Effects of aging on brain networks during swallowing: general linear model and independent component analyses

Abstract

Swallowing disorders occur more frequently in older adults. However, the effects of the aging process on neural activation when swallowing are unclear. We aimed to identify neural regions activated during swallowing and evaluate changes in neural activation and neural networks with aging. Using a general linear model (GLM) and independent component (IC) analyses, blood oxygen level-dependent (BOLD) signals were observed in the lateral precentral gyrus, postcentral gyrus, anterior insular cortices, supramarginal gyri, and medial frontal gyrus during swallowing. The right thalamus and anterior cingulate gyri were found to be active areas by GLM and IC analyses, respectively. In the correlational analyses, age was negatively correlated with BOLD signals of the lateral precentral gyri, postcentral gyri, and insular cortices in swallowing tasks. Additionally, correlation analyses between ICs of all participants and age revealed negative correlations in the right supramarginal gyrus, both anterior cingulate cortices, putamen, and cerebellum. In the network analysis, the BOLD signal positively correlated with age in the default mode network (DMN), and was negatively correlated in the lateral precentral gyri, postcentral gyri, and insular cortices. The amplitude of low-frequency fluctuations was significantly decreased in the DMN and increased in swallowing-related areas during swallowing tasks. These results suggest that aging has negative effects on the activation of swallowing-related regions and task-induced deactivation of the DMN. These changes may be used to detect early functional decline during swallowing.

Clinical determinants and neural correlates of presbyphagia in community-dwelling older adults

“…However, age was associated with increased brain-activation in the default-mode-network, which is assumed to represent resting-state activation. The authors conclude that aging decreases task-related activation of the swallowing network and reduces task-induced deactivation of the default mode network ( Tae et al, 2021 ). A further fMRI study on 9 healthy older participants (age range 66–77 years) showed reduced activation, especially in somatosensory areas compared to a young control group.…”

“…In addition, neurostimulation techniques in dysphagia rehabilitation also modulate the cortical swallowing network (Suntrup et al, 2013b(Suntrup et al, , 2015. However, there are only few studies investigating age-related changes in central swallowing control (Martin et al, 2007;Humbert et al, 2009;Malandraki et al, 2010Malandraki et al, , 2011bTeismann et al, 2010;Windel et al, 2015;Tae et al, 2021), with partly inconclusive results: Some studies indicate an increase in cortical activation 10.3389/fnagi.2022.912691 (Martin et al, 2007;Humbert et al, 2009;Teismann et al, 2010), while other studies assume that the swallowing network remains essentially stable regardless of age (Windel et al, 2015) or even decreases in somatosensory areas (Malandraki et al, 2011b;Tae et al, 2021). Common to all of these studies is that neither swallowing function itself nor clinical parameters were related to neuroimaging findings.…”

Brain functional activity of swallowing: A meta‐analysis of functional magnetic resonance imaging

“…This inference may be derived from the action execution function of the SMA proper 66 . But these articles did not segment SMA, or reported activation of SMA proper only, while pre‐SMA has only recently been mentioned as possibly being related to swallowing 14 . In early studies, pre‐SMA was considered to be associated with motor sequences, learning and executive control, which is more like a pre‐frontal area than a motor area.…”

“…66 But these articles did not segment SMA, or reported activation of SMA proper only, while pre-SMA has only recently been mentioned as possibly being related to swallowing. 14 In early studies, pre-SMA was considered to be associated with motor sequences, learning and executive control, which is more like a pre-frontal area than a motor area.. 66,68 Some articles suggested that pre-SMA played an important role in controlling voluntary movements by inhibiting or evoking movement. 64,68 Our findings on pre-SMA activation during saliva swallowing supported that advanced motor control is required for saliva swallowing.…”

“…10 The use of fMRI to study the activation areas of swallowing has reproducibility. 11 Nonetheless, some studies have controversial views, such as which part of Brodmann area (BA) 6 is activated during swallowing 10,[12][13][14] and whether swallowing significantly activated primary motor cortex. 15 The discrepancies between studies may be due to the following reasons: (1) the potential artefacts caused by movement 16 or automatic saliva swallowing while lying in the supine position 10,13 ; (2) a variety of acquisition, 9,17 pre-processing 17,18 and analysis techniques 18 ; (3) differences in age, 15,19 sample size, 13,17 bolus types 19 and task paradigms.…”