Somatosensory

Functional MRI during oropharyngeal air-pulse stimulation

Sörös P, Lalone E, Smith R, Stevens T, Theurer J, Menon R, Martin R. Functional MRI of oropharyngeal air-pulse stimulation. Neuroscience 2008;153:1300-1308. PubMed Reprint

Background and rationale

The posterior oral cavity, and adjacent oropharynx, are believed to play critical roles in bolus transport and triggering of pharyngeal swallowing. Supporting this notion, a previous study of our group demonstrated that trains of air pulses delivered to the oropharynx increased the frequency of saliva swallowing in healthy younger adults (Theurer et al. Dysphagia 2005). While the peripheral and brainstem innervation of the oropharynx have been described, the extent to which the oropharynx is represented within central cortical and subcortical structures, and the nature of this representation, remain poorly understood.

Specific aims

This study had two aims:
(1) To investigate the central processing of somatosensory stimulation to the oropharynx with functional magnetic resonance imaging
(2) To clarify the neural mechanisms that contribute to the increased swallowing frequency following oropharyngeal air-pulse stimulation.

Methods

Seven right-handed female volunteers with no history of swallowing, orofacial, gastrointestinal, respiratory, or neurological problems participated in the study (mean age: 27 years, age range: 21 - 45 years). Trains of air pulses were delivered through a custom-made lower dental splint to the left, right or bilateral peritonsillar region of the lateral oropharynx. Splints were made of human-implant-grade silicone with a thickness of less than 2 mm. Functional MR images of the brain were acquired continuously during the stimulation at 4 T using echoplanar imaging. Data were analyzed with FSL using the general linear model (for individual analysis) and an analysis of mixed effects (for group analysis).

Results

Brain activation was characterized by a considerable interindividual variability. Activation strength (as represented by the Z value of the test statistics) and location of the maximum activation varied over a wide range. During bilateral stimulation, activation was seen in the bilateral postcentral gyrus (primary somatosensory cortex, SI), the supplementary motor area (SMA), the anterior cingulate gyrus (cingulate motor areas, CMA) and the bilateral insula. In addition, the bilateral putamen and the right thalamus were active during bilateral stimulation. No significant differences were found between left, right and bilateral stimulation.

Significance and conclusions

The present fMRI study on the central processing of oropharyngeal sensation indicates the activation of a widely distributed network of brain areas. This network includes core areas of the somatosensory system, including the thalamus and the primary somatosensory cortex. In addition, classical motor areas (primary motor cortex, supplementary motor area, cingulate motor areas and basal ganglia) and polymodal areas (such as insula, inferior parietal cortex and frontal cortex) were active following air-pulse stimulation.
The characterization of the neural correlates of oropharyngeal stimulation may have important implications for dysphagia therapy. Our finding that both, the primary somatosensory cortex and the primary motor cortex, are activated during experimental air-pulse stimulation enhances our understanding of the mechanisms of therapeutic air-pulse stimulation in dysphagia.
Moreover, our findings demonstrate the value of the reported air-pulse stimulation technique for the investigation of oral somatosensory processing.

Acknowledgments

This research was supported by a grant from the Heart and Stroke Foundation of Ontario (REM), Ontario Ministry of Health and Long-Term Care Salary Support (R. E. Martin), Premier’s Research Excellence Award (R. E. Martin), Canada Research Chair Support (R. S. Menon), and Canadian Institutes of Health Research Maintenance Grant (R. S. Menon).

Presentation

Sörös P, Lalone E, Smith R, Stevens T, Theurer J, Menon R, Martin R. Functional MRI of oropharyngeal air-pulse stimulation. A talk given at the 2008 meeting of the Dysphagia Research Society in Charleston, SC, USA. Download

Additional work on somatosensory processing

Sörös P, Marmurek J, Tam F, Baker N, Staines WR, Graham SJ. Functional MRI of working memory and selective attention in vibrotactile frequency discrimination. BMC Neuroscience 2007; 8:48. PubMed Abstract Reprint

Sörös P, Knecht S, Bantel C, Imai T, Wüsten R, et al. Functional reorganization of the human primary somatosensory cortex after acute pain demonstrated by magnetoencephalography. Neurosci Lett. 2001;298(3):195-8. PubMed Reprint

Sörös P, Knecht S, Imai T, Gürtler S, Lütkenhöner B, et al. Cortical asymmetries of the human somatosensory hand representation in right- and left-handers. Neurosci Lett. 1999;271(2):89-92. PubMed Reprint