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Supportive effect of interferential current stimulation on susceptibility of swallowing in guinea pigs

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Abstract

Sensory-motor control of the pharyngeal swallow requires sensory afferent inputs from the pharynx and larynx evoked by introducing bolus into the pharynx. Patients with reduced sensitivity of the pharynx and larynx are likely to have a swallowing impairment, such as pre-swallow aspiration due to delayed swallow triggering. Interferential current stimulation applied to the neck is thought to improve the swallowing function of dysphagic patients, although the mechanism underlying the facilitatory effect of such stimulation remains unknown. In the present study, we examined the changes in the elicitability of swallowing due to the stimulation and the responses of the swallowing-related neurons in the nucleus tractus solitarius and in the area adjacent to the stimulation in decerebrate and paralyzed guinea pigs. The swallowing delay time was shortened by the stimulation, whereas the facilitatory effect of eliciting swallowing was attenuated by kainic acid injection into the nucleus tractus solitarius. Approximately half of the swallowing-related neurons responded to the stimulation. These data suggest that the interferential current stimulation applied to the neck could enhance the sensory afferent pathway of the pharynx and larynx, subserving excitatory inputs to the neurons of the swallowing pattern generator, thereby facilitating the swallowing reflex.

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References

  • Altschuler SM (2001) Laryngeal and respiratory protective reflexes. Am J Med 111(Suppl):90S–94S

    Article  PubMed  Google Scholar 

  • Altschuler SM, Bao X, Bieger D et al (1989) Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol 283:248–268

    Article  CAS  PubMed  Google Scholar 

  • Aviv JE (1997) Effects of aging on sensitivity of the pharyngeal and supraglottic areas. Am J Med 103:74S–76S

    Article  CAS  PubMed  Google Scholar 

  • Bautista TG, Dutschmann M (2014) Ponto-medullary nuclei involved in the generation of sequential pharyngeal swallowing and concomitant protective laryngeal adduction in situ. J Physiol 592:2605–2623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bautista TG, Fong AY, Dutschmann M (2014) Spontaneous swallowing occurs during autoresuscitation in the in situ brainstem preparation of rat. Respir Physiol Neurobiol 202:35–43

    Article  PubMed  Google Scholar 

  • Berkley KJ, Scofield SL (1990) Relays from the spinal cord and solitary nucleus through the parabrachial nucleus to the forebrain in the cat. Brain Res 529:333–338

    Article  CAS  PubMed  Google Scholar 

  • Bolser D (1991) Fictive cough in the cat. J Appl Physiol 71:2325–2331

    Article  CAS  PubMed  Google Scholar 

  • Bülow M, Speyer R, Baijens L et al (2008) Neuromuscular electrical stimulation (NMES) in stroke patients with oral and pharyngeal dysfunction. Dysphagia 23:302–309

    Article  PubMed  Google Scholar 

  • Coyle JT, Molliver ME, Kuhar MJ (1978) In situ injection of kainic acid: a new method for selectively lesioning neuronal cell bodies while sparing axons of passage. J Comp Neurol 180:301–323

    Article  CAS  PubMed  Google Scholar 

  • de Lama Lazzara G, Lazarus C, Logemann JA (1986) Impact of thermal stimulation on the triggering of the swallowing reflex. Dysphagia 1:73–77

    Article  Google Scholar 

  • Dutschmann M, Dick TE (2012) Pontine mechanisms of respiratory control. Compr Physiol 2:2443–2469

    PubMed  PubMed Central  Google Scholar 

  • El Solh AA, Saliba R (2007) Pharmacologic prevention of aspiration pneumonia: a systematic review. Am J Geriatr Pharmacother 5:352–362

    Article  CAS  PubMed  Google Scholar 

  • Ertekin C (2011) Voluntary versus spontaneous swallowing in man. Dysphagia 26:183–192

    Article  PubMed  Google Scholar 

  • Freed ML, Freed L, Chatburn RL, Christian M (2001) Electrical stimulation for swallowing disorders caused by stroke. Respir Care 46:466–474

    CAS  PubMed  Google Scholar 

  • Fulwiler CE, Saper CB (1984) Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res Rev 7:229–259

    Article  Google Scholar 

  • Furuta T, Takemura M, Tsujita J, Oku Y (2011) Interferential electric stimulation applied to the neck increases swallowing frequency. Dysphagia 27:94–100

    Article  PubMed  Google Scholar 

  • Herbert H, Moga MM, Saper CB (1990) Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J Comp Neurol 293:540–580

    Article  CAS  PubMed  Google Scholar 

  • Jean A (1984) Control of the central swallowing program by inputs from the peripheral receptors. A review. J Auton Nerv Syst 10:225–233

    Article  CAS  PubMed  Google Scholar 

  • Jean A (2001) Brain stem control of swallowing: neuronal network and cellular mechanisms. Physiol Rev 81:929–969

    Article  CAS  PubMed  Google Scholar 

  • Jean A, Car A (1979) Inputs to the swallowing medullary neurons from the peripheral afferent fibers and the swallowing cortical area. Brain Res 178:567–572

    Article  CAS  PubMed  Google Scholar 

  • Jia YX, Sekizawa K, Ohrui T et al (1998) Dopamine D1 receptor antagonist inhibits swallowing reflex in guinea pigs. Am J Physiol 274:R76–R80

    CAS  PubMed  Google Scholar 

  • Kahrilas PJ, Lin S, Rademaker AW, Logemann JA (1997) Impaired deglutitive airway protection: a videofluoroscopic analysis of severity and mechanism. Gastroenterology 113:1457–1464

    Article  CAS  PubMed  Google Scholar 

  • Kessler JP, Jean A (1985) Identification of the medullary swallowing regions in the rat. Exp Brain Res 57:256–263

    Article  CAS  PubMed  Google Scholar 

  • King GW (1980) Topology of ascending brainstem projections to nucleus parabrachialis in the cat. J Comp Neurol 191:615–638

    Article  CAS  PubMed  Google Scholar 

  • Koga K, Furue H, Rashid MH et al (2005) Selective activation of primary afferent fibers evaluated by sine-wave electrical stimulation. Mol Pain 1:1744-8069-1–1744-8069-13

    Article  CAS  Google Scholar 

  • Krukoff TL, Harris KH, Jhamandas JH (1993) Efferent projections from the parabrachial nucleus demonstrated with the anterograde tracer Phaseolus vulgaris leucoagglutinin. Brain Res Bull 30:163–172

    Article  CAS  PubMed  Google Scholar 

  • Lawson EE, Richter DW, Czyzyk-Krzeska MF et al (1991) Respiratory neuronal activity during apnea and other breathing patterns induced by laryngeal stimulation. J Appl Physiol 70:2742–2749

    Article  CAS  PubMed  Google Scholar 

  • Leelamanit V, Limsakul C, Geater A (2002) Synchronized electrical stimulation in treating pharyngeal dysphagia. Laryngoscope 112:2204–2210

    Article  PubMed  Google Scholar 

  • Ludlow CL, Humbert I, Saxon K et al (2007) Effects of surface electrical stimulation both at rest and during swallowing in chronic pharyngeal dysphagia. Dysphagia 22:1–10

    Article  PubMed  PubMed Central  Google Scholar 

  • Macht M, Wimbish T, Bodine C, Moss M (2013) ICU-acquired swallowing disorders. Crit Care Med 41:2396–2405

    Article  PubMed  Google Scholar 

  • Miller AJ (2002) Oral and pharyngeal reflexes in the mammalian nervous system: their diverse range in complexity and the pivotal role of the tongue. Crit Rev Oral Biol Med 13:409–425

    Article  CAS  PubMed  Google Scholar 

  • Miller AJ, Loizzi RF (1974) Anatomical and functional differentiation of superior laryngeal nerve fibers affecting swallowing and respiration. Exp Neurol 42:369–387

    Article  CAS  PubMed  Google Scholar 

  • Miyaji H, Umezaki T, Adachi K et al (2012) Videofluoroscopic assessment of pharyngeal stage delay reflects pathophysiology after brain infarction. Laryngoscope 122:2793–2799

    Article  PubMed  Google Scholar 

  • Nativ-Zeltzer N, Logemann J, Kahrilas PJ (2014) Comparison of timing abnormalities leading to penetration versus aspiration during the oropharyngeal swallow. Laryngoscope 124:935–941

    Article  Google Scholar 

  • Olney JW, Rhee V, Ho OL (1974) Kainic acid: a powerful neurotoxic analogue of glutamate. Brain Res 77:507–512

    Article  CAS  PubMed  Google Scholar 

  • Ootani S, Umezaki T, Shin T, Murata Y (1995) Convergence of afferents from the SLN and GPN in cat medullary swallowing neurons. Brain Res Bull 37:397–404

    Article  CAS  PubMed  Google Scholar 

  • Palmer ST, Martin DJ, Steedman WM, Ravey J (1999) Alteration of interferential current and transcutaneous electrical nerve stimulation frequency: effects on nerve excitation. Arch Phys Med Rehabil 80:1065–1071

    Article  CAS  PubMed  Google Scholar 

  • Poorjavad M, Talebian Moghadam S, Nakhostin Ansari N et al (2014) Surface electrical stimulation for treating swallowing disorders after stroke: a review of the stimulation intensity levels and the electrode placements. Stroke Res Treat 2014:5–7

    Google Scholar 

  • Popovic DB, Popovic MB, Sinkjaer T (2002) Neurorehabilitation of upper extremities in humans with sensory-motor impairment. Neuromodulation Technol Neural Interface 5:54–66

    Article  Google Scholar 

  • Remmers JE, Richter DW, Ballantyne D et al (1986) Reflex prolongation of stage I of expiration. Pflügers Arch Eur J Physiol 407:190–198

    Article  CAS  Google Scholar 

  • Richter DW, Ballantyne D, Remmers JE (1987) The differential organization of medullary post-inspiratory activities. Pflügers Arch Eur J Physiol 410:420–427

    Article  CAS  Google Scholar 

  • Rosenbek JC, Roecker EB, Wood JL, Robbins J (1996) Thermal application reduces the duration of stage transition in dysphagia after stroke. Dysphagia 11:225–233

    Article  CAS  PubMed  Google Scholar 

  • Sacco RL, Diamond B, Aviv JE et al (1997) Silent laryngopharyngeal sensory deficits after stroke. Ann Otol Rhinol Laryngol 106:87–93

    Article  PubMed  Google Scholar 

  • Schwarcz R, Scholz D, Coyle J (1978) Structure-activity relations for the neurotoxicity of kainic acid derivatives and glutamate analogues. Neuropharmacology 17:145–151

    Article  CAS  PubMed  Google Scholar 

  • Sessle BJ (1973) Excitatory and inhibitory inputs to single neurones in the solitary tract nucleus and adjacent reticular formation. Brain Res 53:319–331

    Article  CAS  PubMed  Google Scholar 

  • Shannon R, Baekey DMM, Morris KFF, Lindsey BGG (1996) Brainstem respiratory networks and cough. Pulm Pharmacol 9:343–347

    Article  CAS  PubMed  Google Scholar 

  • Sugishita S, Imai T, Matsui T et al (2015) Effects of short term interferential current stimulation on swallowing reflex in dysphagic patients. Int J Speech Lang Pathol Audiol 3:1–8

    Article  Google Scholar 

  • Sugiyama Y, Shiba K, Nakazawa K et al (2011a) Axonal projections of medullary swallowing neurons in guinea pigs. J Comp Neurol 519:2193–2211

    Article  PubMed  Google Scholar 

  • Sugiyama Y, Suzuki T, DeStefino VJ, Yates BJ (2011b) Integrative responses of neurons in nucleus tractus solitarius to visceral afferent stimulation and vestibular stimulation in vertical planes. Am J Physiol Regul Integr Comp Physiol 301:R1380–R1390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugiyama Y, Shiba K, Mukudai S et al (2014) Activity of respiratory neurons in the rostral medulla during vocalization, swallowing, and coughing in guinea pigs. Neurosci Res 80:17–31

    Article  PubMed  Google Scholar 

  • Suzuki T, Sugiyama Y, Yates BJ (2012) Integrative responses of neurons in parabrachial nuclei to a nauseogenic gastrointestinal stimulus and vestibular stimulation in vertical planes. Am J Physiol Regul Integr Comp Physiol 302:R965–R975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takeuchi Y, McLean JH, Hopkins D (1982) Reciprocal connections between the amygdala and parabrachial nuclei: ultrastructural demonstration by degeneration and axonal transport of horseradish peroxidase in the cat. Brain Res 239:583–588

    Article  CAS  PubMed  Google Scholar 

  • Umezaki T, Zheng Y, Shiba K, Miller AD (1997) Role of nucleus retroambigualis in respiratory reflexes evoked by superior laryngeal and vestibular nerve afferents and in emesis. Brain Res 769:347–356

    Article  CAS  PubMed  Google Scholar 

  • Umezaki T, Matsuse T, Shin T (1998a) Medullary swallowing-related neurons in the anesthetized cat. Neuroreport 9:1793–1798

    Article  CAS  PubMed  Google Scholar 

  • Umezaki T, Shiba K, Zheng Y, Miller AD (1998b) Upper airway motor outputs during vomiting versus swallowing in the decerebrate cat. Brain Res 781:25–36

    Article  CAS  PubMed  Google Scholar 

  • Ward AR (2009) Electrical stimulation using kilohertz-frequency alternating current. Phys Ther 89:181–190

    Article  PubMed  Google Scholar 

  • Ward AR, Robertson VJ (1998) Sensory, motor, and pain thresholds for stimulation with medium frequency alternating current. Arch Phys Med Rehabil 79:273–278

    Article  CAS  PubMed  Google Scholar 

  • Williams JB, Murphy DM, Reynolds KE et al (1996) Demonstration of a bilateral projection from the rostral nucleus of the solitary tract to the medial parabrachial nucleus in rat. Brain Res 737:231–237

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Yoshitaka Oku for comments on an earlier version of the manuscript. Yoichiro Sugiyama equally contributed as the first author to this manuscript. This work was supported by Grant-in-Aid for Young Scientists (B) Grant number 15K20220.

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  1. Toshiro Umezaki and Yoichiro Sugiyama are equally contributing first authors.

Authors and Affiliations

  1. Department of Speech and Hearing Sciences, International University of Health and Welfare, and the Voice and Swallowing Center, Fukuoka Sanno Hospital, Fukuoka, 814-0001, Japan

    Toshiro Umezaki

  2. Department of Otolaryngology-Head and Neck Surgery, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, Kyoto, Kyoto, 602-8566, Japan

    Yoichiro Sugiyama, Shinya Fuse, Shigeyuki Mukudai & Shigeru Hirano

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  1. Toshiro Umezaki
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  2. Yoichiro Sugiyama
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  4. Shigeyuki Mukudai
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  5. Shigeru Hirano
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Correspondence to Yoichiro Sugiyama.

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Umezaki, T., Sugiyama, Y., Fuse, S. et al. Supportive effect of interferential current stimulation on susceptibility of swallowing in guinea pigs. Exp Brain Res 236, 2661–2676 (2018). https://doi.org/10.1007/s00221-018-5325-0

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  • DOI: https://doi.org/10.1007/s00221-018-5325-0

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