The Role of White Matter in the Neural Control of Swallowing: A Systematic Review

Abstract

Background: Swallowing disorders (dysphagia) can negatively impact quality of life and health. For clinicians and researchers seeking to improve outcomes for patients with dysphagia, understanding the neural control of swallowing is critical. The role of gray matter in swallowing control has been extensively documented, but knowledge is limited regarding the contributions of white matter. Our aim was to identify, evaluate, and summarize the populations, methods, and results of published articles describing the role of white matter in neural control of swallowing.Methods: We completed a systematic review with a multi-engine search following PRISMA-P 2015 standards. Two authors screened articles and completed blind full-text review and quality assessments using an adapted U.S. National Institute of Health's Quality Assessment. The senior author resolved any disagreements. Qualitative synthesis of evidence was completed.Results: The search yielded 105 non-duplicate articles, twenty-two of which met inclusion criteria. Twenty were rated as Good (5/22; 23%) or Fair (15/22; 68%) quality. Stroke was the most represented diagnosis (n = 20; 91%). All studies were observational, and half were retrospective cohort design. The majority of studies (13/22; 59%) quantified white matter damage with lesion-based methods, whereas 7/22 (32%) described intrinsic characteristics of white matter using methods like fractional anisotropy. Fifteen studies (68%) used instrumental methods for swallowing evaluations. White matter areas commonly implicated in swallowing control included the pyramidal tract, internal capsule, corona radiata, superior longitudinal fasciculus, external capsule, and corpus callosum. Additional noteworthy themes included: severity of white matter damage is related to dysphagia severity; bilateral white matter lesions appear particularly disruptive to swallowing; and white matter adaptation can facilitate dysphagia recovery. Gaps in the literature included limited sample size and populations, lack of in-depth evaluations, and issues with research design.Conclusion: Although traditionally understudied, there is sufficient evidence to conclude that white matter is critical in the neural control of swallowing. The reviewed studies indicated that white matter damage can be directly tied to swallowing deficits, and several white matter structures were implicated across studies. Further well-designed interdisciplinary research is needed to understand white matter's role in neural control of normal swallowing and in dysphagia recovery and rehabilitation.

Swallowing function in the chronic stage following stroke is associated with white matter integrity of the callosal tract between the interhemispheric S1 swallowing representation areas

“…Prior studies investigating the role of the corpus callosum in swallowing impairment ( Li et al, 2014 , Mourão et al, 2017 ) only used lesion mapping, with no individual quantification of white matter fibers. Therefore, the elaborate approach used in this study is of great importance to the research field relating to biomarkers for dysphagia following brain damage ( Alvar et al, 2021 ).…”

“…Although the widespread pattern of areas relevant to swallowing function derived from functional imaging and patient lesion data have been described extensively, there is a discrepancy in the number of studies investigating the role of structural connectivity. In particular, there are very few studies that apply modern quantification methods, such as fractional anisotrophy (FA; the most suited parameter for quantification of demyelization; see ( Ding et al, 2021 )) on white matter integrity in dysphagic patients following a stroke ( Alvar et al, 2021 ). In the case of dysphagia caused by a stroke, several white matter structures might be of special interest: the corticospinal tract (CST) between the sensorimotor swallowing representation areas and the internal capsule, the callosal tracts interconnecting the sensorimotor centers between hemispheres, and the areas interconnecting the brainstem to swallowing centers.…”

“…We now intended to investigate the relevance of the integrity of swallowing-related callosal fibers for partially restituted swallowing function in the same group of patients. A recent review concerning the role of white matter in the neural control of swallowing ( Alvar et al, 2021 ) identified two studies of the corpus callosum’s role in swallowing impairment, both of which used only lesion mapping, with no individual quantification of white matter fibers ( Li et al, 2014 , Mourão et al, 2017 ). In a prior characterization of somatotopic fibers interconnecting the two hemispheres via the corpus callosum, we described a method that we believe allows for more exact quantification of these fibers, at least in the case of M1 ( Domin and Lotze, 2019 ).…”

Characterization of Two Mouse Chd7 Heterozygous Loss-of-Function Models Shows Dysgenesis of the Corpus Callosum and Previously Unreported Features of CHARGE Syndrome

“…The size of the mammillothalamic tracts increased by 100%, whilst the area of the internal capsule was decreased by 36%. Lesions of the mammillothalamic tract have been associated with impairments in temporal and contextual memory (reviewed in [ 27 ]), and numerous reports have linked motor functions such as swallowing (reviewed in [ 28 ]) or grip strength and hand coordination to the internal capsule. The later are exemplified by functional magnetic resonance imaging (fMRI) studies of stroke patients where motor defects associate with impaired internal capsule integrity, or in animal models with internal capsule lesions [ 29 , 30 ].…”

Expanding Rehabilitation Options for Dysphagia: Skill-Based Swallowing Training

“…Eventually, Daniels et al [37] presented a model that framed swallowing with predominant cortical generation, discussing several cortical and subcortical areas that descend to the brainstem and modulate the pharyngeal response. More recently, the role of white matter structures-specifically, the pyramidal tract, corona radiata, internal capsule, corpus callosum, and superior longitudinal fasciculus-have also been identified as playing crucial roles in the neural control of swallowing [38,39].…”