Early deficits in cortical control of swallowing in Alzheimer's disease

Abstract

The goal of this study was to determine whether functional changes in cortical control of swallowing are evident in early Alzheimer's disease (AD), before dysphagia (swallowing impairment) is evident. Cortical function was compared between an early AD group and a group of age-matched controls during swallowing. Swallowing oropharyngeal biomechanics examined from videofluoroscopic recordings were also obtained to more comprehensively characterize changes in swallowing associated with early AD. Our neuroimaging results show that the AD group had significantly lower Blood-Oxygen-Level-Dependent (BOLD) response in many cortical areas that are traditionally involved in normal swallowing (i.e., pre and postcentral gyri, Rolandic and frontal opercula). There were no regions where the AD group showed more brain activity than the healthy controls during swallowing, and only 13% of all active voxels were unique to the AD group, even at this early stage. This suggests that the AD group is not recruiting new regions, nor are they compensating within regions that are active during swallowing. In videofluoroscopic measures, the AD group had significantly reduced hyo-laryngeal elevation than the controls. Although, swallowing impairment is usually noted in the late stages of AD, changes in cortical control of swallowing may begin long before dysphagia becomes apparent.

Figures

Figure 1. Interaction and Group Comparisons (All Swallows)

A. Significant interaction was found only in the left frontal lobe. In graphs: 1=healthy-saliva; 2=healthy-water; 3=healthy-barium; 4=AD-saliva; 5=AD-water; 6=AD-barium B. Group comparisons show significant BOLD response. Healthy > AD activation bilaterally in the ventro-lateral frontal and parietal lobes and right temporal lobes. Abbreviations: SM1 – precentral and poscentral gyri; Inf OFG – inferior frontal orbital lobe; IFG Oper - inferior frontal gyrus pars opecularis; S1 – Postcentral gyrus; MTG – middle temporal gyrus. Left of image is left side of brain. For all figures, ROI restricted cortical regions that are reported in the literature to be involved in swallowing: precentral gyrus, postcentral gyrus, insular cortex, anterior cingulate cortex, supplementary motor area, supramarginal gyrus, superior frontral gyrus, middle frontal gyrus, inferior frontal gyrus, superior parietal gyrus, middle parietal gyrus, inferior parietal gyrus, frontal inferior opercularis, frontal inferior triangularis, and the Rolandic operculum.

Figure 2. Group Comparisons by Swallow Type (Saliva and Water)

A. Saliva swallow healthy > AD contrast shows activation in the frontal, temporal, insular and parietal lobes. B. Water contrasts are significant for BOLD response in frontal, temporal, and parietal lobes. Abbreviations: STP - superior temporal pole; SPG – superior parietal gyrus; ITG – inferor temporal gyrus; SMG – supramarginal gyrus.

Figure 3. Swallow Type Comparisons within the AD Group

A. Saliva > Water contrasts show activation in the frontal and temporal lobes. B. Saliva > Barium differences are found in more regions within the frontal and temporal lobes. C. Water > Saliva is only significant in the parietal lobe. Abbreviations: SMA – supplemental motor area; MCC – middle cingulate cortex.