2013 ; Wang et al, 2018 ), and biological aging ( Connor et al, 2009 ; Kletzien et al, 2013 ) via putative neuroplastic mechanisms that are not yet well understood. Moreover, a growing body of evidence has emerged over the past two decades in favor of exercise training in general (i.e., not tongue-specific) in MND patients ( Sheikh and Vissing, 2019 ).…”

Alterations in white matter microstructural properties after lingual strength exercise in patients with dysphagia

“…While imaging data related to swallowing function and rehabilitation are limited, there have been several studies in animals [6] and humans [7,8] showing changes in microstructural properties and cortical representation postlingual strengthening exercise. A task-based functional magnetic resonance imaging (fMRI) study of a single subject recovering from a stroke showed neural network changes following a lingual strengthening exercise protocol, indicating an effect of training on neuroplasticity [8].…”