Cerebral Areas Processing Swallowing and Tongue Movement Are Overlapping but Distinct: A Functional Magnetic Resonance Imaging Study

Abstract

Although multiple regions of the cerebral cortex have been implicated in swallowing, the functional contributions of each brain area remain unclear. The present study sought to clarify the roles of these cortical foci in swallowing by comparing brain activation associated with voluntary saliva swallowing and voluntary tongue elevation. Fourteen healthy right-handed subjects were examined with single-event-related functional magnetic resonance imaging (fMRI) while laryngeal movements associated with swallowing and tongue movement were simultaneously recorded. Both swallowing and tongue elevation activated 1) the left lateral pericentral and anterior parietal cortex, and 2) the anterior cingulate cortex (ACC) and adjacent supplementary motor area (SMA), suggesting that these brain regions mediate processes shared by swallowing and tongue movement. Tongue elevation activated a larger total volume of cortex than swallowing, with significantly greater activation within the ACC, SMA, right precentral and postcentral gyri, premotor cortex, right putamen, and thalamus. Although a contrast analysis failed to identify activation foci specific to swallowing, superimposed activation maps suggested that the most lateral extent of the left pericentral and anterior parietal cortex, rostral ACC, precuneus, and right parietal operculum/insula were preferentially activated by swallowing. This finding suggests that these brain areas may mediate processes specific to swallowing. Approximately 60% of the subjects showed a strong functional lateralization of the postcentral gyrus toward the left hemisphere for swallowing, whereas 40% showed a similar activation bias for the tongue elevation task. This finding supports the view that the oral sensorimotor cortices within the left and right hemispheres are functionally nonequivalent.

Normal Swallowing and Functional Magnetic Resonance Imaging: A Systematic Review

“…Fourteen articles that used fMRI in healthy adults while swallowing were relevant and are detailed in Table 1 [41,[53][54][55][56][57][58][59][60][61][62][63][64][65].…”

“…These areas of focus include cortical [41,53,54,56,61,63], cortical and subcortical [55,57,59,60,62,65], lower brain stem and cervical spinal cord regions [58], and the cerebellum and basal ganglia [64].…”

“…Visual cues were provided using written instructions, drawings, or even flashlight [41,53,54,60,65] and auditory cues were typically instructions given by the investigator [64]. Some studies used subject selfinfusion of a water bolus as a swallow stimulus [55] or varied the stimulus depending on the task [57,58,[61][62][63] (i.e., saliva swallow used an audio cue and water swallow was initiated by water infusion).…”

“…Six studies in this review used only event-related designs [54,55,57,59,60,65]. Two additional studies used both block and event-related designs to compare and contrast the two data acquisition methods during swallowing [53,56].…”

“…On the other hand, other studies clearly indicated that an "off" swallow [64] or "no-go" [65] task was included. Swallowing was also compared with motor tasks that were non-swallow-related [53,62,63], swallow-related [56], or both [60]. Swallows of different types were compared with each other (i.e., saliva and water swallows) [41,54,57,59], and comparisons were made between different types of swallows and non-swallow-related tasks [61].…”