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DOI: 10.1055/s-0029-1202780
© Georg Thieme Verlag KG Stuttgart · New York
Kortikale Repräsentation des Schluckaktes – Neues zur Physiologie und Pathophysiologie des Schluckens
Cortical Representation of Swallowing − New Aspects on the Physiology and Pathophysiology of DeglutitionPublikationsverlauf
Publikationsdatum:
03. September 2009 (online)
Zusammenfassung
Im Gegensatz zur seit vielen Jahren etablierten klinischen Bedeutung der neurogenen Dysphagie ist die Aufklärung der zentralen Koordination des Schluckaktes Gegenstand der aktuellen Forschung. Während sogenannte Schluckzentren des Hirnstammes den unwillkürlichen Schluckreflex steuern, kommt dem zerebralen Kortex eine entscheidende Bedeutung bei der willkürlichen Initiierung des Schluckaktes zu. Der physiologische Schluckakt wird bilateral im sensomotorischen Kortex und in mehreren weiteren kortikalen und subkortikalen Hirnregionen verarbeitet. Klinische Beobachtungen bei Schlaganfallpatienten und neue bildgebende Studien legen eine Hemisphärenspezialisierung für einzelne Phasen des Schluckaktes nahe. Dabei werden eine vorwiegend linkslateralisierte Verarbeitung der oralen Phase und eine rechtshemisphärische Lateralisation der pharyngealen Phase angenommen. Auch für pathologische und iatrogene Veränderungen konnten bereits Anpassungs- und Kompensationsmechanismen nachgewiesen werden. Läsionen des ersten Motoneurons führen zu einer Abnahme der kortikalen schluckakt-assoziierten Aktivität. Bei unilateraler Läsion, wie z. B. beim Schlaganfall, können parallel zur klinischen Erholung Reorganisationsprozesse beobachtet werden. Schädigungen jenseits des ersten Motoneurons, z. B. infolge einer bulbospinalen Muskelatrophie, resultieren typischerweise in einer Vergrößerung der kortikalen Repräsentation des Schluckaktes. Wir nehmen an, dass die bisherigen Resultate zukünftig bei der Entwicklung neuer Therapien und deren Evaluation von großem Wert sein werden.
Abstract
In spite of the long established clinical relevance of neurogenic dysphagia, clarification of the central control of deglutition is the object of ongoing research. While central swallowing pattern generators in the brainstem control the involuntary swallowing reflex, the cerebral cortex plays a decisive role in the voluntary initiation of deglutition. Physiological deglutition is processed bilaterally in the sensorimotor cortex and in several additional cortical and subcortical brain regions. Clinical observations in stroke patients and recent imaging studies suggest hemispheric specialisations for the different phases of deglutition. Predominantly left lateralised processing of the oral phase and right hemispheric lateralisation of the pharyngeal phase are assumed. Adaptation and compensation mechanisms have moreover been shown for pathological and iatrogenic changes. Lesions of the upper motor neuron result in a decrease of swallowing-related cortical activation. In the case of unilateral affection as in stroke, reorganisation processes can be observed parallel to clinical recovery. Lesions beyond the upper motor neuron, e.g., bulbospinal muscle atrophy, typically result in an increase of the cortical representation of swallowing. We assume that the hitherto existing results will be of value for the development of new therapies and their evaluation.
Schlüsselwörter
kortikale Verarbeitung - Schlucken - Dysphagie - funktionelle Bildgebung - MEG
Key words
cortical processing - swallowing - dysphagia - functional imaging - MEG
Literatur
- 1 Amato AA, Prior TW, Barohn RJ. et al . Kennedy's disease: a clinicopathologic correlation with mutations in the androgen receptor gene. Neurology. 1993; 43 791-794
- 2 Aviv JE. Effects of aging on sensitivity of the pharyngeal and supraglottic areas. Am J Med. 1997; 103 S74-S76
- 3 Aviv JE, Martin JH, Sacco RL. et al . Supraglottic and pharyngeal sensory abnormalities in stroke patients with dysphagia. Ann Otol Rhinol Laryngol. 1996; 105 92-97
- 4 Boillee S, Yamanaka K, Lobsiger CS. et al . Onset and progression in inherited ALS determined by motor neurons and microglia. Science. 2006; 312 1389-1392
- 5 Brodmann K. Brodmann's Areas. Localisation in the Cerebral Cortex. 2005;
- 6 Broussard DL, Altschuler SM. Brainstem viscerotopic organization of afferents and efferents involved in the control of swallowing. Am J Med. 2000; 108 ((Suppl 4a)) 79S-86S
- 7 Chee C, Arshad S, Singh S. et al . The influence of chemical gustatory stimuli and oral anaesthesia on healthy human pharyngeal swallowing. Chem Senses. 2005; 30 393-400
- 8 Cook IJ, Dodds WJ, Dantas RO. et al . Opening mechanisms of the human upper esophageal sphincter. Am J Physiol. 1989; 257 G748-59
- 9 Daniels SK. Swallowing apraxia: a disorder of the Praxis system?. Dysphagia. 2000; 15 159-166
- 10 Daniels SK, Corey DM, Fraychinaud A. et al . Swallowing lateralization: the effects of modified dual-task interference. Dysphagia. 2006; 21 21-27
- 11 Daniels SK, Foundas AL, Iglesia GC. et al . Lesion site in unilateral stroke patients with dysphagia. J Stroke Cerebrovas Dis. 1996; 6 30-34
- 12 Derambure P, Defebvre L, Dujardin K. et al . Effect of aging on the spatio-temporal pattern of event-related desynchronization during a voluntary movement. Electroencephalogr Clin Neurophysiol. 1993; 89 197-203
- 13 Ding R, Logemann JA. Pneumonia in stroke patients: a retrospective study. Dysphagia. 2000; 15 51-57
- 14 Dodds WJ, Stewart ET, Logemann JA. Physiology and radiology of the normal oral and pharyngeal phases of swallowing. Am J Roentgenol. 1990; 154 953-963
- 15 Dodds WJ, Taylor AJ, Stewart ET. et al . Tipper and dipper types of oral swallows. Am J Roentgenol. 1989; 153 1197-1199
- 16 Donner MW. Radiologic evaluation of swallowing. Am Rev Respir Dis. 1985; 131 S20-3
- 17 Downar J, Crawley AP, Mikulis DJ. et al . A multimodal cortical network for the detection of changes in the sensory environment. Nat Neurosci. 2000; 3 277-283
- 18 Dziewas R, Soros P, Ishii R. et al . Neuroimaging evidence for cortical involvement in the preparation and in the act of swallowing. Neuroimage. 2003; 20 135-144
- 19 Dziewas R, Soros P, Ishii R. et al . Cortical processing of esophageal sensation is related to the representation of swallowing. Neuroreport. 2005; 16 439-443
- 20 Dziewas R, Teismann IK, Suntrup S. et al . Cortical compensation associated with dysphagia caused by selective degeneration of bulbar motor neurons. Hum Brain Mapp. 2008;
- 21 Ertekin C, Aydogdu I, Yuceyar N. et al . Pathophysiological mechanisms of oropharyngeal dysphagia in amyotrophic lateral sclerosis. Brain. 2000a; 123 ((Pt 1)) 125-140
- 22 Ertekin C, Kiylioglu N, Tarlaci S. et al . Effect of mucosal anaesthesia on oropharyngeal swallowing. Neurogastroenterol Motil. 2000b; 12 567-572
- 23 Foltys H, Krings T, Meister IG. et al . Motor representation in patients rapidly recovering after stroke: a functional magnetic resonance imaging and transcranial magnetic stimulation study. Clin Neurophysiol. 2003; 114 2404-2415
- 24 Fraser C, Power M, Hamdy S. et al . Driving plasticity in human adult motor cortex is associated with improved motor function after brain injury. Neuron. 2002; 34 831-840
- 25 Fraser C, Rothwell J, Power M. et al . Differential changes in human pharyngoesophageal motor excitability induced by swallowing, pharyngeal stimulation, and anesthesia. Am J Physiol Gastrointest Liver Physiol. 2003; 285 G137-44
- 26 Furlong PL, Hobson AR, Aziz Q. et al . Dissociating the spatio-temporal characteristics of cortical neuronal activity associated with human volitional swallowing in the healthy adult brain. Neuroimage. 2004; 22 1447-1455
- 27 Gow D, Hobson AR, Furlong P. et al . Characterising the central mechanisms of sensory modulation in human swallowing motor cortex. Clin Neurophysiol. 2004; 115 2382-2390
- 28 Guidetti D, Sabadini R, Ferlini A. et al . Epidemiological survey of X-linked bulbar and spinal muscular atrophy, or Kennedy disease, in the province of Reggio Emilia, Italy. Eur J Epidemiol. 2001; 17 587-591
- 29 Hamdy S, Aziz Q, Rothwell JC. et al . Explaining oropharyngeal dysphagia after unilateral hemispheric stroke. Lancet. 1997a; 350 686-692
- 30 Hamdy S, Aziz Q, Rothwell JC. et al . Cranial nerve modulation of human cortical swallowing motor pathways. Am J Physiol. 1997b; 272 G802-8
- 31 Hamdy S, Aziz Q, Rothwell JC. et al . Sensorimotor modulation of human cortical swallowing pathways. J Physiol. 1998a; 506 ((Pt 3)) 857-866
- 32 Hamdy S, Aziz Q, Rothwell JC. et al . Recovery of swallowing after dysphagic stroke relates to functional reorganization in the intact motor cortex. Gastroenterology. 1998b; 115 1104-1112
- 33 Hamdy S, Aziz Q, Rothwell JC. et al . The cortical topography of human swallowing musculature in health and disease. Nat Med. 1996; 2 1217-1224
- 34 Hamdy S, Jilani S, Price V. et al . Modulation of human swallowing behaviour by thermal and chemical stimulation in health and after brain injury. Neurogastroenterol Motil. 2003; 15 69-77
- 35 Hamdy S, Mikulis DJ, Crawley A. et al . Cortical activation during human volitional swallowing: an event-related fMRI study. Am J Physiol. 1999a; 277 G219-25
- 36 Hamdy S, Rothwell JC. Gut feelings about recovery after stroke: the organization and reorganization of human swallowing motor cortex. Trends Neurosci. 1998; 21 278-282
- 37 Hamdy S, Rothwell JC, Aziz Q. et al . Long-term reorganization of human motor cortex driven by short-term sensory stimulation. Nat Neurosci. 1998c; 1 64-68
- 38 Hamdy S, Rothwell JC, Brooks DJ. et al . Identification of the cerebral loci processing human swallowing with H2(15)O PET activation. J Neurophysiol. 1999b; 81 1917-1926
- 39 Harris ML, Julyan P, Kulkarni B. et al . Mapping metabolic brain activation during human volitional swallowing: a positron emission tomography study using [18F]fluorodeoxyglucose. J Cereb Blood Flow Metab. 2005; 25 520-526
- 40 Higo R, Tayama N, Nito T. Longitudinal analysis of progression of dysphagia in amyotrophic lateral sclerosis. Auris Nasus Larynx. 2004; 31 247-254
- 41 Hillel A, Dray T, Miller R. et al . Presentation of ALS to the otolaryngologist/head and neck surgeon: getting to the neurologist. Neurology. 1999; 53 S22-S25 , ; discussion S35–36
- 42 Horner J, Massey EW, Riski JE. et al . Aspiration following stroke: clinical correlates and outcome. Neurology. 1988; 38 1359-1362
- 43 Huckabee ML, Deecke L, Cannito MP. et al . Cortical control mechanisms in volitional swallowing: the Bereitschaftspotential. Brain Topogr. 2003; 16 3-17
- 44 Humbert IA, Fitzgerald ME, McLaren DG. et al . Neurophysiology of swallowing: effects of age and bolus type. Neuroimage. 2009; 44 982-991
- 45 Hutchinson S, Kobayashi M, Horkan CM. et al . Age-related differences in movement representation. Neuroimage. 2002; 17 1720-1728
- 46 Huttunen J, Wikstrom H, Salonen O. et al . Human somatosensory cortical activation strengths: comparison between males and females and age-related changes. Brain Res. 1999; 818 196-203
- 47 Jacob P, Kahrilas PJ, Logemann JA. et al . Upper esophageal sphincter opening and modulation during swallowing. Gastroenterology. 1989; 97 1469-1478
- 48 Jean A. Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev. 2001; 81 929-969
- 49 Jean A, Car A, Roman C. Comparison of activity in pontine versus medullary neurones during swallowing. Exp Brain Res. 1975; 22 211-220
- 50 Jokelainen M. Amyotrophic lateral sclerosis in Finland. II: Clinical characteristics. Acta Neurol Scand. 1977; 56 194-204
- 51 Kern MK, Jaradeh S, Arndorfer RC. et al . Cerebral cortical representation of reflexive and volitional swallowing in humans. Am J Physiol Gastrointest Liver Physiol. 2001; 280 G354-60
- 52 Kew JJ, Brooks DJ, Passingham RE. et al . Cortical function in progressive lower motor neuron disorders and amyotrophic lateral sclerosis: a comparative PET study. Neurology. 1994; 44 1101-1110
- 53 Kew JJ, Leigh PN, Playford ED. et al . Cortical function in amyotrophic lateral sclerosis. A positron emission tomography study. Brain. 1993; 116 ((Pt 3)) 655-680
- 54 Kim Y, MacCullough GH, Asp CW. Temporal measurements of pharyngeal swallowing in normal populations. Dysphagia. 2005; 20 290-296
- 55 Konrad C, Henningsen H, Bremer J. et al . Pattern of cortical reorganization in amyotrophic lateral sclerosis: a functional magnetic resonance imaging study. Exp Brain Res. 2002; 143 51-56
- 56 Konrad C, Jansen A, Henningsen H. et al . Subcortical reorganization in amyotrophic lateral sclerosis. Exp Brain Res. 2006; 172 361-369
- 57 Lazzara L, Lazarus C, Logemann J. Effects of thermal stimulation on patients with swallowing disorders - A videofluoroscopic analysis. Dysphagia. 1986; 1
- 58 Leder SB, Novella S, Patwa H. Use of fiberoptic endoscopic evaluation of swallowing (FEES) in patients with amyotrophic lateral sclerosis. Dysphagia. 2004; 19 177-181
- 59 Leelamanit V, Limsakul C, Geater A. Synchronized electrical stimulation in treating pharyngeal dysphagia. Laryngoscope. 2002; 112 2204-2210
- 60 Lehman R, Andermann F, Olivier A. et al . Seizures with onset in the sensorimotor face area: clinical patterns and results of surgical treatment in 20 patients. Epilepsia. 1994; 35 1117-1124
- 61 Logemann J. Evaluation and treatment of swallowing disorders. San Diego CA: C.H. Press 1983
- 62 Logemann JA. The need for clinical trials in dysphagia. Dysphagia. 1998; 13 10-11
- 63 Lowell SY, Poletto CJ, Knorr-Chung BR. et al . Sensory stimulation activates both motor and sensory components of the swallowing system. Neuroimage. 2008; 42 285-295
- 64 Ludlow CL, Humbert I, Saxon K. et al . Effects of surface electrical stimulation both at rest and during swallowing in chronic pharyngeal Dysphagia. Dysphagia. 2007; 22 1-10
- 65 Mann G, Hankey GJ, Cameron D. Swallowing function after stroke: prognosis and prognostic factors at 6 months. Stroke. 1999; 30 744-748
- 66 Mansson I, Sandberg N. Manometry of the pharynx and the esophagus in relation to laryngectomy. JFORL J Fr Otorhinolaryngol Audiophonol Chir Maxillofac. 1974; 23 737-743
- 67 Martin R, Barr A, Macintosh B. et al . Cerebral cortical processing of swallowing in older adults. Exp Brain Res. 2006;
- 68 Martin RE, Goodyear BG, Gati JS. et al . Cerebral cortical representation of automatic and volitional swallowing in humans. J Neurophysiol. 2001; 85 938-950
- 69 Martin RE, MacIntosh BJ, Smith RC. et al . Cerebral areas processing swallowing and tongue movement are overlapping but distinct: a functional magnetic resonance imaging study. J Neurophysiol. 2004; 92 2428-2443
- 70 Martin RE, Sessle BJ. The role of the cerebral cortex in swallowing. Dysphagia. 1993; 8 195-202
- 71 MacDowd JM. Inhibition in attention and aging. J Gerontol B Psychol Sci Soc Sci. 1997; 52 P265-73
- 72 Miller AJ. Significance of sensory inflow to the swallowing reflex. Brain Res. 1972; 43 147-159
- 73 Mosier K, Bereznaya I. Parallel cortical networks for volitional control of swallowing in humans. Exp Brain Res. 2001; 140 280-289
- 74 Mosier K, Liu WC, Behin B. et al . Cortical adaptation following partial glossectomy with primary closure: implications for reconstruction of the oral tongue. Ann Otol Rhinol Laryngol. 2005; 114 681-687
- 75 Mosier K, Patel R, Liu WC. et al . Cortical representation of swallowing in normal adults: functional implications. Laryngoscope. 1999a; 109 1417-1423
- 76 Mosier KM, Liu WC, Maldjian JA. et al . Lateralization of cortical function in swallowing: a functional MR imaging study. Am J Neuroradiol. 1999b; 20 1520-1526
- 77 Narita N, Yamamura K, Yao D. et al . Effects of functional disruption of lateral pericentral cerebral cortex on primate swallowing. Brain Res. 1999; 824 140-145
- 78 Neumann S, Bartolome G, Buchholz D. et al . Swallowing therapy of neurologic patients: correlation of outcome with pretreatment variables and therapeutic methods. Dysphagia. 1995; 10 1-5
- 79 Onozuka M, Fujita M, Watanabe K. et al . Age-related changes in brain regional activity during chewing: a functional magnetic resonance imaging study. J Dent Res. 2003; 82 657-660
- 80 Pommerenke W. A study of the sensory areas eliciting the swallowing reflex. Am J Physiol. 1927; 84 36-41
- 81 Power M, Fraser C, Hobson A. et al . Changes in pharyngeal corticobulbar excitability and swallowing behavior after oral stimulation. Am J Physiol Gastrointest Liver Physiol. 2004; 286 G45-50
- 82 Power ML, Fraser CH, Hobson A. et al . Evaluating oral stimulation as a treatment for dysphagia after stroke. Dysphagia. 2006; 21 49-55
- 83 Robbins J, Levin RL. Swallowing after unilateral stroke of the cerebral cortex: preliminary experience. Dysphagia. 1988; 3 11-17
- 84 Robbins J, Levine RL, Maser A. et al . Swallowing after unilateral stroke of the cerebral cortex. Arch Phys Med Rehabil. 1993; 74 1295-1300
- 85 Rosenbek JC, Robbins J, Fishback B. et al . Effects of thermal application on dysphagia after stroke. J Speech Hear Res. 1991; 34 1257-1268
- 86 Rosenbek JC, Roecker EB, Wood JL. et al . Thermal application reduces the duration of stage transition in dysphagia after stroke. Dysphagia. 1996; 11 225-233
- 87 Satow T, Ikeda A, Yamamoto J. et al . Role of primary sensorimotor cortex and supplementary motor area in volitional swallowing: a movement-related cortical potential study. Am J Physiol Gastrointest Liver Physiol. 2004; 287 G459-70
- 88 Schoenfeld MA, Tempelmann C, Gaul C. et al . Functional motor compensation in amyotrophic lateral sclerosis. J Neurol. 2005; 252 944-952
- 89 Selinger M, Prescott TE, Hoffman I. Temperature acceleration in cold oral stimulation. Dysphagia. 1994; 9 83-87
- 90 Shaw DW, Cook IJ, Gabb M. et al . Influence of normal aging on oral-pharyngeal and upper esophageal sphincter function during swallowing. Am J Physiol. 1995; 268 G389-96
- 91 Soros P, Lalone E, Smith R. et al . Functional MRI of oropharyngeal air-pulse stimulation. Neuroscience. 2008; 153 1300-1308
- 92 Sperfeld AD, Karitzky J, Brummer D. et al . X-linked bulbospinal neuronopathy: Kennedy disease. Arch Neurol. 2002; 59 1921-1926
- 93 Suzuki M, Asada Y, Ito J. et al . Activation of cerebellum and basal ganglia on volitional swallowing detected by functional magnetic resonance imaging. Dysphagia. 2003; 18 71-77
- 94 Teismann IK, Dziewas R, Steinstraeter O. et al . Time-dependent hemispheric shift of the cortical control of volitional swallowing. Hum Brain Mapp. 2007a;
- 95 Teismann IK, Steinstraeter O, Schwindt W. et al . Age-related changes in cortical swallowing processing. Neurobiol Aging. 2008a;
- 96 Teismann IK, Steinstraeter O, Stoeckigt K. et al . Functional oropharyngeal sensory disruption interferes with the cortical control of swallowing. BMC Neurosci. 2007b; 8 62
- 97 Teismann IK, Steinstraeter O, Warnecke T. et al . Cortical processing of swallowing in ALS patients with rapidly progressive neurogenic dysphagia. , submitted
- 98 Teismann IK, Steinstraeter O, Warnecke T. et al . Cortical recovery of swallowing function in wound botulism. BMC Neurol. 2008b; 8 13
- 99 Traversa R, Cicinelli P, Bassi A. et al . Mapping of motor cortical reorganization after stroke. A brain stimulation study with focal magnetic pulses. Stroke. 1997; 28 110-117
- 100 Valeriani M, Ranghi F, Giaquinto S. The effects of aging on selective attention to touch: a reduced inhibitory control in elderly subjects?. Int J Psychophysiol. 2003; 49 75-87
- 101 Van Hoesen GW. The modern concept of association cortex. Curr Opin Neurobiol. 1993; 3 150-154
- 102 Walker AE, Robins M, Weinfeld FD. The National Survey of Stroke. Clinical findings. Stroke. 1981; 12 I13-44
- 103 Yoshikawa M, Yoshida M, Nagasaki T. et al . Aspects of swallowing in healthy dentate elderly persons older than 80 years. J Gerontol A Biol Sci Med Sci. 2005; 60 506-509
- 104 Young EC, Durant-Jones L. Developing a dysphagia program in an acute care hospital: a needs assessment. Dysphagia. 1990; 5 159-165
- 105 Zacks R, Hasher L. Cognitive gerontology and attentional inhibition: a reply to Burke and McDowd. J Gerontol B Psychol Sci Soc Sci. 1997; 52 P274-83
- 106 Zald DH, Pardo JV. The functional neuroanatomy of voluntary swallowing. Ann Neurol. 1999; 46 281-286
Korrespondenzadresse
Dr. med. I. K. Teismann
Klinik und Poliklinik für Neurologie
Universitätsklinikum Münster
Albert-Schweitzer-Straße 33
48149 Münster
eMail: i.teismann@uni-muenster.de