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: 6.13). 02/2013; 76(1). DOI: 10.1016/j.neuroimage.2013.01.037
Source: PubMed

ABSTRACT INTRODUCTION: 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. METHODS: 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 540s 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. RESULTS: 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. CONCLUSIONS: 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.

  • Source
    [Show abstract] [Hide abstract]
    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.
    03/2014; 2(3). DOI:10.1002/phy2.239
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Paired associative stimulation (PAS), is a novel non-invasive technique where two neural substrates are employed in a temporally coordinated manner in order to modulate cortico-motor excitability within the motor cortex (M1). In swallowing, combined pharyngeal electrical and transcranial-magnetic-stimulation induced beneficial neurophysiological and behavioural effects in healthy subjects and dysphagic stroke patients. Here, we aimed to investigate the whole-brain changes in neural activation during swallowing using functional magnetic resonance imaging (fMRI) following PAS application and in parallel assess associated GABA changes with magnetic resonance spectroscopy (MRS).
    NeuroImage 05/2015; 117. DOI:10.1016/j.neuroimage.2015.05.007 · 6.13 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Background and Objectives: Central and peripheral neural regulation of swallowing and aero-digestive reflexes is unclear in human neonates. Functional near infrared spectroscopy (NIRS) is a noninvasive method to measure changes in oxy-hemoglobin (HbO) and deoxy-hemoglobin (HbD). Pharyngo-esophageal manometry permits evaluation of aero-digestive reflexes. Modalities were combined to investigate feasibility and to test neonatal fronto-parietal cortical changes during pharyngo-esophageal (visceral) stimulation and/or swallowing. Methods: Ten neonates (45.6±3.0wks PMA, 4.1±0.5kg) underwent novel pharyngo-esophageal manometry concurrent with NIRS. To examine esophagus-brain interactions, we analyzed cortical hemodynamic response (HDR) latency and durations during aerodigestive provocation and esophageal reflexes. Data are presented as mean ± SE or %. Results: HDR rates were 8.84 times more likely with basal spontaneous deglutition compared to sham stimuli (P=0.004). Of 182 visceral stimuli, 95% were analyzable for esophageal responses, 38% for HDR, and 36% for both. Of analyzable HDR (N=70): a) HbO concentration (µmol/L) baseline 1.5±0.7 vs. 3.7±0.7 post- stimulus was significant (P=0.02) b) HbD concentration (µmol/L) between baseline 0.1±0.4 vs. post-stimulus -0.5±0.4 was not significant (P=0.73). c) Hemispheric lateralization was 21% left only, 29% right only, and 50% bilateral. During concurrent esophageal and NIRS responses (N=66): a) Peristaltic reflexes were present in 74% and HDR in 61%. b) HDR was 4.75 times more likely with deglutition reflex vs. secondary peristaltic reflex (P=0.016). Conclusions: Concurrent NIRS with visceral stimulation is feasible in neonates, and fronto-parietal cortical activation is recognized. Deglutition contrasting with secondary peristalsis is related to cortical activation; thus, implicating higher hierarchical aerodigestive protective functional neural networks.
    AJP Gastrointestinal and Liver Physiology 05/2014; 307(1). DOI:10.1152/ajpgi.00350.2013 · 3.74 Impact Factor