The cellular basis of mechanosensation in mammalian tongue

Moayedi, Yalda; Xu, Shan; Obayashi, Sophie K.; Hoffman, Benjamin U.; Gerling, Gregory J.; Lumpkin, Ellen A.

doi:10.1016/j.celrep.2023.112087

Cited by 12 publications

(7 citation statements)

References 71 publications

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“…The tongue is capable of a vast repertoire of unique movements and regional deformations due to its complex patterns of muscle fiber orientations and motor unit activation ( 49 ). Additionally, the tongue has unique mechanosensory structures and acuity comparable to fingertips ( 56 , 57 ). These unique motor and sensory innervations and movement patterns may contribute to divergent recovery and rehabilitation plasticity.…”

Section: Discussionmentioning

confidence: 99%

Differential impact of unilateral stroke on the bihemispheric motor cortex representation of the jaw and tongue muscles in young and aged rats

Cullins,

Connor

2024

Front. Neurol.

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IntroductionDysphagia commonly occurs after stroke, yet the mechanisms of post-stroke corticobulbar plasticity are not well understood. While cortical activity associated with swallowing actions is bihemispheric, prior research has suggested that plasticity of the intact cortex may drive recovery of swallowing after unilateral stroke. Age may be an important factor as it is an independent predictor of dysphagia after stroke and neuroplasticity may be reduced with age. Based on previous clinical studies, we hypothesized that cranial muscle activating volumes may be expanded in the intact hemisphere and would contribute to swallowing function. We also hypothesized that older age would be associated with limited map expansion and reduced function. As such, our goal was to determine the impact of stroke and age on corticobulbar plasticity by examining the jaw and tongue muscle activating volumes within the bilateral sensorimotor cortices.MethodsUsing the middle cerebral artery occlusion rat stroke model, intracortical microstimulation (ICMS) was used to map regions of sensorimotor cortex that activate tongue and jaw muscles in both hemispheres. Young adult (7 months) and aged (30 months) male F344 × BN rats underwent a stroke or sham-control surgery, followed by ICMS mapping 8 weeks later. Videofluoroscopy was used to assess oral-motor functions.ResultsIncreased activating volume of the sensorimotor cortex within the intact hemisphere was found only for jaw muscles, whereas significant stroke-related differences in tongue activating cortical volume were limited to the infarcted hemisphere. These stroke-related differences were correlated with infarct size, such that larger infarcts were associated with increased jaw representation in the intact hemisphere and decreased tongue representation in the infarcted hemisphere. We found that both age and stroke were independently associated with swallowing differences, weight loss, and increased corticomotor thresholds. Laterality of tongue and jaw representations in the sham-control group revealed variability between individuals and between muscles within individuals.ConclusionOur findings suggest the role of the intact and infarcted hemispheres in the recovery of oral motor function may differ between the tongue and jaw muscles, which may have important implications for rehabilitation, especially hemisphere-specific neuromodulatory approaches. This study addressed the natural course of recovery after stroke; future work should expand to focus on rehabilitation.

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Section: Discussionmentioning

confidence: 99%

Differential impact of unilateral stroke on the bihemispheric motor cortex representation of the jaw and tongue muscles in young and aged rats

Cullins,

Connor

2024

Front. Neurol.

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“…Regarding the response of a population of afferents, force‐related cues have been correlated with the total number of active fibres (Friedman et al., 2008; Saal et al., 2009) and the change rate of contact area is probably better related to the number and rate of afferents recruited. Emerging efforts to record afferent population responses using calcium imaging in mice may open new avenues for a direct coupling with patterns of skin surface deformation (Broussard et al., 2018; Moayedi et al., 2023).…”

Section: Discussionmentioning

confidence: 99%

An individual's skin stiffness predicts their tactile discrimination of compliance

Li,

Gerling

2023

The Journal of Physiology

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Individual differences in tactile acuity have been correlated with age, gender and finger size, whereas the role of the skin's stiffness has been underexplored. Using an approach to image the 3‐D deformation of the skin surface during contact with transparent elastic objects, we evaluate a cohort of 40 young participants, who present a diverse range of finger size, skin stiffness and fingerprint ridge breadth. The results indicate that skin stiffness generally correlates with finger size, although individuals with relatively softer skin can better discriminate compliant objects. Analysis of contact at the skin surface reveals that softer skin generates more prominent patterns of deformation, in particular greater rates of change in contact area, which correlate with higher rates of perceptual discrimination of compliance, regardless of finger size. Moreover, upon applying hyaluronic acid to soften individuals’ skin, we observe immediate, marked and systematic changes in skin deformation and consequent improvements in perceptual acuity in differentiating compliance. Together, the combination of 3‐D imaging of the skin surface, biomechanics measurements, multivariate regression and clustering, and psychophysical experiments show that subtle distinctions in skin stiffness modulate the mechanical signalling of touch and shape individual differences in perceptual acuity. imageKey points Although declines in tactile acuity with ageing are a function of multiple factors, for younger people, the current working hypothesis has been that smaller fingers are better at informing perceptual discrimination because of a higher density of neural afferents. To decouple relative impacts on tactile acuity of skin properties of finger size, skin stiffness, and fingerprint ridge breadth, we combined 3‐D imaging of skin surface deformation, biomechanical measurements, multivariate regression and clustering, and psychophysics. The results indicate that skin stiffness generally correlates with finger size, although it more robustly correlates with and predicts an individual's perceptual acuity. In particular, more elastic skin generates higher rates of deformation, which correlate with perceptual discrimination, shown most dramatically by softening each participant's skin with hyaluronic acid. In refining the current working hypothesis, we show the skin's stiffness strongly shapes the signalling of touch and modulates individual differences in perceptual acuity.

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“…Previous work has shown that cutaneous C- and Aδ-LTMRs can be stimulated by rapid cooling of the skin (Li et al, 2011). A recent study using in vivo calcium imaging of mouse trigeminal neurons also identified lingual mechanosensory neurons that were responsive to a cooling stimulus applied to the tongue surface (Moayedi et al, 2023). Here, our experimental setup and the range of force stimuli we employed were designed in such a way that only lingual LTMRs were recorded, excluding the possibility of recording from potential multimodal nociceptors and neurons innervating deeper tissues.…”

Section: Discussionmentioning

confidence: 99%

Trigeminal innervation and tactile responses in mouse tongue

Zhang,

Nagel,

Olson

et al. 2023

Preprint

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The mammalian tongue is richly innervated with somatosensory, gustatory and motor fibers. These form the basis of many ethologically important functions such as eating, speaking and social grooming. Despite its high tactile acuity and sensitivity, the neural basis of tongue mechanosensation remains largely mysterious. Here we explored the organization of mechanosensory afferents in the tongue and found that each lingual papilla is innervated by Piezo2+ trigeminal neurons. Notably, each fungiform papilla contained highly specialized ring-like sensory neuron terminations that circumscribe the taste buds. Myelinated lingual afferents in the mouse lingual papillae did not form corpuscular sensory end organs but rather had only free nerve endings. In vivo single-unit recordings from the trigeminal ganglion revealed two types of lingual low-threshold mechanoreceptors (LTMRs) with conduction velocities in the Aδ range or above and distinct response properties: intermediately adapting (IA) units and rapidly adapting (RA) units. IA units were sensitive to static indentation and stroking, while RA units had a preference for tangential forces applied by stroking. Lingual LTMRs were not directly responsive to rapid cooling or chemicals that can induce astringent or numbing sensations. Genetic labeling of lingual afferents in the tongue revealed at least two types of nerve terminal patterns, involving dense innervation of individual fungiform papillae by multiple putatively distinct afferents, and relatively sparse innervation of filiform papillae. Together, our results indicate that fungiform papillae are mechanosensory structures, while suggesting a simple model that links the functional and anatomical properties of tactile sensory neurons in the tongue.

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The cellular basis of mechanosensation in mammalian tongue

Cited by 12 publications

References 71 publications

Differential impact of unilateral stroke on the bihemispheric motor cortex representation of the jaw and tongue muscles in young and aged rats

Differential impact of unilateral stroke on the bihemispheric motor cortex representation of the jaw and tongue muscles in young and aged rats

An individual's skin stiffness predicts their tactile discrimination of compliance

Trigeminal innervation and tactile responses in mouse tongue

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