Neural activation of swallowing and swallowing-related tasks in healthy young adults: an attempt to separate the components of deglutition

Abstract

Understanding the underlying neural pathways that govern the highly complex neuromuscular action of swallowing is considered crucial in the process of correctly identifying and treating swallowing disorders. The aim of the present investigation was to identify the neural activations of the different components of deglutition in healthy young adults using functional magnetic resonance imaging (fMRI). Ten right-handed young healthy individuals were scanned in a 3-Tesla Siemens Allegra MRI scanner. Participants were visually cued for both a "Swallow" task and for component/control tasks ("Prepare to swallow", "Tap your tongue", and "Clear your throat") in a randomized order (event-related design). Behavioral interleaved gradient (BIG) methodology was used to address movement-related artifacts. Areas activated during each of the three component tasks enabled a partial differentiation of the neural localization for various components of the swallow. Areas that were more activated during throat clearing than other components included the posterior insula and small portions of the post- and pre-central gyri bilaterally. Tongue tapping showed higher activation in portions of the primary sensorimotor and premotor cortices and the parietal lobules. Planning did not show any areas that were more activated than in the other component tasks. When swallowing was compared with all other tasks, there was significantly more activation in the cerebellum, thalamus, cingulate gyrus, and all areas of the primary sensorimotor cortex bilaterally.

Figure 1

Time course of the output of a bellows positioned around the subject's neck over the thyroid cartilage for a water‐swallowing trial (red), for a single subject. Time = 0 indicates the time at which the subject was visually cued to complete the task. AU on the y‐axis stands for Arbitrary Units. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 2

Time course of the output of a bellows positioned around the subject's neck over the thyroid cartilage for one throat‐clearing event (blue) for a single subject. Time = 0 indicates the time at which the subject was visually cued to complete the task. AU stands for on the y‐axis Arbitrary Units. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 3

a–d: Areas of significant activation (Z score = 3–5.5) during swallowing (N = 10). Boxes report the major activated areas. Images are shown in radiological convention (the right hemisphere is shown on the left). Coordinates are given in MNI space in mm. A = Anterior, P = Posterior, L= Left Hemisphere, R = Right Hemisphere.

Figure 4

a and b: Areas of significant activation (Z score = 3–5.5) during throat clearing (N = 10). The boxes report the major activated areas. Images are shown in radiological convention (the right hemisphere is shown on the left). Coordinates are given in MNI space. A = Anterior, P = Posterior, L = Left Hemisphere, R = Right Hemisphere.

Figure 5

a–c: Areas of significant activation (Z score = 3–5.3) during tongue tapping (N = 10). The boxes report the major activated areas. Images are shown in radiological convention (the right hemisphere is shown on the left). Coordinates are given in MNI space. A = Anterior, P = Posterior, L = Left Hemisphere, R = Right Hemisphere.

Figure 6

Areas of significant activation (Z score = 3–4.3) during planning of deglutition without execution. The boxes report the major activated areas. Images are shown in radiological convention (the right hemisphere is shown on the left). Coordinates are given in MNI space. A = Anterior, P = Posterior, L = Left Hemisphere, R = Right Hemisphere.

Figure 7

Areas of most significant activation during swallowing (shown in red), during throat clearing (shown in blue), and during tongue tapping (shown in yellow). Boxes report the areas. Images are shown in radiological convention (the right hemisphere is shown on the left). Coordinates are given in MNI space.

Figure 8

Mean percent signal change in all ROIs for all four tasks. BA = Brodmann Area. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]