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New determinants for causal neural mechanism of dry mouth in Parkinson’s disease induced by destruction of superior salivatory nucleus, facial nerve, and submandibular gland circuitry: an experimental study

Year 2023, , 153 - 159, 27.03.2023
https://doi.org/10.38053/acmj.1242763

Abstract

Aim: Dry mouth has been considered a clinical finding of Parkinson’s disease (PD), but we think otherwise. We studied if the olfactory bulbectomy (OBX) might rely on the superior salivatory nucleus (SSN), submandibular ganglia (SMGn), and submandibular glands (SLGl) circuity disruption induced submandibular gland degeneration related dry mouth in rats.
Material and Method: This study was carried out on twenty-six male rats. Five (GI-n=5), six (GII, n=6), and sixteen (GIII, n=15) of them were used as control, SHAM, and OBX groups, respectively, and followed eight weeks. PD-related clinical examinations were done before and after the experiment (1/day), and animals were decapitated. The olfactory bulb volumes (mm3), degenerated neuron densities of SSN/SMG (n/mm3 and SMGl follicles volumes were detected serologically. Olfactory bulb volume values and degenerated neuron density values of SSN/SMGn/SMGl follicles volumes were compared statistically.
Results: OBX-applied animals showed anosmia, tremors, rigidity, and memory loss. The mean olfactory bulb volumes (mm3), degenerated neuron density of SSN (n/mm3), SMGn (n/mm3), and follicles volumes of SMGl (cubic micrometer/mm3) were measured in the order written as; (4.27±0.21), (4±1), (5±2), (81.23±13.34).106 in GI; (3.67±0.33), (14±3), (17±4), (72.45±11.78).106 in GII and (2.91±0.14), (23±5), (29±8), (57.19±11.93).106 in Group III. The mean P values between olfactory bulb volumes, degenerated neuron densities of SSN and SMGn, and salivary follicles volumes were: p<0.005 in GI/GII; p<0.0005 in GII/GIII; p<0.0001 in GI/GIII.
Conclusion: OBX-related olfactory network designalisation may be responsible for SSN/SMGn circuitry degeneration-induced SMGl atrophy-based dry mouth. The OBX-related dry mouth should be considered a causative factor for Parkinson’s disease, not a result.

References

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  • Kang P, Kloke J, Jain S. Olfactory dysfunction and parasympathetic dysautonomia in Parkinson’s disease. Clin Auton Res 2012; 22: 161-6.
  • Morley JF, Weintraub D, Mamikonyan E, Moberg PJ, Siderowf AD, Duda JE. Olfactory dysfunction is associated with neuropsychiatric manifestations in Parkinson’s disease. Mov Disord 2011; 26: 2051-7.
  • Proserpio C, de Graaf C, Laureati M, Pagliarini E, Boesveldt S. Impact of ambient odors on food intake, saliva production and appetite ratings. Physiol Behav 2017; 174: 35-41.
  • Henkin RI, Velicu I. Decreased parotid salivary cyclic nucleotides related to smell loss severity in patients with taste and smell dysfunction. Metabolism 2009; 58: 1717-23.
  • Watanabe H, Mizunami M. Pavlov’s cockroach: classical conditioning of salivation in an insect. PLoS One 2007; 2: e529.
  • Zang Y, Han P, Burghardt S, Knaapila A, Schriever V, Hummel T. Influence of olfactory dysfunction on the perception of food. Eur Arch Otorhinolaryngol 2019; 276: 2811-7.
  • Dickson DW. Parkinson’s disease and parkinsonism: neuropathology. Cold Spring Harb Perspect Med. 2012; 2(8).
  • Paşahan R, Yardım A, Karadağ MK, Alpaslan A, Aydın MD. Dry mouth caused by facial nerve ischemia due to subarachnoid hemorrhage: an experimental study. World Neurosurg 2021; 154: e488-e94.
  • Aydin MD, Kanat A, Hacimuftuoglu A, Ozmen S, Ahiskalioglu A, Kocak MN. A new experimental evidence that olfactory bulb lesion may be a causative factor for substantia nigra degeneration; preliminary study. Int J Neurosci 2021; 131: 220-7.
  • Yeomans MR. Olfactory influences on appetite and satiety in humans. Physiol Behav. 2006; 87: 800-4.
  • Lee VM, Linden RW. An olfactory-submandibular salivary reflex in humans. Exp Physiol 1992; 77: 221-4.
  • Lee VM, Linden RW. An olfactory-parotid salivary reflex in humans? Exp Physiol 1991; 76: 347-55.
  • Savica R, Rocca WA, Ahlskog JE. When does Parkinson disease start? Arch Neurol 2010; 67: 798-801.
  • Alvarez MV, Grogan PM. Hyposmia in Parkinson’s disease. Psychiatry Clin Neurosci 2012; 66: 370.
  • Suchowersky O. Non-motor symptoms and parkinsonism. Can J Neurol Sci 2013; 40: 1-2.
  • Lasiter PS, Deems DA, Glanzman DL. Thalamocortical relations in taste aversion learning: I. Involvement of gustatory thalamocortical projections in taste aversion learning. Behav Neurosci 1985; 99: 454-76.
  • Mitoh Y, Funahashi M, Fujii A, Fujita M, Kobashi M, Matsuo R. Development of inhibitory synaptic transmission to the superior salivatory nucleus in rats. Brain Res 2008; 1191: 47-54.
  • Nicholson JE, Severin CM. The superior and inferior salivatory nuclei in the rat. Neurosci Lett 1981; 21: 149-54.
  • Ng YK, Wong WC, Ling EA. A light and electron microscopical localisation of the superior salivatory nucleus of the rat. J Hirnforsch 1994; 35: 39-48.
  • Li C, Fitzgerald ME, Del Mar N, Reiner A. Disinhibition of neurons of the nucleus of solitary tract that project to the superior salivatory nucleus causes choroidal vasodilation: Implications for mechanisms underlying choroidal baroregulation. Neurosci Lett 2016; 633: 106-11.
  • Takeuchi Y, Fukui Y, Ichiyama M, Miyoshi S, Nishimura Y. Direct amygdaloid projections to the superior salivatory nucleus: a light and electron microscopic study in the cat. Brain Res Bull 1991; 27: 85-92.
  • Way JS. Evidence for the site of the superior salivatory nucleus in the guinea pig: a retrograde HRP study. Anat Rec 1981; 201: 119-26.
  • Matsuo R, Yamamoto T, Kawamura Y. Morphological and functional evaluation of the superior salivatory nucleus in rabbits. Exp Neurol 1980; 68: 147-57.
  • Fukami H, Bradley RM. Biophysical and morphological properties of parasympathetic neurons controlling rats’ parotid and von Ebner salivary glands. J Neurophysiol. 2005; 93: 678-86.
  • Eisenman JS. Response of rat superior salivatory units to chorda tympani stimulation. Brain Res Bull. 1983; 10: 811-5.
  • Templeton D, Thulin A. Secretory, motor and vascular effects in the sublingual gland of the rat caused by autonomic nerve stimulation. Q J Exp Physiol Cogn Med Sci 1978; 63: 59-66.
  • Ramos JMJ, Castillo ME, Puerto A. Relationship between prandial drinking behavior and supersensitivity of salivary glands after superior salivatory nucleus lesions in rats. Physiol Behav 2020; 224: 113022.
  • Kim M, Chiego DJ, Jr., Bradley RM. Morphology of parasympathetic neurons innervating rat lingual salivary glands. Auton Neurosci 2004; 111: 27-36.
  • Karadeniz E, Kocak MN, Ahiskalioglu A, et al. Exploring of the unpredicted effects of olfactory network injuries on mammary gland degeneration: a preliminary experimental study. J Invest Surg 2019; 32: 624-31.
  • Firinci B, Caglar O, Karadeniz E, Ahiskalioglu A, Demirci T, Aydin MD. Mysterious effects of olfactory pathway lesions on intestinal immunodeficiency targeting Peyer’s patches: The first experimental study. Med Hypotheses 2019; 125: 31-6.
  • Aydin N, Ramazanoglu L, Onen MR, et al. Rationalization of the irrational neuropathologic basis of hypothyroidism-olfaction disorders paradox: experimental study. World Neurosurg 2017; 107: 400-8.
  • Oral E, Aydin MD, Aydin N, et al. How olfaction disorders can cause depression? The role of habenular degeneration. Neuroscience 2013; 240: 63-9.
  • Caglar O, Firinci B, Aydin MD, et al. Disruption of the network between Onuf’s nucleus and myenteric ganglia, and developing Hirschsprung-like disease following spinal subarachnoid haemorrhage: an experimental study. Int J Neurosci. 2019; 129: 1076-84.
  • Caglar O, Firinci B, Aydin ME, et al. First emerging evidence of the relationship between Onuf’s nucleus degeneration and reduced sperm number following spinal subarachnoid haemorrhage: Experimental study. Andrologia 2021; 53: e14030.
  • Saatçi Ö, Yılmaz NH, Zırh A, Yulug B. The therapeutic effect of deep brain stimulation on olfactory functions and clinical scores in Parkinson’s disease. J Clin Neurosci. 2019; 68: 55-61.
  • Cury RG, Carvalho MJ, Lasteros FJL, et al. Effects of subthalamic stimulation on olfactory function in Parkinson disease. World Neurosurg 2018; 114: e559-e64.
  • Kola S, Prichard DO, Bharucha AE, Hassan A. A prospective pilot study of the effects of deep brain stimulation on olfaction and constipation in Parkinson’s disease. Clin Neurol Neurosurg 2021; 207: 106774.
  • Dafsari HS, Dos Santos Ghilardi MG, Visser-Vandewalle V, et al. Beneficial nonmotor effects of subthalamic and pallidal neurostimulation in Parkinson’s disease. Brain Stimul 2020; 13: 1697-705.
  • Fonoff ET, de Oliveira YS, Driollet S, et al. Pet findings in reversible improvement of olfactory dysfunction after STN stimulation in a Parkinson’s disease patient. Mov Disord. 2010; 25: 2466-8.
  • Khaindrava V, Salin P, Melon C, Ugrumov M, Kerkerian-Le-Goff L, Daszuta A. High frequency stimulation of the subthalamic nucleus impacts adult neurogenesis in a rat model of Parkinson’s disease. Neurobiol Dis 2011; 42: 284-91.
  • Zibetti M, Torre E, Cinquepalmi A, et al. Motor and nonmotor symptom follow-up in parkinsonian patients after deep brain stimulation of the subthalamic nucleus. Eur Neurol 2007; 58: 218-23.
  • Yavasoglu NG, Comoglu SS. The effect of subthalamic deep brain stimulation on autonomic dysfunction in Parkinson’s disease: clinical and electrophysiological evaluation. Neurol Res. 2021; 43: 894-9.
Year 2023, , 153 - 159, 27.03.2023
https://doi.org/10.38053/acmj.1242763

Abstract

References

  • Tarakad A, Jankovic J. Anosmia and ageusia in Parkinson’s disease. Int Rev Neurobiol 2017; 133: 541-56.
  • Kang P, Kloke J, Jain S. Olfactory dysfunction and parasympathetic dysautonomia in Parkinson’s disease. Clin Auton Res 2012; 22: 161-6.
  • Morley JF, Weintraub D, Mamikonyan E, Moberg PJ, Siderowf AD, Duda JE. Olfactory dysfunction is associated with neuropsychiatric manifestations in Parkinson’s disease. Mov Disord 2011; 26: 2051-7.
  • Proserpio C, de Graaf C, Laureati M, Pagliarini E, Boesveldt S. Impact of ambient odors on food intake, saliva production and appetite ratings. Physiol Behav 2017; 174: 35-41.
  • Henkin RI, Velicu I. Decreased parotid salivary cyclic nucleotides related to smell loss severity in patients with taste and smell dysfunction. Metabolism 2009; 58: 1717-23.
  • Watanabe H, Mizunami M. Pavlov’s cockroach: classical conditioning of salivation in an insect. PLoS One 2007; 2: e529.
  • Zang Y, Han P, Burghardt S, Knaapila A, Schriever V, Hummel T. Influence of olfactory dysfunction on the perception of food. Eur Arch Otorhinolaryngol 2019; 276: 2811-7.
  • Dickson DW. Parkinson’s disease and parkinsonism: neuropathology. Cold Spring Harb Perspect Med. 2012; 2(8).
  • Paşahan R, Yardım A, Karadağ MK, Alpaslan A, Aydın MD. Dry mouth caused by facial nerve ischemia due to subarachnoid hemorrhage: an experimental study. World Neurosurg 2021; 154: e488-e94.
  • Aydin MD, Kanat A, Hacimuftuoglu A, Ozmen S, Ahiskalioglu A, Kocak MN. A new experimental evidence that olfactory bulb lesion may be a causative factor for substantia nigra degeneration; preliminary study. Int J Neurosci 2021; 131: 220-7.
  • Yeomans MR. Olfactory influences on appetite and satiety in humans. Physiol Behav. 2006; 87: 800-4.
  • Lee VM, Linden RW. An olfactory-submandibular salivary reflex in humans. Exp Physiol 1992; 77: 221-4.
  • Lee VM, Linden RW. An olfactory-parotid salivary reflex in humans? Exp Physiol 1991; 76: 347-55.
  • Savica R, Rocca WA, Ahlskog JE. When does Parkinson disease start? Arch Neurol 2010; 67: 798-801.
  • Alvarez MV, Grogan PM. Hyposmia in Parkinson’s disease. Psychiatry Clin Neurosci 2012; 66: 370.
  • Suchowersky O. Non-motor symptoms and parkinsonism. Can J Neurol Sci 2013; 40: 1-2.
  • Lasiter PS, Deems DA, Glanzman DL. Thalamocortical relations in taste aversion learning: I. Involvement of gustatory thalamocortical projections in taste aversion learning. Behav Neurosci 1985; 99: 454-76.
  • Mitoh Y, Funahashi M, Fujii A, Fujita M, Kobashi M, Matsuo R. Development of inhibitory synaptic transmission to the superior salivatory nucleus in rats. Brain Res 2008; 1191: 47-54.
  • Nicholson JE, Severin CM. The superior and inferior salivatory nuclei in the rat. Neurosci Lett 1981; 21: 149-54.
  • Ng YK, Wong WC, Ling EA. A light and electron microscopical localisation of the superior salivatory nucleus of the rat. J Hirnforsch 1994; 35: 39-48.
  • Li C, Fitzgerald ME, Del Mar N, Reiner A. Disinhibition of neurons of the nucleus of solitary tract that project to the superior salivatory nucleus causes choroidal vasodilation: Implications for mechanisms underlying choroidal baroregulation. Neurosci Lett 2016; 633: 106-11.
  • Takeuchi Y, Fukui Y, Ichiyama M, Miyoshi S, Nishimura Y. Direct amygdaloid projections to the superior salivatory nucleus: a light and electron microscopic study in the cat. Brain Res Bull 1991; 27: 85-92.
  • Way JS. Evidence for the site of the superior salivatory nucleus in the guinea pig: a retrograde HRP study. Anat Rec 1981; 201: 119-26.
  • Matsuo R, Yamamoto T, Kawamura Y. Morphological and functional evaluation of the superior salivatory nucleus in rabbits. Exp Neurol 1980; 68: 147-57.
  • Fukami H, Bradley RM. Biophysical and morphological properties of parasympathetic neurons controlling rats’ parotid and von Ebner salivary glands. J Neurophysiol. 2005; 93: 678-86.
  • Eisenman JS. Response of rat superior salivatory units to chorda tympani stimulation. Brain Res Bull. 1983; 10: 811-5.
  • Templeton D, Thulin A. Secretory, motor and vascular effects in the sublingual gland of the rat caused by autonomic nerve stimulation. Q J Exp Physiol Cogn Med Sci 1978; 63: 59-66.
  • Ramos JMJ, Castillo ME, Puerto A. Relationship between prandial drinking behavior and supersensitivity of salivary glands after superior salivatory nucleus lesions in rats. Physiol Behav 2020; 224: 113022.
  • Kim M, Chiego DJ, Jr., Bradley RM. Morphology of parasympathetic neurons innervating rat lingual salivary glands. Auton Neurosci 2004; 111: 27-36.
  • Karadeniz E, Kocak MN, Ahiskalioglu A, et al. Exploring of the unpredicted effects of olfactory network injuries on mammary gland degeneration: a preliminary experimental study. J Invest Surg 2019; 32: 624-31.
  • Firinci B, Caglar O, Karadeniz E, Ahiskalioglu A, Demirci T, Aydin MD. Mysterious effects of olfactory pathway lesions on intestinal immunodeficiency targeting Peyer’s patches: The first experimental study. Med Hypotheses 2019; 125: 31-6.
  • Aydin N, Ramazanoglu L, Onen MR, et al. Rationalization of the irrational neuropathologic basis of hypothyroidism-olfaction disorders paradox: experimental study. World Neurosurg 2017; 107: 400-8.
  • Oral E, Aydin MD, Aydin N, et al. How olfaction disorders can cause depression? The role of habenular degeneration. Neuroscience 2013; 240: 63-9.
  • Caglar O, Firinci B, Aydin MD, et al. Disruption of the network between Onuf’s nucleus and myenteric ganglia, and developing Hirschsprung-like disease following spinal subarachnoid haemorrhage: an experimental study. Int J Neurosci. 2019; 129: 1076-84.
  • Caglar O, Firinci B, Aydin ME, et al. First emerging evidence of the relationship between Onuf’s nucleus degeneration and reduced sperm number following spinal subarachnoid haemorrhage: Experimental study. Andrologia 2021; 53: e14030.
  • Saatçi Ö, Yılmaz NH, Zırh A, Yulug B. The therapeutic effect of deep brain stimulation on olfactory functions and clinical scores in Parkinson’s disease. J Clin Neurosci. 2019; 68: 55-61.
  • Cury RG, Carvalho MJ, Lasteros FJL, et al. Effects of subthalamic stimulation on olfactory function in Parkinson disease. World Neurosurg 2018; 114: e559-e64.
  • Kola S, Prichard DO, Bharucha AE, Hassan A. A prospective pilot study of the effects of deep brain stimulation on olfaction and constipation in Parkinson’s disease. Clin Neurol Neurosurg 2021; 207: 106774.
  • Dafsari HS, Dos Santos Ghilardi MG, Visser-Vandewalle V, et al. Beneficial nonmotor effects of subthalamic and pallidal neurostimulation in Parkinson’s disease. Brain Stimul 2020; 13: 1697-705.
  • Fonoff ET, de Oliveira YS, Driollet S, et al. Pet findings in reversible improvement of olfactory dysfunction after STN stimulation in a Parkinson’s disease patient. Mov Disord. 2010; 25: 2466-8.
  • Khaindrava V, Salin P, Melon C, Ugrumov M, Kerkerian-Le-Goff L, Daszuta A. High frequency stimulation of the subthalamic nucleus impacts adult neurogenesis in a rat model of Parkinson’s disease. Neurobiol Dis 2011; 42: 284-91.
  • Zibetti M, Torre E, Cinquepalmi A, et al. Motor and nonmotor symptom follow-up in parkinsonian patients after deep brain stimulation of the subthalamic nucleus. Eur Neurol 2007; 58: 218-23.
  • Yavasoglu NG, Comoglu SS. The effect of subthalamic deep brain stimulation on autonomic dysfunction in Parkinson’s disease: clinical and electrophysiological evaluation. Neurol Res. 2021; 43: 894-9.
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Details

Primary Language English
Subjects Health Care Administration
Journal Section Research Articles
Authors

Mete Zeynal 0000-0002-7398-443X

Publication Date March 27, 2023
Published in Issue Year 2023

Cite

AMA Zeynal M. New determinants for causal neural mechanism of dry mouth in Parkinson’s disease induced by destruction of superior salivatory nucleus, facial nerve, and submandibular gland circuitry: an experimental study. Anatolian Curr Med J / ACMJ / acmj. March 2023;5(2):153-159. doi:10.38053/acmj.1242763

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