Neural activation of swallowing and swallowing‐related tasks in healthy young adults: An attempt to separate the components of deglutition

Understanding the underlying neural pathways that govern the highly complex neuromuscular action of swallowing is considered crucial in the process of correctly identifying and treating swallowing disorders. The aim of the present investigation was to identify the neural activations of the different components of deglutition in healthy young adults using functional magnetic resonance imaging (fMRI). Ten right‐handed young healthy individuals were scanned in a 3‐Tesla Siemens Allegra MRI scanner. Participants were visually cued for both a “Swallow” task and for component/control tasks (“Prepare to swallow”, “Tap your tongue”, and “Clear your throat”) in a randomized order (event‐related design). Behavioral interleaved gradient (BIG) methodology was used to address movement‐related artifacts. Areas activated during each of the three component tasks enabled a partial differentiation of the neural localization for various components of the swallow. Areas that were more activated during throat clearing than other components included the posterior insula and small portions of the post‐ and pre‐central gyri bilaterally. Tongue tapping showed higher activation in portions of the primary sensorimotor and premotor cortices and the parietal lobules. Planning did not show any areas that were more activated than in the other component tasks. When swallowing was compared with all other tasks, there was significantly more activation in the cerebellum, thalamus, cingulate gyrus, and all areas of the primary sensorimotor cortex bilaterally. Hum Brain Mapp 2009. © 2009 Wiley‐Liss, Inc.

[1]  Ziad S. Saad,et al.  Functional neuroanatomy of human voluntary cough and sniff production , 2007, NeuroImage.

[2]  Vincent L. Gracco,et al.  Imaging speech production using fMRI , 2005, NeuroImage.

[3]  Jun Tanji,et al.  New concepts of the supplementary motor area , 1996, Current Opinion in Neurobiology.

[4]  Arno Villringer,et al.  Visual Feature and Conjunction Searches of Equal Difficulty Engage Only Partially Overlapping Frontoparietal Networks , 2002, NeuroImage.

[5]  Masao Yukie,et al.  Neural connections of auditory association cortex with the posterior cingulate cortex in the monkey , 1995, Neuroscience Research.

[6]  S. Daniels,et al.  Swallowing Apraxia: A Disorder of the Praxis System? , 2000, Dysphagia.

[7]  Arthur J. Miller,et al.  The search for the central swallowing pathway: The quest for clarity , 2005, Dysphagia.

[8]  L. Parnetti,et al.  Dysphagia following Stroke , 2004, European Neurology.

[9]  S K Holland,et al.  Functional Magnetic Resonance Imaging of the Pediatric Swallow: Imaging the Cortex and the Brainstem , 2001, The Laryngoscope.

[10]  Michael P. Cannito,et al.  Cortical Control Mechanisms in Volitional Swallowing: The Bereitschaftspotential , 2004, Brain Topography.

[11]  A Jesmanowicz,et al.  Swallow-related cerebral cortical activity maps are not specific to deglutition. , 2001, American journal of physiology. Gastrointestinal and liver physiology.

[12]  J. Pardo,et al.  Cortical activation induced by intraoral stimulation with water in humans. , 2000, Chemical senses.

[13]  B. Canning Anatomy and neurophysiology of the cough reflex: ACCP evidence-based clinical practice guidelines. , 2006, Chest.

[14]  G. Gerard,et al.  Dysphagia as the sole manifestation of bilateral strokes. , 1990, The American journal of gastroenterology.

[15]  Reza Shaker,et al.  Pressure-flow dynamics of the oral phase of swallowing , 2006, Dysphagia.

[16]  Joachim Hermsdörfer,et al.  The role of the cerebellum for predictive control of grasping , 2008, The Cerebellum.

[17]  M. Hallett,et al.  The functional neuroanatomy of simple and complex sequential finger movements: a PET study. , 1998, Brain : a journal of neurology.

[18]  B. Vogt,et al.  Pain and Stroop interference tasks activate separate processing modules in anterior cingulate cortex , 1998, Experimental Brain Research.

[19]  J G Widdicombe,et al.  Sensory neurophysiology of the cough reflex. , 1996, The Journal of allergy and clinical immunology.

[20]  Julie M. Liss,et al.  Clinical Anatomy & Physiology of the Swallow Mechanism , 2004 .

[21]  M Hallett,et al.  Stimulation over the human supplementary motor area interferes with the organization of future elements in complex motor sequences. , 1997, Brain : a journal of neurology.

[22]  V. Wedeen,et al.  Brain parenchyma motion: measurement with cine echo-planar MR imaging. , 1992, Radiology.

[23]  Dr. Stefan Geyer The Microstructural Border Between the Motor and the Cognitive Domain in the Human Cerebral Cortex , 2004, Advances in Anatomy Embryology and Cell Biology.

[24]  R. Passingham,et al.  Self-initiated versus externally triggered movements. II. The effect of movement predictability on regional cerebral blood flow. , 2000, Brain : a journal of neurology.

[25]  C. Lazarus Tongue strength and exercise in healthy individuals and in head and neck cancer patients. , 2006, Seminars in speech and language.

[26]  Thalamus: Organization and Function (Vol. 1), Experimental and Clinical Aspects (Vol. 2) , 1998, Trends in Neurosciences.

[27]  A. Crawley,et al.  Cortical activation during human volitional swallowing: an event-related fMRI study. , 1999, American journal of physiology. Gastrointestinal and liver physiology.

[28]  Maria Beatriz Duarte Gavião,et al.  MASTICATION AND SWALLOWING: INFLUENCE OF FLUID ADDITION TO FOODS , 2007, Journal of applied oral science : revista FOB.

[29]  M. Hallett,et al.  Cerebral structures participating in motor preparation in humans: a positron emission tomography study. , 1996, Journal of neurophysiology.

[30]  C. Ludlow,et al.  Laryngeal activity during upright vs. supine swallowing. , 2002, Journal of applied physiology.

[31]  J. Rothwell,et al.  Explaining oropharyngeal dysphagia after unilateral hemispheric stroke , 1997, The Lancet.

[32]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

[33]  J. Widdicombe,et al.  Cough: what's in a name? , 2006, European Respiratory Journal.

[34]  R E Stephens,et al.  Assessing the laryngeal cough reflex and the risk of developing pneumonia after stroke. , 1999, Archives of physical medicine and rehabilitation.

[35]  E. Tan,et al.  Severe bruxism following basal ganglia infarcts: insights into pathophysiology , 2004, Journal of the Neurological Sciences.

[36]  P. Kahrilas,et al.  Deglutitive tongue action: volume accommodation and bolus propulsion. , 1993, Gastroenterology.

[37]  K. Zilles,et al.  Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex 2. Spatial Normalization to Standard Anatomical Space , 2000, NeuroImage.

[38]  A. Jean Brain stem control of swallowing: neuronal network and cellular mechanisms. , 2001, Physiological reviews.

[39]  Yul-Wan Sung,et al.  Functional magnetic resonance imaging , 2004, Scholarpedia.

[40]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[41]  Naoki Miura,et al.  The human parietal cortex is involved in spatial processing of tongue movement—an fMRI study , 2004, NeuroImage.

[42]  S. Kinomura,et al.  PET study of pointing with visual feedback of moving hands. , 1998, Journal of neurophysiology.

[43]  Ravi S. Menon,et al.  Cerebral areas processing swallowing and tongue movement are overlapping but distinct: a functional magnetic resonance imaging study. , 2004, Journal of neurophysiology.

[44]  J. Pardo,et al.  The functional neuroanatomy of voluntary swallowing , 1999, Annals of neurology.

[45]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[46]  J. R. Augustine Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

[47]  C. Dalton,et al.  Pharyngeal and upper esophageal sphincter manometry in humans. , 1990, The American journal of physiology.

[48]  J. Dent,et al.  Influence of gravity and body position on normal oropharyngeal swallowing. , 1995, The American journal of physiology.

[49]  R Turner,et al.  Cortical and subcortical control of tongue movement in humans: a functional neuroimaging study using fMRI. , 1999, Journal of applied physiology.

[50]  L. Gray,et al.  Aspiration after stroke: Lesion analysis by brain MRI , 1992, Dysphagia.

[51]  K. Doya,et al.  Parallel neural networks for learning sequential procedures , 1999, Trends in Neurosciences.

[52]  Significance of gravity on the passage of bolus through the human pharynx. , 1973, Archives of oral biology.

[53]  A. Miller,et al.  Precentral Cortical Modulation of Mastication and Swallowing , 1977, Journal of dental research.

[54]  E T Stewart,et al.  Physiology and radiology of the normal oral and pharyngeal phases of swallowing. , 1990, AJR. American journal of roentgenology.

[55]  D.D.S. Andrew Blitzer M.D. Approaches to the patient with aspiration and swallowing disabilities , 2006, Dysphagia.

[56]  J C Rothwell,et al.  Identification of the cerebral loci processing human swallowing with H2(15)O PET activation. , 1999, Journal of neurophysiology.

[57]  K. Mosier,et al.  Parallel cortical networks for volitional control of swallowing in humans , 2001, Experimental Brain Research.

[58]  J Tanji,et al.  Comparison of neuronal activity in the supplementary motor area and primary motor cortex. , 1996, Brain research. Cognitive brain research.

[59]  Dysphagia with Bilateral Lesions of the Insular Cortex , 2003, Dysphagia.

[60]  John C. Rothwell,et al.  The cortical topography of human swallowing musculature in health and disease , 1996, Nature Medicine.

[61]  J. Stierwalt,et al.  Measures of Tongue Function Related to Normal Swallowing , 2006, Dysphagia.

[62]  B. Sessle,et al.  Input-output relationships of the primary face motor cortex in the monkey (Macaca fascicularis). , 1989, Journal of neurophysiology.

[63]  A. Foundas,et al.  The Role of the Insular Cortex in Dysphagia , 1997, Dysphagia.

[64]  N. Dronkers A new brain region for coordinating speech articulation , 1996, Nature.

[65]  P. Sörös,et al.  Functional MRI of oropharyngeal air-pulse stimulation , 2008, Neuroscience.

[66]  M. Mandelli,et al.  Epidemiology and risk factors of pneumonia in critically ill patients , 1991, European Journal of Epidemiology.

[67]  Stephen M. Smith,et al.  General multilevel linear modeling for group analysis in FMRI , 2003, NeuroImage.

[68]  R Shaker,et al.  Cerebral cortical representation of reflexive and volitional swallowing in humans. , 2001, American journal of physiology. Gastrointestinal and liver physiology.

[69]  K. Zilles,et al.  Human Somatosensory Area 2: Observer-Independent Cytoarchitectonic Mapping, Interindividual Variability, and Population Map , 2001, NeuroImage.

[70]  Stefan Geyer,et al.  Prologue: Toward the Concept of a Cortical Control of Voluntary Movements , 2004 .

[71]  Deborah L. Harrington,et al.  From preparation to online control: Reappraisal of neural circuitry mediating internally generated and externally guided actions , 2006, NeuroImage.

[72]  A M Dale,et al.  Optimal experimental design for event‐related fMRI , 1999, Human brain mapping.

[73]  A. Schleicher,et al.  Two different areas within the primary motor cortex of man , 1996, Nature.

[74]  T. Ono,et al.  Coordination of Tongue Pressure and Jaw Movement in Mastication , 2006, Journal of dental research.

[75]  G. M. Murray,et al.  Features of cortically evoked swallowing in the awake primate (Macaca fascicularis). , 1999, Journal of neurophysiology.

[76]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[77]  Y Miyaoka,et al.  Influences of body posture on duration of oral swallowing in normal young adults. , 2007, Journal of oral rehabilitation.

[78]  R E Stephens,et al.  Assessing the laryngeal cough reflex and the risk of developing pneumonia after stroke: an interhospital comparison. , 1999, Stroke.

[79]  Richard C. Reynolds,et al.  Sensory stimulation activates both motor and sensory components of the swallowing system , 2008, NeuroImage.

[80]  J. Widdicombe,et al.  Supramedullary influences on cough , 2006, Respiratory Physiology & Neurobiology.

[81]  Ravi S. Menon,et al.  Cerebral cortical representation of automatic and volitional swallowing in humans. , 2001, Journal of neurophysiology.

[82]  Joseph S. Gati,et al.  Discrete functional contributions of cerebral cortical foci in voluntary swallowing: a functional magnetic resonance imaging (fMRI) “Go, No-Go” study , 2005, Experimental Brain Research.

[83]  A. Schleicher,et al.  Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex 1. Microstructural Organization and Interindividual Variability , 1999, NeuroImage.

[84]  Ravi S. Menon,et al.  Cerebral cortical processing of swallowing in older adults , 2006, Experimental Brain Research.

[85]  J. Logemann,et al.  Evaluation and treatment of swallowing disorders , 1983 .

[86]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[87]  P. Roland,et al.  Supplementary motor area and other cortical areas in organization of voluntary movements in man. , 1980, Journal of neurophysiology.

[88]  J A Maldjian,et al.  Lateralization of cortical function in swallowing: a functional MR imaging study. , 1999, AJNR. American journal of neuroradiology.

[89]  J. Rothwell,et al.  Sensorimotor modulation of human cortical swallowing pathways , 1998, The Journal of physiology.

[90]  J. Kellow Mastication and Swallowing , 1996 .

[91]  W T Thach,et al.  The cerebellum and the adaptive coordination of movement. , 1992, Annual review of neuroscience.

[92]  J. Robbins,et al.  Swallowing after unilateral stroke of the cerebral cortex: Preliminary experience , 2006, Dysphagia.

[93]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[94]  L. Shah,et al.  Functional magnetic resonance imaging. , 2010, Seminars in roentgenology.

[95]  Kouji Hayashi,et al.  Activation of Cerebellum and Basal Ganglia on Volitional Swallowing Detected by Functional Magnetic Resonance Imaging , 2003, Dysphagia.

[96]  M. L. Wood,et al.  Functional MRI of pain- and attention-related activations in the human cingulate cortex. , 1997, Journal of neurophysiology.

[97]  Scott T. Grafton,et al.  Functional Anatomy of Nonvisual Feedback Loops during Reaching: A Positron Emission Tomography Study , 2001, The Journal of Neuroscience.

[98]  B. Larsen,et al.  Activation of the supplementary motor area during voluntary movement in man suggests it works as a supramotor area. , 1979, Science.

[99]  M E Raichle,et al.  Memory mechanisms in the processing of words and word-like symbols. , 1991, Ciba Foundation symposium.

[100]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[101]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[102]  M. Mandelli,et al.  Epidemiology and risk factors of pneumonia in critically ill patients. Intensive Care Unit Group for Infection Control. , 1991, European journal of epidemiology.

[103]  I. Aydogdu,et al.  Neurophysiology of swallowing , 2003, Clinical Neurophysiology.

[104]  Arthur J. Miller,et al.  Neurophysiological basis of swallowing , 1986, Dysphagia.