Enhancing effects of flavored nutritive stimuli on cortical swallowing network activity

Abstract

A better understanding of the central control of the physiology of deglutition is necessary for devising interventions aimed at correcting pathophysiological conditions of swallowing. Positive modulation of the cortical swallowing network can have clinical ramifications in dysphagia due to central nervous system deficits. Our aim was to determine the effect of nutritive sensory input on the cortical swallowing network. In 14 healthy right-handed volunteers, we utilized a paradigm-driven protocol to quantify the number of activated voxels and their signal intensity within the left hemispheric cortical swallowing network by high-resolution functional MRI (fMRI) during five different swallowing conditions. Swallowing conditions included a dry swallow (saliva) and natural water-, lemon-, popcorn-, and chocolate-flavored liquid swallows. Each flavored liquid was presented simultaneously by its image, scent, and taste in random order and tested over three runs. fMRIs were analyzed in a blinded fashion. Average fMRI blood oxygenation level-dependent signal intensity and number of activated voxels during swallowing concurrent with nutritive gustatory, olfactory, and visual stimulations were significantly increased compared with dry/natural water swallows throughout the cortical swallowing network (P Ͻ 0.001 and P Ͻ 0.05, respectively). Subregion analysis showed the increased activity for flavored liquids in prefrontal, cingulate gyrus, and sensory/motor cortex, but not in precuneus and insula. Concurrent gustatory, olfactory, and visual nutritive stimulation enhances the activity of the cortical swallowing network. This finding may have clinical implications in management of swallowing disorders due to cortical lesions. flavor; deglutition; olfaction; gustation THE MAIN PHYSIOLOGICAL FUNCTION of the digestive tract and ingestion-related behavior in all multicellular life forms in the animal kingdom is to acquire food and water to meet the nutritional needs of the organism (30, 39). Deglutition, the primary ingestive behavior that develops in utero in mammalian species (42), contributes to several critical fetal developmental processes (39). The physical act of swallowing requires extensive sensory/motor coordination of oral, pharyngeal, laryngeal, esophageal, and diaphragmatic muscles (1, 2) that are primarily mediated by the "swallowing center" of the brain stem (19,20). However, a large body of physiological evidence indicates that the cerebral cortex plays a fundamental role, not only in initiation (5, 36), but also in regulation and modulation, of deglutition (18,29,35). Furthermore, clinical observations have long documented the development of swallowing disorders due to cerebrovascular accident (13, 37) or traumatic brain injury (7,12) in the absence of brain stem involvement (9, 14). In humans, recent cortical mapping studies using functional brain imaging (4,10,15,16,24,28,33,45,47) show that volitional swallowing bilaterally activates a number of cerebral cortical areas, including cingulate gyrus, prefrontal an...

Ressonância magnética funcional e deglutição: revisão sistemática

“…Scientific articles were categorized specific features to the swallowing cortical representation (3,(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25) . Research on elderly and patients with dysphagia underwent compared to control groups.…”

“…A chronological analysis of the presented studies, observed that initially the concern was the confirmation of cortical activation mechanisms for swallowing Therefore, procedures such as saliva (1,3,5,7,(16)(17)(18)(19)(20)22,23,26,(29)(30)(31)(32) , water (5,11,12,17,(24)(25)(26)28,29,31) , barium (5,26,29,31) swallowing were performed, comparing swallow and not swallow (1,7,14,27) . Later on, studies began to analyze differences in the cortical areas, responsible for each motor phase, differentiating the role of the structures involved.…”

“…Later on, studies began to analyze differences in the cortical areas, responsible for each motor phase, differentiating the role of the structures involved. To this end, electrical stimulation (24) , swallowing by means of air pulses in the oral cavity (13,31) , gustatory stimulation (12,17,24) , olfactory (9) and stimulation of the esophagus (1,6,15 ) were employed.…”

“…Guidance provided to different groups of surveyed subjects included visual (3,7,8,10,14,(16)(17)(18)(19)(23)(24)(25)(26)(27)(28)(30)(31)(32) , hearing (6,16,21,29) and sensorial clues (5,9,11,13,15,17,19,24,29) . In studies examining the food swallowing, its ingestion was the track for the patient to swallow, i.e., the absence of formal statement was a major factor, differentiating it from studies with other types of tasks.…”

Swallowing Disorders in Clinical Practice: Functional Anatomy, Assessment and Rehabilitation Strategies

“…It may lead to a facilitation of both the oral and the pharyngeal phase of deglutition, producing also increased bihemispheric activation with predominant activation of the left somatosensory cortical areas during the whole swallowing interval (19) The enhancement of neural circuits of swallowing by sensory stimulation have been demonstrated by studies using functional MRI. Babaei and collab (17) tested swallowing after taste stimulation with intense flavors concomitant with presentation of olfactive and visual characters of same aliments, during fMRI scanning.Flavor increases cortical activation in the swallowing neural network: greater intensity and extension of activated cortical areas compared with dry swallowing ave been demonstrated, showing that cortical swallowing network activity can be increased by food-related sensory stimuli .…”