Українська English

ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2022; 68(1): 74-86


PHYSIOLOGICAL FUNCTIONS DISORDERS OF THE SUPERIOR CERVICAL GANGLION NEURONS IN DIABETES MELLITUS

A.O. Nastenko, H.E. Purnyn, N.S. Veselovsky

    O.O.Bogomoletz Institute of Physiology NAS of Ukraine, Kyiv, Ukraine
DOI: https://doi.org/10.15407/fz68.01.074


Abstract

A large number of extra- and intramural ganglia in humans and animals exist. All pathways of central regulation of vegetative functions and peripheral reflex pathways pass through them, providing coordinated automatic activity of many organs and tissues. It is well known that sympathetic and sensory neurons are affected in the early stages of diabetes. Patients with diabetes often have autonomic neuropathies. They suffer from disorders of the cardiovascular system and vessels functions, from disorders of the thermoregulatory and pupilomotor functions. These disorders may be the result of the superior cervical ganglion neurons functional defects. This ganglion involves in homeostasis, innervates pineal gland, thyroid, vascular plexus, vestibular system, pupillary, carotid bodies, salivary and lacrimal glands, innervates vessels of the skull and brain. The superior cervical ganglion’s postganglionic axons also innervate the heart. However, disorders of the synaptic transmission in superior cervical ganglion neurons in diabetes remain insufficiently studied to date. Therefore, this article is about the physiological properties of the superior cervical ganglion neurons and their pathological changes in diabetes mellitus. The works about synaptic neurotransmission disorders in superior cervical ganglion neurons of animals with experimental diabetes mellitus are analyzed.

Keywords: superior cervical ganglion; diabetes; synaptic transmission.

References

  1. Wehrwein EA, Orer HS, Barman SM. Overview of the anatomy, physiology, and pharmacology of the autonomic nervous system. Compr Physiol. 2016 Jun 13;6(3):1239-78. CrossRef PubMed
  2. Savastano LE, Castro AE, Fitt MR, Rath MF, Romeo HE, Muñoz EM. A standardized surgical technique for rat superior cervical ganglionectomy. J Neurosci Methods. 2010 Sep 30;192(1):22-33. CrossRef PubMed
  3. Aydin MD, Kanat A, Yolas C, Soyalp C, Onen MR, Yilmaz I, Karaavci NC, Calik M, Baykal O, Ramazanoglu L. Spinal subarachnoid hemorrhage induced intractable miotic pupil. A reminder of ciliospinal sympathetic center ischemia based miosis: An experimental study. Turk Neurosurg. 2019;29(3):434-39. CrossRef
  4. Zhang W, Xiong K, Zhang Y, Wenling MA. Afferent pathway of the vagal nerve fibers conveying cardiac pain information via the superior cervical ganglion. Acta Anatomica Sinica. 2002;2:140-3.
  5. Bowers CW, Zigmond RE. Sympathetic neurons in lower cervical ganglia send axons through the superior cervical ganglion. Neuroscience. 1981;6(9):1783-91. CrossRef
  6. Purnyn, H, Rikhalsky O, Fedulova S, Veselovsky N. Transmission pathways in the rat superior cervical ganglion. Neurophysiology. 2007;39:347-9. CrossRef
  7. Baklavajian OH. Vegetative regulation of electrical activity in the brain. Leningrad: Science; 1967. [Russian].
  8. Perreau-Lenz S, Kalsbeek A, Garidou ML, Wortel J, van der Vliet J, van Heijningen C, Simonneaux V, Pévet P, Buijs RM. Suprachiasmatic control of melatonin synthesis in rats: inhibitory and stimulatory mechanisms. Eur J Neurosci. 2003 Jan;17(2):221-8. CrossRef PubMed
  9. Lichtman JW, Purves D, Yip JW. On the purpose of selective innervation of guinea-pig superior cervical ganglion cells. J Physiol. 1979 Jul;292:69-84. CrossRef PubMed PubMedCentral
  10. Chang HH, Lee YC, Chen MF, Kuo JS, Lee TJ. Sympathetic activation increases basilar arterial blood flow in normotensive but not hypertensive rats. Am J Physiol Heart Circ Physiol. 2012 Mar 1;302(5):H1123-30. CrossRef PubMed
  11. Nakajima S, Moriuchi H, Baba M, Egami T, Kumagami H. Anisocoria in inner ear lesions. ORL J Otorhinolaryngol Relat Spec. 1980;42(4):206-19. CrossRef PubMed
  12. Eccles JC. Facilitation and inhibition in the superior cervical ganglion. J Physiol. 1935 Oct 26;85(2):207-38. CrossRef PubMed PubMedCentral
  13. Purves D, Wigston DJ. Neural units in the superior cervical ganglion of the guinea-pig. J Physiol. 1983;334:169-78. CrossRef PubMed PubMedCentral
  14. Skok VI, Selyanko AA, Derkach VA. Neuronal cholinergic receptors. Moscow: Science. 1987. [Russian].
  15. Bowers CW, Zigmond RE. Localization of neurons in the rat superior cervical ganglion that project into different postganglionic trunks. J Comp Neurol. 1979 May 15;185(2):381-91. CrossRef PubMed
  16. Jacobowitz D, Woodward JK. Adrenergic neurons in the cat superior cervical ganglion and cervical sympathetic nerve trunk. A histochemical study. J Pharmacol Exp Ther. 1968 Aug;162(2):213-26.
  17. Li C, Horn JP. Physiological classification of sympathetic neurons in the rat superior cervical ganglion. J Neurophysiol. 2006 Jan;95(1):187-95. CrossRef PubMed
  18. Eranko O, Eranko L. Small, intensely fluorescent granulecontaining cells in, the sympathetic ganglion of the rat. Prog Brain Res. 1971;34(3):39-51. CrossRef
  19. Case CP, Matthews MR. A quantitative study of structural features, synapses and nearest-neighbour relationships of small, granule-containing cells in the rat superior cervical sympathetic ganglion at various adult stages. Neuroscience. 1985 May;15(1):237-82. CrossRef
  20. Björklund A, Cegrell L, Falck B, Ritzén M, Rosengren E. Dopamine-containing cells in sympathetic ganglia. Acta Physiol Scand. 1970 Mar;78(3):334-8. CrossRef PubMed
  21. Häppölä O, Päivärinta H, Soinila S, Steinbusch H. Preand postnatal development of 5-hydroxytryptamine immunoreactive cells in the superior cervical ganglion of the rat. J Auton Nerv Syst. 1986 Jan;15(1):21-31. CrossRef
  22. Case CP, Matthews MR. Outgoing synapses of small granule-containing cells in the rat superior cervical ganglion after post-ganglionic axotomy. J Physiol. 1986 May;374:1-32. CrossRef PubMed PubMedCentral
  23. Elfvin LG, Hökfelt T, Goldstein M. Fluorescence microscopical, immunohistochemical and ultrastructural studies on sympathetic ganglia of the guinea pig, with special reference to the sif cells and their catecholamine content. J Ultrastruct Res. 1975 Jun;51(3):377-96. CrossRef
  24. Williams T, Jew J. Monoamine connections in sympathetic ganglia. In: Elfvin LG autonomic ganglia. Chichester: John Wiley & Sons. 1983:145-82.
  25. Skok VI. Physiology of the autonomic ganglia. Leningrad: Science; 1970. [Russian].
  26. Skok VI. Ganglionic transmission: Morphology and physiology. Springer. 1980;53(2):9-38. CrossRef
  27. Akasu T, Koketsu K. Muscarinic transmission. In: Karczmar AG, Koketsu K, Nishi S (Eds). Autonomic and Enteric Ganglia: Transmission and Its Pharmacology. New York: Plenum Press. 1986: 161-80. CrossRef
  28. Kuba K, Koketsu K. Synaptic events in sympathetic ganglia. Prog Neurobiol. 1978;11(2):77-169. CrossRef
  29. Koketsu K. Inhibitory transmission: slow inhibitory postsynaptic potential. New York, London: Plenum press. 1986: 201-21. CrossRef
  30. Kafka MS, Thoa NB. Alpha-adrenergic receptors in the rat superior cervical ganglion. Biochem Pharmacol. 1979 Aug 15;28(16):2485-9. CrossRef
  31. De Groat WC, Volle RL. The actions of the catecholamines on transmission in the superior cervical ganglion of the cat. J Pharmacol Exp Ther. 1966 Oct;154(1):1-13.
  32. Lundberg JM, Hökfelt T, Anggård A, Terenius L, Elde R, Markey K, Goldstein M, Kimmel J. Organizational principles in the peripheral sympathetic nervous system: subdivision by coexisting peptides (somatostatin-, avian pancreatic polypeptide-, and vasoactive intestinal polypeptide-like immunoreactive materials). Proc Natl Acad Sci USA. 1982 Feb;79(4):1303-7. CrossRef PubMed PubMedCentral
  33. Baffi J, Görcs T, Slowik F, Horváth M, Lekka N, Pásztor E, Palkovits M. Neuropeptides in the human superior cervical ganglion. Brain Res. 1992 Jan 20;570(1-2):272-8. CrossRef
  34. Katayama Y, Nishi S. Peptidergic transmission. In: Karczmar AG, Koketsu K, Nishi S (Eds). Autonomic and Enteric Ganglia: Transmission and Its Pharmacology. New York: Plenum Press. 1986: 181-96. CrossRef
  35. Campanucci VA, Krishnaswamy A, Cooper E. Mitochondrial reactive oxygen species inactivate neuronal nicotinic acetylcholine receptors and induce long-term depression of fast nicotinic synaptic transmission. J Neurosci. 2008 Feb 13;28(7):1733-44. CrossRef PubMed PubMedCentral
  36. Tomlinson DR, Gardiner NJ. Glucose neurotoxicity. Nat Rev Neurosci. 2008 Jan;9(1):36-45. CrossRef PubMed
  37. Vinik AI, Maser RE, Mitchell BD, Freeman R. Diabetic autonomic neuropathy. Diabetes Care. 2003 May;26(5):1553-79. CrossRef PubMed
  38. Appenzeller O, Richardson EP Jr. The sympathetic chain in patients with diabetic and alcoholic polyneuropathy. Neurology. 1966 Dec;16(12):1205-9. CrossRef PubMed
  39. Low PA, Walsh JC, Huang CY, McLeod JG. The sympathetic nervous system in diabetic neuropathy. A clinical and pathological study. Brain. 1975 Sep;98(3):341-56. CrossRef PubMed
  40. Li G, Sheng X, Xu Y, Jiang H, Zheng C, Guo J, Sun S, Yi Z, Qin S, Liu S, Gao Y, Zhang C, Xu H, Wu B, Zou L, Liang S, Zhu G. Co-expression changes of lncRNAs and mRNAs in the cervical sympathetic ganglia in diabetic cardiac autonomic neuropathic rats. J Neurosci Res. 2017 Aug;95(8):1690-9. CrossRef PubMed
  41. Campanucci V, Krishnaswamy A, Cooper E. Diabetes depresses synaptic transmission in sympathetic ganglia by inactivating nAChRs through a conserved intracellular cysteine residue. Neuron. 2010 Jun 24;66(6):827-34. CrossRef PubMed
  42. Schmidt RE, Plurad SB, Parvin CA, Roth KA. Effect of diabetes and aging on human sympathetic autonomic ganglia. Am J Pathol. 1993 Jul;143(1):143-53.
  43. Schmidt RE, Plurad SB. Ultrastructural and biochemical characterization of autonomic neuropathy in rats with chronic streptozotocin diabetes. J Neuropathol Exp Neurol. 1986 Sep;45(5):525-44. CrossRef PubMed
  44. Schmidt RE, Dorsey DA, Roth KA. Immunohistochemical characterization of NPY and substance P containing nerve terminals in aged and diabetic human sympathetic ganglia. Brain Res. 1992 Jun 26;583(1-2):320-6. CrossRef
  45. Yagihashi S, Sima AA. Diabetic autonomic neuropathy in BB rat. Ultrastructural and morphometric changes in parasympathetic nerves. Diabetes. 1986 Jul;35(7):733-43. CrossRef PubMed
  46. Lindh B, Hökfelt T, Elfvin LG, Terenius L, Fahrenkrug J, Elde R, Goldstein M. Topography of NPY-, somatostatin-, and VIP-immunoreactive, neuronal subpopulations in the guinea pig celiac-superior mesenteric ganglion and their projection to the pylorus. J Neurosci. 1986 Aug;6(8):2371-83. CrossRef PubMed PubMedCentral
  47. Krishnaswamy A, Cooper E. Reactive oxygen species inactivate neuronal nicotinic acetylcholine receptors through a highly conserved cysteine near the intracellular mouth of the channel: implications for diseases that involve oxidative stress. J Physiol. 2012 Jan 1;590(1):39-47. CrossRef PubMed PubMedCentral
  48. Vernino S, Low PA, Fealey RD, Stewart JD, Farrugia G, Lennon VA. Autoantibodies to ganglionic acetylcholine receptors in autoimmune autonomic neuropathies. N Engl J Med. 2000 Sep 21;343(12):847-55. CrossRef PubMed
  49. Greene DA, Mackway AM. Decreased myo-inositol content and Na+-K+-ATPase activity in superior cervical ganglion of STZ-diabetic rat and prevention by aldose reductase inhibition. Diabetes. 1986 Oct;35(10):1106-8. CrossRef PubMed
  50. Silva-Dos-Santos NM, Oliveira-Abreu K, Moreira-Junior L, Santos-Nascimento TD, Silva-Alves KSD, Coelhode-Souza AN, Ferreira-da-Silva FW, Leal-Cardoso JH. Diabetes mellitus alters electrophysiological properties in neurons of superior cervical ganglion of rats. Brain Res. 2020 Feb 15;1729. CrossRef PubMed
  51. Alzoubi KH, Khabour OF, Alhaidar IA, Aleisa AM, Alkadhi KA. Diabetes impairs synaptic plasticity in the superior cervical ganglion: possible role for BDNF and oxidative stress. J Mol Neurosci. 2013 Nov;51(3):763-70. CrossRef PubMed
  52. Alzoubi KH, Aleisa AM, Alkadhi KA. Expression of gLTP in sympathetic ganglia from stress-hypertensive rats: molecular evidence. J Mol Neurosci. 2008 Jun;35(2):201-9. CrossRef PubMed
  53. Racaniello M, Cardinale A, Mollinari C, D'Antuono M, De Chiara G, Tancredi V, Merlo D. Phosphorylation changes of CaMKII, ERK1/2, PKB/Akt kinases and CREB activation during early long-term potentiation at Schaffer collateral-CA1 mouse hippocampal synapses. Neurochem Res. 2010 Feb;35(2):239-46. CrossRef PubMed
  54. Carroll SL, Byer SJ, Dorsey DA, Watson MA, Schmidt RE. Ganglion-specific patterns of diabetes-modulated gene expression are established in prevertebral and paravertebral sympathetic ganglia prior to the development of neuroaxonal dystrophy. J Neuropathol Exp Neurol. 2004 Nov;63(11):1144-54. CrossRef PubMed
  55. Bitar MS, Pilcher CW, Khan I, Waldbillig RJ. Diabetesinduced suppression of IGF-1 and its receptor mRNA levels in rat superior cervical ganglia. Diabetes Res Clin Pract. 1997 Nov;38(2):73-80. CrossRef
  56. Fontana P, Genesio R, Casertano A, Cappuccio G, Mormile A, Nitsch L, Iolascon A, Andria G, Melis D. Loeys-Dietz syndrome type 4, caused by chromothripsis, involving the TGFB2 gene. Gene. 2014 Mar 15;538(1):69-73. CrossRef PubMed
  57. Hsieh CH, Chung RH, Lee WJ, Lin MW, Chuang LM, Quertermous T, Assimes T, Hung YJ, Yu YW. Effect of common genetic variants of growth arrest-specific 6 gene on insulin resistance, obesity and type 2 diabetes in an Asian population. PLoS One. 2015 Aug 18;10(8):e0135681. CrossRef PubMed PubMedCentral
  58. Solari R, Pease JE, Begg M. «Chemokine receptors as therapeutic targets: Why aren't there more drugs?» Eur J Pharmacol. 2015 Jan 5;746:363-7. CrossRef PubMed
  59. Mundinger TO, Cooper E, Coleman MP, Taborsky GJ Jr. Short-term diabetic hyperglycemia suppresses celiac ganglia neurotransmission, thereby impairing sympathetically mediated glucagon responses. Am J Physiol Endocrinol Metab. 2015 Aug 1;309(3):E246-55. CrossRef PubMed PubMedCentral
  60. Cotter MA, Jack AM, Cameron NE. Effects of the protein kinase C beta inhibitor LY333531 on neural and vascular function in rats with streptozotocin-induced diabetes. Clin Sci (Lond). 2002 Sep;103(3):311-21. CrossRef PubMed
  61. Cameron NE, Cotter MA. Diabetes causes an early reduction in autonomic ganglion blood flow in rats. J Diabetes Complicat. 2001 Jul-Aug;15(4):198-202. CrossRef

© National Academy of Sciences of Ukraine, Bogomoletz Institute of Physiology, 2014-2024.