Reproducibility of swallow-induced cortical BOLD positive and negative fMRI activity

Department of Medicine, Medical College of Wisconsin, Milwaukee, USA.
AJP Gastrointestinal and Liver Physiology (Impact Factor: 3.8). 07/2012; 303(5):G600-9. DOI: 10.1152/ajpgi.00167.2012
Source: PubMed


Functional MRI (fMRI) studies have demonstrated that a number of brain regions (cingulate, insula, prefrontal, and sensory/motor cortices) display blood oxygen level-dependent (BOLD) positive activity during swallow. Negative BOLD activations and reproducibility of these activations have not been systematically studied. The aim of our study was to investigate the reproducibility of swallow-related cortical positive and negative BOLD activity across different fMRI sessions. We studied 16 healthy volunteers utilizing an fMRI event-related analysis. Individual analysis using a general linear model was used to remove undesirable signal changes correlated with motion, white matter, and cerebrospinal fluid. The group analysis used a mixed-effects multilevel model to identify active cortical regions. The volume and magnitude of a BOLD signal within each cluster was compared between the two study sessions. All subjects showed significant clustered BOLD activity within the known areas of cortical swallowing network across both sessions. The cross-correlation coefficient of percent fMRI signal change and the number of activated voxels across both positive and negative BOLD networks were similar between the two studies (r ≥ 0.87, P < 0.0001). Swallow-associated negative BOLD activity was comparable to the well-defined "default-mode" network, and positive BOLD activity had noticeable overlap with the previously described "task-positive" network. Swallow activates two parallel cortical networks. These include a positive and a negative BOLD network, respectively, correlated and anticorrelated with swallow stimulus. Group cortical activity maps, as well as extent and amplitude of activity induced by volitional swallowing in the cortical swallowing network, are reproducible between study sessions.

Download full-text


Available from: James Hyde, Nov 16, 2015
  • Source
    • "These reductions were significant in several primary somatosensory areas, indicating a decline in neural processing of sensory signals to coordinate the swallowing response. Babaei et al., 2012 26 To investigate the reproducibility of positive and negative cortical activity (BOLD) related to swallowing in different sessions of fMRI in regions of interest previously demonstrated in other studies. 16 right-handed asymptomatic adult individuals aged 20---34 years, of whom nine were women. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Introduction: Aspects of the neuroanatomical representation of swallowing have been investigated in humans through brain mapping techniques, such as functional magnetic resonance imaging (fMRI). Objective: 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. Methods: 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. Results: A total of 649 articles were identified, of which 21 matched the inclusion criteria. Conclusion: 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.
    Brazilian journal of otorhinolaryngology 09/2015; DOI:10.1016/j.bjorl.2015.08.006 · 0.65 Impact Factor
  • [Show abstract] [Hide abstract]
    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 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. 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.
    NeuroImage 02/2013; 76(1). DOI:10.1016/j.neuroimage.2013.01.037 · 6.36 Impact Factor
  • [Show abstract] [Hide abstract]
    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.
    Neurogastroenterology and Motility 12/2013; 25(12):992-e779. DOI:10.1111/nmo.12238 · 3.59 Impact Factor
Show more