Swallowing is a complex sensory-motor process that involves several physiological stages.1 The hypothesis has been proven that multiple brain areas are activated during swallowing, both in children and adults, reflecting regions that are responsible for different aspects of the swallowing process.2

It is known that the cerebral cortex plays an important functional role in the regulation of swallowing.3 The reflexive components of swallowing depend on the brainstem swallowing centers; the onset of swallowing is a voluntary action, which depends on the integrity of the motor areas of the cortex.4

Some aspects of the neuroanatomical representation of cortical function that controls swallowing have been investigated and identified in humans, using brain imaging techniques such as the functional magnetic resonance imaging (fMRI), considered one of the most recent and advanced methods of functional neuroimaging without the use of ionizing radiation.5

The advent of functional magnetic resonance imaging has facilitated or a better detection and quantification of organizational changes in cortical activation, with improved spatial and temporal resolution.5 fMRI is a safe and non-invasive method to investigate the human brain, and has been indicated in the investigation of dysphagia after brain damage.6

The aim of this study was to perform a critical analytic summary of relevant articles on the fMRI findings during swallowing in different groups studied in the international literature.

Since this was a non-experimental study, there was no need for consent forms or institutional ethics committee approval. The Cochrane Handbook precepts were followed to establish the research method.7

The articles used in this study were selected through the PubMed database using the keywords: “deglutition”, “deglutition disorders”, “magnetic resonance”, and “magnetic resonance spectroscopy”, limited to studies performed in adult individuals, published in English and Portuguese, carried out from January 2002 to December 2013.

The search for publications in the database was independently conducted by the researchers to minimize possible citation losses. Each article recovered from the database was independently analyzed by the researchers to determine its relevance for selection and inclusion in the study. Articles in languages other than Portuguese and English were excluded, as well as publications that did not allow access to the full text (obtained from the CAPES Journal Portal) and those repeated due to overlapping keywords. Of the full texts obtained, those related to case studies, literature reviews, studies with animals, letters to the editor, and those that were not directly related to the topic of investigation were excluded. Texts that were effectively related to the research topic were analyzed. All stages of the study were independently conducted by the researchers. In case of disagreement among the researchers, only texts with a consensual final opinion were included. Due to its nature, this was not a single-blind study.

After crossing “deglutition×magnetic resonance”, “deglutition×magnetic resonance spectroscopy”, “deglutition disorders×magnetic resonance”, and “deglutition disorders×magnetic resonance spectroscopy”, a total of 649 articles were found, of which 151 had unavailable summaries. Of the remaining 498, 189 were repeated. Thus, 309 articles were evaluated and of these, only 21 were included in this study.

The reason for the exclusion of 288 articles from the study is shown in Table 1. The 21 selected articles were critically evaluated regarding the following: objectives; number and gender of participants; age range; criteria and evaluation methods; results; and conclusions.

The study results are briefly described in Table 2.

Thirteen different groups of authors were identified. There was no prevalence or differentiation of results between genders. All items had quantitative analysis, supported by statistical results. Of the 21 selected articles, only one23 included the participation of raters, to give reliability to the videofluoroscopic evaluation.

Of the assessed articles, nine2,10,15,17–24 used control groups to make comparisons. In 20 articles,2,8–27 the study design was cross-sectional, with evaluation/performance of a single examination, and in only one21 the design was longitudinal, including the evaluation/performance of examination at two different moments, i.e., pre- and post-operatively. According to the methodological design of this study, all articles used the fMRI exam, but other exams were also used in association, such as electromyography (EMG) and videofluoroscopic swallowing study (VFSS).

The parameters considered for evaluation during the fMRI examination were not consistent. Some studies evaluated the role of swallowing saliva, water, and barium15,16,23,24; others, the swallowing of saliva and/or water2,9,10,13,17–21; whereas another assessed the swallowing of solids, liquids, and semisolids to differentiate consistencies.12 Regarding the instructions to perform the tasks, verbal commands were used, such as “swallow” and “do not swallow”,8,11 as well as the visual and/or auditory and/or gustatory stimulation.14,22,25–27

In general, to analyze the results of the fMRI examination, the blood oxygenation level dependent (BOLD), regions of interest (ROI), cortical lateralization, and diffusion tensor imaging (DTI) criteria were used, as well as time latency.

After a critical review of the articles, it was observed that studies that presented the findings of fMRI during swallowing tasks can be divided into three groups: studies describing brain activation in healthy individuals in different conditions and with different stimuli8,11–14,16,19,22,26,27; studies of patients with diseases/comorbidities, who were compared to healthy individuals,10,17,18,21,23–25 with the following comorbidities: Alzheimer's disease (AD),23,24 obesity,25 tongue cancer,10,21 amyotrophic lateral sclerosis (ALS),17 and ischemic cerebrovascular accident (CVA)18; and studies comparing brain activation at different ages.2,15,20,24

For better presentation and discussion of the study findings, thematic agglutination was performed according to the abovementioned groups. In cases of AD, in brief, significantly lower response (BOLD) was observed in several cortical areas that are traditionally involved in normal swallowing. One of the studies23 concluded that, while the swallowing disorder is generally observed in the final stages of AD, changes in cortical control of swallowing can start long before the dysphagia becomes apparent.

Studies of patients with tongue cancer10,21 sought to determine the adaptation mechanisms of the nervous system, after the glossectomy. The fMRI findings of glossectomized patients showed greater activation in the parietal cortex and adaptive responses (in cortex areas associated with tongue movement planning during swallowing) of the CNS after glossectomy.

The study that explored the structural and functional changes in patients with amyotrophic lateral sclerosis, with or without dysphagia17 found that, during voluntary saliva swallowing, all individuals had the same activated cortical area, but the dysphagic patients showed a decrease in activation. It was also demonstrated that, even in cases in which the disease cannot be detected by conventional MRI, fMRI may disclose the alterations in brain function during swallowing, showing possible swallowing disorders that may develop in the future.

The findings of articles8,9,11–14,16,19,22,26,27 that only studied brain activation in healthy patients in the presence of different stimuli – consistency, flavor, different instructions to perform the task of swallowing, different ages, and different central nervous system foci – showed the following: (1) higher brain activation: during liquid swallowing compared to solids; during water swallowing compared to saliva swallowing; when the food offered had flavor, compared to saliva and water; when there was a verbal command to perform swallowing; when using olfactory, gustatory, and visual stimuli associated with swallowing; and when using sensory stimulation with air injection in the oral cavity during the swallowing (compared to the times in which there was no injection of air); (2) increased activation in areas of interest (programming and performance) when visual and auditory stimuli associated with swallowing were used in combination to carry out the function; (3) that the oral sensorimotor cortex in the left and right hemispheres are not functionally equivalent; and (4) that spontaneous swallowing involves the activation of the cerebellum and basal ganglia, as well as cortical structures.

By analyzing the normal standards for brain activation during swallowing tasks, it was observed that although the contrast analysis failed to identify the specific activation foci for swallowing, overlapping activation maps suggest that the most lateral extent of the precentral and anterior parietal cortex, rostral anterior cingulate cortex, precuneus and left parietal operculum are preferentially activated in swallowing.9 Suzuki et al. (2003),8 however, found that regions activated during swallowing were observed in the sensorimotor cortex, insula, cerebellum, putamen, globus pallidus, thalamus, anterior cingulate gyrus, supplementary motor area, superior temporal gyrus, and in the substantia nigra; the cerebellum was bilaterally activated, especially on the left side; activation of the globus pallidus and putamen was bilateral.

In the past few years, a growing number of neuroimaging studies in healthy subjects have shown multiple cortical regions involved in the control of swallowing. Functional brain imaging may help to elucidate the relevant neural mechanisms, identifying the neural patterns that control this complex sensory-motor action, providing evidence of functional changes in the cerebral cortex after a comorbidity, such as those cited in this review, helping to identify and the correct rehabilitation of dysphagia.

This critical review showed that the examination is of great importance in the early identification of brain alterations, facilitating the choice of a better rehabilitation approach for dysphagic patients, or those at risk for dysphagia, allowing improvement of the clinical picture or risk prevention.

This study demonstrated that the fMRI is a non-invasive, quantitative method that provides specific answers, which are sometimes not clinically identified.

It can be used associated with and/or in addition to other imaging tests to confirm results or as a validation method. As a negative aspect, this study showed that for all examinations, all patients should swallow in the supine position, which may influence the adequate performance of the swallowing function. Another aspect that must be considered is that there was no standardization of the methodologies used in the assessed articles, both in case selection and in the study materials and methods.

The authors declare no conflicts of interest.