Reduced somatosensory activations in swallowing with age

Understanding the neural functional organization of swallowing in healthy elders is essential in diagnosing and treating older adults with swallowing difficulties. The primary aims of this investigation were to identify the neural activation sites of different components of deglutition in healthy elders using functional Magnetic Resonance Imaging (fMRI) and to investigate age differences in the neural control of swallowing. Ten young (age range 19–25 years of age) and nine older (age range 66–77 years of age) right‐handed healthy individuals were scanned in a 3‐Tesla MRI scanner. Subjects were visually cued for both a “Swallow” task and for component/control tasks (“Prepare to swallow,” “Tap your tongue,” and “Clear your throat”). Behavioral interleaved gradient (BIG) methodology was used to address movement related artifacts. Between‐group comparisons revealed statistically stronger activations in the primary somatosensory cortex of young adults during the motor tasks examined. Both groups showed activations in the major motor areas involved in the initiation and execution of movement; however, areas involved in sensory processing, sensorimotor integration and/or motor coordination and control, showed reduced or limited activity in the elderly. Potential implications of these findings for clinical practice are discussed. Hum Brain Mapp, 2011. © 2010 Wiley‐Liss, Inc.

[1]  Bradley P Sutton,et al.  Neural activation of swallowing and swallowing‐related tasks in healthy young adults: An attempt to separate the components of deglutition , 2009, Human brain mapping.

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

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

[4]  P. Linden,et al.  Dysphagia: predicting laryngeal penetration. , 1983, Archives of physical medicine and rehabilitation.

[5]  Hiroshi Uematsu,et al.  Influences of aging on taste perception and oral somatic sensation. , 2005, The journals of gerontology. Series A, Biological sciences and medical sciences.

[6]  J. Weiss,et al.  Senescent swallowing: impact, strategies, and interventions. , 2009, Nutrition in clinical practice : official publication of the American Society for Parenteral and Enteral Nutrition.

[7]  H. Chauncey,et al.  Aging and Mastication: Changes in Performance and in the Swallowing Threshold with Natural Dentition † , 1980, Journal of the American Geriatrics Society.

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

[9]  L. Weisberg,et al.  Aspiration in patients with acute stroke. , 1998, Archives of physical medicine and rehabilitation.

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

[11]  Sterling C. Johnson,et al.  Neurophysiology of swallowing: Effects of age and bolus type , 2009, NeuroImage.

[12]  R. Yemm,et al.  Changes in human masseter and medial pterygoid muscles with age: a study by computed tomography. , 1987, Gerodontics.

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

[14]  P. A. Price,et al.  FORCE AND MOBILITY IN THE AGEING HUMAN TONGUE , 1981, The Medical journal of Australia.

[15]  Raquel E Gur,et al.  Brain region and sex differences in age association with brain volume: a quantitative MRI study of healthy young adults. , 2002, The American journal of geriatric psychiatry : official journal of the American Association for Geriatric Psychiatry.

[16]  J. Aviv Effects of aging on sensitivity of the pharyngeal and supraglottic areas. , 1997, The American journal of medicine.

[17]  J. Robbins,et al.  Age effects on the temporal evolution of isometric and swallowing pressure. , 2000, The journals of gerontology. Series A, Biological sciences and medical sciences.

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

[19]  G. Ford,et al.  Swallow respiratory patterns and aging: presbyphagia or dysphagia? , 2005, The journals of gerontology. Series A, Biological sciences and medical sciences.

[20]  I. Cook,et al.  Influence of aging on oral-pharyngeal bolus transit and clearance during swallowing: scintigraphic study. , 1994, The American journal of physiology.

[21]  K. Amunts,et al.  Brodmann's Areas 17 and 18 Brought into Stereotaxic Space—Where and How Variable? , 2000, NeuroImage.

[22]  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.

[23]  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.

[24]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

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

[26]  E. Massey,et al.  Aspiration in bilateral stroke patients , 1990, Neurology.

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

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

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

[30]  G. Lof,et al.  Oropharyngeal swallowing in normal adults of different ages. , 1992, Gastroenterology.

[31]  Denise C. Park,et al.  Aging reduces neural specialization in ventral visual cortex. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Jay Rosenbek,et al.  Differentiation of Normal and Abnormal Airway Protection during Swallowing Using the Penetration–Aspiration Scale , 1999, Dysphagia.

[33]  J. Minton,et al.  Age‐related changes in oral sensation , 1992, The Laryngoscope.

[34]  B. Sutton,et al.  Age-Related Differences in Laterality of Cortical Activations in Swallowing , 2010, Dysphagia.

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

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

[37]  JoAnne Robbins,et al.  The Effects of Lingual Exercise on Swallowing in Older Adults , 2005, Journal of the American Geriatrics Society.

[38]  E. Luschei,et al.  Age effects on lingual pressure generation as a risk factor for dysphagia. , 1995, The journals of gerontology. Series A, Biological sciences and medical sciences.

[39]  Michael Alexander,et al.  Age-Related Differences in Movement Representation , 2002, NeuroImage.

[40]  J. Callicott,et al.  Neurophysiological correlates of age-related changes in human motor function , 2002, Neurology.

[41]  J. Rosenbek,et al.  Thermal application reduces the duration of stage transition in dysphagia after stroke , 2004, Dysphagia.

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

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

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

[45]  J. Faulkner,et al.  Muscle atrophy and weakness with aging: contraction-induced injury as an underlying mechanism. , 1995, The journals of gerontology. Series A, Biological sciences and medical sciences.

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

[47]  J. Rosenbek,et al.  Mechanism of sequential swallowing during straw drinking in healthy young and older adults. , 2004, Journal of speech, language, and hearing research : JSLHR.

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

[49]  A. Soulas,et al.  [Deglutition and its disorders]. , 1956, Les Annales d'oto-laryngologie.

[50]  Mark Speechley,et al.  Dysphagia After Stroke: Incidence, Diagnosis, and Pulmonary Complications , 2005, Stroke.

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

[52]  Faith M. Gunning-Dixon,et al.  Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume , 2004, Neurobiology of Aging.

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

[54]  J. Holloszy,et al.  What insights into age-related changes in skeletal muscle are provided by animal models? , 1995, The journals of gerontology. Series A, Biological sciences and medical sciences.

[55]  A. Rademaker,et al.  Temporal and biomechanical characteristics of oropharyngeal swallow in younger and older men. , 2000, Journal of speech, language, and hearing research : JSLHR.

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

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

[58]  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.

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

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