Functional connectivity of the cortical swallowing network in humans
Gastroenterology and Hepatology, Department of Medicine, Medical College of Wisconsin, Milwaukee, WI, USA. NeuroImage
(Impact Factor: 6.36).
02/2013; 76(1). DOI: 10.1016/j.neuroimage.2013.01.037
Coherent fluctuations of blood oxygenation level dependent (BOLD) signal have been referred to as "functional connectivity" (FC). Our aim was to systematically characterize FC of underlying neural network involved in swallowing, and to evaluate its reproducibility and modulation during rest or task performance.
Activated seed regions within known areas of the cortical swallowing network (CSN) were independently identified in 16 healthy volunteers. Subjects swallowed using a paradigm driven protocol, and the data analyzed using an event-related technique. Then, in the same 16 volunteers, resting and active state data were obtained for 540 s in three conditions: 1) swallowing task; 2) control visual task; and 3) resting state; all scans were performed twice. Data was preprocessed according to standard FC pipeline. We determined the correlation coefficient values of member regions of the CSN across the three aforementioned conditions and compared between two sessions using linear regression. Average FC matrices across conditions were then compared.
Swallow activated twenty-two positive BOLD and eighteen negative BOLD regions distributed bilaterally within cingulate, insula, sensorimotor cortex, prefrontal and parietal cortices. We found that: 1) Positive BOLD regions were highly connected to each other during all test conditions while negative BOLD regions were tightly connected among themselves; 2) Positive and negative BOLD regions were anti-correlated at rest and during task performance; 3) Across all three test conditions, FC among the regions was reproducible (r>0.96, p<10(-5)); and 4) The FC of sensorimotor region to other regions of the CSN increased during swallowing scan.
1) Swallow activated cortical substrates maintain a consistent pattern of functional connectivity; 2) FC of sensorimotor region is significantly higher during swallow scan than that observed during a non-swallow visual task or at rest.
Available from: Laura Davison Mangilli
- "+Model Functional magnetic resonance and swallowing 9 Table 2 (Continued) Article Objective Study sample Method Results and Conclusions Babaei et al., 2013 27 "
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Aspects of the neuroanatomical representation of swallowing have been investigated in humans through brain mapping techniques, such as functional magnetic resonance imaging (fMRI).
This critical qualitative review of the literature analyzed international scientific publications in the PubMed database that investigated the activation of the central nervous system in humans during the act of swallowing.
This investigation was limited to articles that investigated adults older than 18 years, published in English or Portuguese, between January 2002 and December 2013. Publications that did not have access to the full text, that were repeated by overlapping keywords, case studies, literature reviews, letters to the editor, and those not directly related to the topic of the investigation were excluded.
A total of 649 articles were identified, of which 21 matched the inclusion criteria.
The main purpose of the manuscripts that investigate the swallowing process through fMRI were: to characterize swallowing in different pathologies; to compare swallowing in different age groups; to describe brain activation in different stimulation conditions. These studies indicate multiple cortical regions involved in swallowing control. Overall, the studies indicate that fMRI is a non-invasive and quantitative method that allows the investigation of characteristics that are quite often not clinically visible.
Available from: Donald G Mclaren
- "They reported greater clusters of significantly connected voxels from the anterior and posterior insula/rolandic operculum than the other three chosen seed regions; greater functional connectivity was found from the left insula (Lowell et al. 2012). Babaei et al. (2013) examined functional connectivity among three tasks including volitional swallowing, a visual control task, and resting state. The authors reported very high functional connectivity of the anterior and posterior insula within tasks, but comparisons among the tasks revealed no ignificant differences in functional connectivity. "
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ABSTRACT: The insula is a highly integrated cortical region both anatomically and functionally. It has been shown to have cognitive, social–emotional, gustatory, and sensorimotor functions. Insular involvement in both normal and abnormal swallowing behavior is well established, yet its functional connectivity is unclear. Studies of context-dependent connectivity, or the connectivity during different task conditions, have the potential to reveal information about synaptic function of the insula. The goal of this study was to examine the functional connectivity of specific insular regions (ventral anterior, dorsal anterior, and posterior) with distant cortical regions during four swallowing conditions (water, sour, e-stim, and visual biofeedback) using generalized psychophysiological interactions (gPPI). In 19 healthy adults, we found that the visual biofeedback condition was associated with the most and strongest increases in functional connectivity. The posterior insula/rolandic operculum regions had the largest clusters of increases in functional connectivity, but the ventral anterior insula was functionally connected to a more diverse array of cortical regions. Also, laterality assessments showed left lateralized increases in swallowing functional connectivity. Our results are aligned with reports about the insula's interconnectivity and extensive involvement in multisensory and cognitive tasks.
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ABSTRACT: Intrinsic synchronous fluctuations of the functional magnetic resonance imaging signal are indicative of the underlying 'functional connectivity' (FC) and serve as a technique to study dynamics of the neuronal networks of the human brain. Earlier studies have characterized the functional connectivity of a distributed network of brain regions involved in swallowing, called brain swallowing network (BSN). The potential modulatory effect of esophageal afferent signals on the BSN, however, has not been systematically studied.
Fourteen healthy volunteers underwent steady state functional magnetic resonance imaging across three conditions: (i) transnasal catheter placed in the esophagus without infusion; (ii) buffer solution infused at 1 mL/min; and (iii) acidic solution infused at 1 mL/min. Data were preprocessed according to the standard FC analysis pipeline. We determined the correlation coefficient values of pairs of brain regions involved in swallowing and calculated average group FC matrices across conditions. Effects of subliminal esophageal acidification and nasopharyngeal intubation were determined.
Subliminal esophageal acid stimulation augmented the overall FC of the right anterior insula and specifically the FC to the left inferior parietal lobule. Conscious stimulation by nasopharyngeal intubation reduced the overall FC of the right posterior insula, particularly the FC to the right prefrontal operculum.
The FC of BSN is amenable to modulation by sensory input. The modulatory effect of sensory pharyngoesophageal stimulation on BSN is mainly mediated through changes in the FC of the insula. The alteration induced by subliminal visceral esophageal acid stimulation is in different insular connections compared with that of conscious somatic pharyngeal stimulation.
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