Neurophysiology of swallowing: effects of age and bolus type

Abstract

This study examined age-related changes in swallowing from an integrated biomechanical and functional imaging perspective in order to more comprehensively characterize changes in swallowing associated with age. We examined swallowing-related fMRI brain activity and videoflouroscopic biomechanics of three bolus types (saliva, water and barium) in 12 young and 11 older adults. We found that age-related neurophysiological changes in swallowing are evident. The group of older adults recruited more cortical regions than young adults, including the pericentral gyri and inferior frontal gyrus pars opercularis and pars triangularis (primarily right-sided). Saliva swallows elicited significantly higher BOLD responses in regions important for swallowing compared to water and barium. In separate videofluoroscopy sessions, we obtained durational measures of supine swallowing. The older cohort had significantly longer delays before the onset of the pharyngeal swallow response and increased residue of ingested material in the pharynx. These findings suggest that older adults without neurological insult elicit more cortical involvement to complete the same swallowing tasks as younger adults.

Fig. 1

fMRI set up and swallow monitoring: A. Bolus delivery and swallow monitoring system: Barium and water are delivered through 2 tubes that extend from programmable syringes. The water-filled line extends from the oral cavity to the pressure transducer to monitor during swallowing activity during scanning. B. Recordings from intra-oral pressure monitoring device during fMRI procedures for each swallowing task.

Fig. 2

Main effect of age: A. Lateral renderings of the brain showing the left and right hemispheres (IFG—inferior frontal gyrus; Tri—triangularis; Oper—opercularis; MFG—middle frontal gyrus; SFG—superior frontal gyrus; M1—precentral gyrus; S1—postcentral gyrus; IPG—inferior parietal gyrus) B. Three coronal slices (IFG—inferior frontal gyrus; Tri—Triangularis; MFG—middle frontal gyrus; SFG—superior frontal gyrus; M1—precentral gyrus; S1—postcentral gyrus; SMA—supplementary motor area). Left of image is left side of brain. C. Activation in the bilateral ventro-lateral postcentral gyri for each swallow type separated by age group. Within the left ventrolateral postcentral gyrus, only saliva swallows in the old are significantly different from saliva swallows in the young (z = −2.5; p(corr)= 0.011).

Fig. 3

Age comparison: Sagital, coronal and axial views of significant BOLD response. Old> Young activation is seen in the right ventro-lateral precentral and postcentral gyri. Young> Old activation is seen in the left precentral and postcentral gyri. Abbreviations: (IFG—inferior frontal gyrus; Tri—triangularis; MFG—middle frontal gyrus; SFG—superior frontal gyrus; M1—precentral gyrus; S1—postcentral gyrus; IPG—inferior parietal gyrus). Coronal (Y) and axial slices (Z): Left of image is left side of brain.

Fig. 4

Main effect of swallow type: A. Lateral renderings of the brain showing the left and right hemispheres (M1—precentral gyrus; IFG—inferior frontal gyrus) B. Three coronal slices (M1—precentral gyrus; IFG—inferior frontal gyrus; Tri—triangularis; Oper—opercularis; SMA—supplementary motor area) Left of image is left side of brain. C. Activation in the shown graphically. Activation in the bilateral inferior frontal gyrus pars opercularis for each swallow type separated by age group.

Fig. 5

Swallow type comparison: Sagittal, coronal and axial views of significant BOLD response. Saliva> Water activation seen in the left ventro-lateral precentral gyrus and bilateral IFG pars opercularis and SMA. Young> Old significant activation is seen in the left precentral gyrus, rolandic and IFG pars opercularis. Water> Saliva activity within the right insular– operculum. Abbreviations: (IFG—inferior frontal gyrus; Tri—Triangularis; Oper—Opercularis; MFG—middle frontal gyrus; SFG—superior frontal gyrus; M1—precentral gyrus; IPG—inferior parietal gyrus; ACC—Anterior Cingulate Cortex; SMA—supplementary motor area). Coronal (Y) and axial slices (Z): Left of image is left side of brain.

Fig. 6

Saliva swallow output signals. Representative saliva swallow output signals from the oral pressure monitoring device for and older and younger adult.