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Dopaminergic influence on rat tongue function and limb movement initiation

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Abstract

Altering dopamine synaptic transmission can affect both cranial and limb sensorimotor function, but often to a different degree of severity. We hypothesized that haloperidol has dose-dependent but differential effects on lingual forces, lingual movement rates, and limb movement initiation. We measured average and maximal lingual force, tongue press rate and cataleptic descent time in nine Fischer 344/Brown Norway rats in varied doses of haloperidol. Decreases in lingual force and temporal parameters and increases in cataleptic descent time were related to haloperidol dose. However, they were related to a different degree as the relationships were strong between average force and tongue press rate, moderate between maximal force and tongue press rate, moderate between average force and cataleptic descent time, and weak between maximal force and cataleptic descent time. Elucidating the relationships between the cranial and limb sensorimotor systems in the context of altered dopamine synaptic transmission may assist in developing therapies for conditions such as Parkinson’s disease.

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References

  • Allred RP, Adkins DL, Woodlee MT et al (2008) The Vermicelli handling test: a simple quantitative measure of dexterous forepaw function in rats. J Neurosci Methods 170:229–244

    Article  PubMed  Google Scholar 

  • Alvarez-Cervera FJ, Villaneuva-Toledo J, Moo-Puc RE et al (2005) A novel automated rat catalepsy bar test system based on a RISC microcontroller. J Neurosci Methods 146:76–83

    Article  PubMed  Google Scholar 

  • Amtage J, Schmidt WJ (2003) Context-dependent catalepsy intensification is due to classical conditioning and sensitization. Behav Pharmacol 12(2):143–149

    Google Scholar 

  • Bashford G, Bradd P (1996) Drug-induced Parkinsonism associated with dysphagia and aspiration: a brief report. Geriatr Psychiatry Neurol 9:133–135

    CAS  Google Scholar 

  • Bergman H, Deuschl G (2002) Pathophysiology of Parkinson’s disease: from clinical neurology to basic neuroscience and back. Mov Disord 17(suppl 3):S28–S40

    Article  PubMed  Google Scholar 

  • Bird MR, Woodward MC, Gibson EM et al (1994) Asymptomatic swallowing disorders in elderly patients with Parkinson’s disease: a description of findings on clinical examination and videofluoroscopy in sixteen patients. Age Ageing 23:251–254

    Article  PubMed  CAS  Google Scholar 

  • Braak H, Ghebremedhin E, Rub U et al (2004) Stages in the development of Parkinson’s disease-related pathology. Cell Tissue Res 318:121–134

    Article  PubMed  Google Scholar 

  • Cheon SM, Ha MS, Park MJ et al (2008) Nonmotor symptoms of Parkinson’s disease: prevalence and awareness of patients and families. Parkinsonism Relat Disord 14:286–290

    Article  PubMed  Google Scholar 

  • Ciucci MR, Barkmeier-Kraemer JM, Sherman SJ (2008) Subthalamic stimulation improves deglutition in Parkinson’s disease. Mov Disord 23:676–683

    Article  PubMed  Google Scholar 

  • Connor NP, Abbs JH, Cole KJ et al (1989) Parkinsonian deficits in serial multiarticulate movements for speech. Brain 112:997–1009

    Article  PubMed  Google Scholar 

  • Connor NP, Russell JA, Wang H, Jackson MA, Mann L, Kluender KR (2008) Effect of tongue exercise and protrusive force and muscle fiber area in aging rats. J Speech Lang Hear Res (in press)

  • Das S, Fowler SC (1996) An update of Fowler and Das: anticholinergic reversal of haloperidol-induced, within-session decrements in rats’ lapping behavior. Pharmacol Biochem Behav 53(4):853–855

    Article  PubMed  CAS  Google Scholar 

  • Delong MR, Wichmann T (2007) Circuits and circuit disorders of the basal ganglia. Arch Neurol 64:20–24

    Article  PubMed  Google Scholar 

  • Dubois B, Pillon B (1997) Cognitive deficits in Parkinson’s disease. J Neurol 244:2–8

    Article  PubMed  CAS  Google Scholar 

  • Dziewas R, Warnecke T, Schnabel M et al (2007) Neuroleptic-induced dysphagia: case report and literature review. Dysphagia 22:63–67

    Article  PubMed  Google Scholar 

  • Eadie MJ, Tyrer JH (1965) Alimentary disorder in Parkinsonism. Australas Ann Med 14:13–22

    PubMed  CAS  Google Scholar 

  • Farley BG, Koshland GF (2005) Training BIG to move faster: the application of the speed-amplitude relation as a rehabilitation strategy for people with Parkinson Disease. Exp Brain Res 167(3):462–467

    Article  PubMed  Google Scholar 

  • Fioritti A, Giaccotto L, Melega V (1997) Choking incidents among psychiatric patients: retrospective analysis of thirty-one cases from the west Bologna psychiatric wards. Can J Psychiatry 42(5):515–520

    PubMed  CAS  Google Scholar 

  • Fowler SC, Das S (1994) Haloperidol-induced decrements in force and duration of rats’ tongue movements during tongue pressing are attenuated by concomitant anticholinergic treatment. Pharma Biochem Behav 49(4):813–817

    Article  CAS  Google Scholar 

  • Fowler SC, Mortell C (1992) Low doses of haloperidol interfere with rat tongue extensions during licking: a quantitative analysis. Behav Neurosci 106(2):386–395

    Article  PubMed  CAS  Google Scholar 

  • Fuh JL, Lee RC, Wang SJ et al (1997) Swallowing difficulty in Parkinson’s disease. Clin Neurol Neurosurg 99:106–112

    Article  PubMed  CAS  Google Scholar 

  • Gentil M, Garcia-Ruiz P, Pollak P et al (1999) The effect of stimulation of the subthalamic nucleus on oral control of patients with Parkinsonism. J Neurol Neurosurg Psychiatry 67:329–333

    Article  PubMed  CAS  Google Scholar 

  • Gregory RP, Smith PT, Rudge P (1992) Tardive dyskinesia presenting as severe dysphagia. J Neurol Neurosurg Psychiatry 55(12):1203–1204

    Article  PubMed  CAS  Google Scholar 

  • Hayashi T, Nishikawa T, Koga I et al (1997) Life-threatening dysphagia following prolonged neuroleptic therapy. Clin Neuropharmacol 20(1):77–81

    Article  PubMed  CAS  Google Scholar 

  • Horak FB, Frank J, Nutt J (1996) Effects of dopamine of postural control in Parkinsonian subjects: scaling, set, and tone. J Neurophys 75:2380–2396

    CAS  Google Scholar 

  • Hunter PC, Crameri J, Austin S et al (1997) Response of parkinsonian swallowing dysfunction to dopaminergic stimulation. J Neurol Neurosurg Psychiatry 63:579–583

    Article  PubMed  CAS  Google Scholar 

  • Jurgens U (2002) Neural pathways underlying vocal control. Neurosci Biobehav Rev 26:235–258

    Article  PubMed  Google Scholar 

  • Lanis A, Schmidt WJ (2001) NMDA receptor antagonists do not block the development of sensitization of catalepsy, but make its expression state-dependent. Behav Pharmacol 12(2):143–149

    PubMed  CAS  Google Scholar 

  • Leopold NA, Kagel MA (1997) Pharyngo-esophageal dysphagia in Parkinson disease. Dysphagia 12:11–18

    Article  PubMed  CAS  Google Scholar 

  • Marras C, McDermott MP, Rochon PA, Parkinson Study Group DATATOP Investigators et al (2008) Predictors of deterioration in health-related quality of life in Parkinson’s disease: results from the DATATOP trial. Mov Disord 23(5):653–659

    Article  PubMed  Google Scholar 

  • Miller N, Noble E, Jones D et al (2006) Hard to swallow: dysphagia in Parkinson’s disease. Age Ageing 35(6):614–618

    Article  Google Scholar 

  • Miller N, Allcock LM, Hildreth T, Jones D, Noble E, Burn D (2008) Swallowing problems in Parkinson’s disease: frequency and clinical correlates. J Neurol Neurosurg Psychiatry 17:177–190

    Google Scholar 

  • Moss SJ, Wang G, Chen R et al (2001) 3-Acetylpyridine reduces tongue protrusion force but does not abolish lick rhythm in the rat. Brain Res 920:1–9

    Article  PubMed  CAS  Google Scholar 

  • Moss SJ, Birkestrand B, Fowler SC (2002) The neuroimmunophilin GPI-1046 partially protects against 3-acetylpyridine toxicity in the rat. Neurosci Lett 321:53–56

    Article  PubMed  CAS  Google Scholar 

  • Nagaya M, Kachi T, Yamada T et al (1998) Videofluorographic study of swallowing in Parkinson disease. Dysphagia 13:95–100

    Article  PubMed  CAS  Google Scholar 

  • Nilsson H, Ekberg O, Olsson R et al (1996) Quantitative assessment of oral and pharyngeal function in Parkinson’s disease. Dysphagia 11:144–150

    Article  PubMed  CAS  Google Scholar 

  • Owen AM, James M, Leigh PN et al (1992) Fronto-striatal cognitive deficits at different stages of Parkinson’s disease. Brain 115(Pt 6):1727–1751

    Article  PubMed  Google Scholar 

  • Potulska A, Friedman A, Krolicki L et al (2002) Swallowing disorders in Parkinson’s disease. Neurol Neurochir Pol 26:449–456

    Google Scholar 

  • Potulska A, Friedman A, Krolicki L et al (2003) Swallowing disorders in Parkinson’s disease. Parkinsonism Relat Disord 9:349–353

    Article  PubMed  Google Scholar 

  • Sanberg PR, Bunsey MD, Giordano M et al (1988) The catalepsy test: its ups and downs. Behav Neurosci 102(5):759–784

    Article  Google Scholar 

  • Schmidt WJ, Tzschentke TM, Kretschmer BD (1999) State-dependent blockade of haloperidol-induced sensitization of catalepsy by MK-801. Eur J Neurosci 11:3365–3368

    Article  PubMed  CAS  Google Scholar 

  • Schneider JS, Diamond SG, Markham CH (1986) Deficits in orofacial sensorimotor function in Parkinson’s disease. Ann Neurol 19(3):275–282

    Article  PubMed  CAS  Google Scholar 

  • Smittkamp SE, Brown JW, Stanford JA (2008) Time-course and characterization of orolingual motor deficits in B6SJL-Tg(SOD1-G93A)1Gur/J mice. Neuroscience 151(2):613-621.C:\VA Merit Grant\References\larynx4.ref #1191

    Google Scholar 

  • Sokoloff LG, Pavlakovic R (1997) Neuroleptic-induced dysphagia. Dysphagia 12(4):177–179

    Article  PubMed  CAS  Google Scholar 

  • Stanford JA, Vorontsova E, Surgener SP et al (2003) Aged Fischer 344 rats exhibit altered orolingual motor function: relationships with nigrostriatal neurochemical measures. Neurobiol Aging 24(2):259–266

    Article  PubMed  CAS  Google Scholar 

  • Stewart JT (2003) Dysphagia associated with risperidone therapy. Dysphagia 18(4):274–275

    Article  PubMed  Google Scholar 

  • Toth LA, Gardiner GW (2000) Food and water restriction protocols: physiological and behavioral considerations. Contemp Top Lab Anim Sci 2039(6):9–17

    Google Scholar 

  • Wang XD, You GF, Chen HB et al (2002) Clinical course and cause of death in elderly patients with idiopathic Parkinson’s disease. Chin Med J 115:1409–1411

    PubMed  Google Scholar 

  • Yang CC et al (1995) Excitatory innervation of caudal hypoglossal nucleus from nucleus reticularis gigantocellularis in the rat. Neuroscience 65(2):365–374

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Hao Wang, John Russel, Aaron Johnson, Allison Schaser, and Lisa Vinney for assisting with animal training, Glen Leverson for statistical consulting, Kelsey Anderson for editing, Dr. Timothy Schallert for consultation, and Dr. Timothy McCulloch for artwork. This study was supported by grants from the National Institute of Deafness and Other Communication Disorders (R01DC005935 and R01DC008149).

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  1. Division of Otolaryngology, Department of Surgery, University of Wisconsin, 600 Highland Avenue K4/709, Madison, WI, 53792, USA

    Michelle Renee Ciucci & Nadine P. Connor

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  1. Michelle Renee Ciucci
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  2. Nadine P. Connor
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Correspondence to Michelle Renee Ciucci.

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Ciucci, M.R., Connor, N.P. Dopaminergic influence on rat tongue function and limb movement initiation. Exp Brain Res 194, 587–596 (2009). https://doi.org/10.1007/s00221-009-1736-2

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  • DOI: https://doi.org/10.1007/s00221-009-1736-2

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