Parasympathetic varicosity proliferation and synaptogenesis in rat eyelid smooth muscle after sympathectomy

Brain Research

Volumn 786, Issue 1-2, 1998, Pages 171-180

  Smith, Peter G ^a   Marzban, Farshid ^a,b  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b Parker College of Chiropractic   (United States)

Author keywords

Autonomic nervous system; Denervation; Plasticity

Indexed keywords

ANIMAL TISSUE; ARTICLE; AUTONOMIC DENERVATION; EYELID MUSCLE; NERVE CELL PLASTICITY; NERVE INJURY; NONHUMAN; PRIORITY JOURNAL; RAT; SYMPATHECTOMY; SYNAPTOGENESIS;

ANIMALS; EYELIDS; MICROSCOPY, ELECTRON; MUSCLE, SMOOTH; PARASYMPATHETIC NERVOUS SYSTEM; RATS; RATS, SPRAGUE-DAWLEY; SYMPATHECTOMY; SYNAPSES; TIME FACTORS;

EID: 0032498933     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(97)01439-X     Document Type: Article

References (83)

1. [1] J. Aberdeen, L. Corr, P. Milner, J. Lincoln, G. Burnstock, Marked increases in calcitonin gene-related peptide-containing nerves in the developing rat following long-term sympathectomy with guanethidine, Neuroscience 35 (1990) 175-184.
2. [2] J. Aberdeen, D. Moffitt, G. Burnstock, Increases in NPY in non-sympathetic nerve fibres supplying rat mesenteric vessels after immunosympathectomy, Regul. Pept. 34 (1991) 43-54.
3. [3] D. Barker, M. Saito, Autonomic innervation of receptors and muscle fibres in cat skeletal muscle, Proc. R. Soc. Lond. B. Biol. Sci. 212 (1981) 317-332.
4. [4] C.L. Beauregard, P.G. Smith, Parasympathetic innervation of rat peri-orbital smooth muscle: Pre-junctional cholinergic inhibition of sympathetic neurotransmission without direct post-junctional actions, J. Pharmacol. Exp. Ther. 268 (1994) 1284-1288.
5. [5] C.L. Beauregard, P.G. Smith, Parasympathetic excitation of sympathetic innervation after cholinesterase inhibition, Br. J. Pharmacol. 117 (1996) 51-54.
6. [6] M.R. Bennett, Autonomic neuromuscular transmission at a varicosity, Prog. Neurobiol. 50 (1996) 505-532.
7. [7] M.R. Bennett, L. Farrell, W. Gibson, Quantal transmission at purinergic junctions: stochastic interaction between ATP and its receptors, Biophys. J. 68 (1997) 1-11.
8. [8] M.R. Bennett, E.M. McLachlan, R.S. Taylor, The formation of synapses in mammalian striated muscle re-innervated with autonomic pre-ganglionic nerves, J. Physiol. Lond. 233 (1973) 501-517.
9. [9] J.A. Bevan, Some functional consequences of variation in adrenergic synaptic cleft width and in nerve density and distribution, Fed. Proc. 36 (1977) 2439-2443.
10. [10] J.A. Bevan, R.D. Bevan, S.P. Duckies, Adrenergic regulation of vascular smooth muscle, in: D.F. Bohr, A.P. Somlyo, H.V. Sparks, Jr. (Eds.), The Cardiovascular System, Am. Physiol. Soc. Bethesda, MD, 1980, pp. 515-566.
11. [11] J.A. Bevan, D.W. Hosmer, B. Ljung, B.L. Pegram, C. Su, Innervation pattern and neurogenic response of rabbit veins, Blood Vessels 11 (1974) 172-182.
12. [12] H. Björklund, T. Hökfelt, M. Goldstein, L. Terenius, L. Olson, Appearance of the noradrenergic markers tyrosine hydroxylase and neuropeptide Y in cholinergic nerves of the iris following sympathectomy, J. Neurosci. 5 (1985) 1633-1643.
13. [13] G. Burnstock, M. Costa, Adrenergic neurons. Their organization, function and development in the peripheral nervous system, Wiley, New York, 1975, pp. 1-225.
14. [14] J.K. Choate, M. Klemm, G.D.S. Hirst, G.D. Hirst, Sympathetic and parasympathetic neuromuscular junctions in the guinea-pig sino-atrial node, J. Auton. Nerv. Syst. 44 (1993) 1-16.
15. [15] J.R.O. Collin, C. Beard, I. Wood, Terminal course of nerve supply to Muller's muscle in the rhesus monkey and its clinical significance, Am. J. Ophthalmol. 87 (1979) 234-246.
16. [16] L.J. Cottee, N.A. Lavidis, M.R. Bennett, Spatial relationships between sympathetic varicosities and smooth muscle cells in the longitudinal layer of the mouse vas deferens, J. Neurocytol. 25 (1996) 413-425.
17. [17] T. Cowen, An ultrastructural comparison of the relationships in blood vessels with functional and non-functional neuromuscular transmission, J. Neurocytol. 13 (1984) 369-392.
18. [18] J.T. Dodge, R.D. Bevan, J.A. Bevan, Comparison of density of sympathetic varicosities and their closeness to smooth muscle cells in rabbit middle cerebral and ear arteries and their branches, Circ. Res. 75 (1994) 916-925.
19. [19] B. Ehinger, B. Falck, B. Sporrong, Possible axo-axonal synapses between peripheral adrenergic and cholinergic nerve terminals, Z. Zellforsch. Mikrosk. Anat. 107 (1970) 508-521.
20. [20] J. Ekstrom, Sympathetic denervation affects the choline acetyltransferase activity in decentralized parasympathetic neurones of the submaxillary gland of the rat, Acta Physiol. Scand. 112 (1981) 71-75.
21. [21] J. Ekström, Choline acetyltransferase in salivary glands after surgical and chemical sympathectomy, Acta Physiol. Scand. 86 (1972) 539-545.
22. [22] A. Elbadawi, Ultrastructure of vesico-urethral innervation: II. Post-ganglionic axo-axonal synapses in intrinsic innervation of the vesicourethral lissosphincter: a new structural and functional concept in micturition, J. Urol. 131 (1984) 781-790.
23. [23] A. Elbadawi, M.A. Atta, Intrinsic neuromuscular defects in the neurogenic bladder: V. Autonomic re-innervation of the male feline rhabdosphincter following somatic denervation by bilateral sacral ventral rhizotomy, Neurourol. Urodyn. 5 (1986) 65-85.
24. [24] A.C. Esterhuizen, J.D.P. Graham, J.D. Lever, T.L.B. Spriggs, Catecholamine and acetylcholinesterase distribution in relation to noradrenaline release. An enzyme histochemical and autoradiographic study on the innervation of the cat nictitating muscle, Br. J. Pharmacol. 32 (1968) 46-56.
25. [25] U.S. von Euler, J.H. Gaddum, Pseudomotor contractures after degeneration of the facial nerve, J. Physiol. Lond. 73 (1931) 54-66.
26. [26] Q. Fan, P.G. Smith, Decreased vasoactive intestinal polypeptide-immunoreactivity of parasympathetic neurons and target innervation following long-term sympathectomy, Regul. Pept. 48 (1993) 337-343.
27. [27] E.A. Fike IV, E. Simons, C. Boswell, P.G. Smith, Sensory nerves impair sympathetic re-innervation and recovery of smooth muscle function, Exp. Neurol. 118 (1992) 85-94.
28. [28] G. Gabella, The structural relations between nerve fibres and muscle cells in the urinary bladder of the rat, J. Neurocytol. 24 (1995) 159-187.
29. [29] C. Gall, G. Lynch, Rapid axon sprouting in the neonatal rat hippocampus, Brain Res. 153 (1978) 357-362.
30. [30] J.R. Garrett, Changes in autonomic nerves of salivary glands on degeneration and regeneration, Prog. Brain Res. 34 (1971) 475-488.
31. [31] I.L. Gibbins, C.J. Haller, Ultrastructural identification of non-adrenergic, non-cholinergic nerves in the rat anococcygeus muscle, Cell Tissue Res. 200 (1979) 257-271.
32. [32] I.L. Gibbins, J.L. Morris, Co-existence of immunoreactivity to neuropeptide Y and vasoactive intestinal peptide in non-noradrenergic axons innervating guinea pig cerebral arteries, Brain Res. 444 (1988) 402-406.
33. [33] S. Gulbenkian, A. Merighi, J. Wharton, I.M. Varndell, J.M. Polak, Ultrastructural evidence for the coexistence of calcitonin gene-related peptide and substance P in secretory vesicles of peripheral nerves in the guinea pig, J. Neurocytol. 15 (1986) 535-542.
34. 1 muscarine receptor at post-ganglionic cardiac noradrenergic nerve fibres that is activated by endogenous acetylcholine, Naunyn Schmiedebergs Arch. Pharmacol. 342 (1990) 483-489.
35. [35] C.E. Hill, M. Klemm, F.R. Edwards, G.D.S. Hirst, Sympathetic transmission to the dilator muscle of the rat iris, J. Auton. Nerv. Syst. 45 (1993) 107-123.
36. [36] L.G. Isaacson, D. Ondris, K.A. Crutcher, Plasticity of mature sensory cerebrovascular axons following intracranial infusion of nerve growth factor, J. Comp. Neurol. 361 (1995) 451-460.
37. [37] D. Jacobowitz, G.B. Koelle, Histochemical correlations of acetylcholinesterase and catecholamines in post-ganglionic autonomic nerves of the cat, rabbit, and guinea pig, J. Pharmacol. Exp. Ther. 148 (1965) 225-237.
38. [38] J.A. Kessler, Parasympathetic, sympathetic and sensory interactions in the iris: nerve growth factor regulates cholinergic ciliary ganglion innervation in vivo, J. Neurosci. 5 (1985) 2719-2725.
39. [39] M.F. Klemm, D.F. Van Helden, S.E. Luff, Ultrastructural analysis of sympathetic neuromuscular junctions on mesenteric veins of the guinea pig, J. Comp. Neurol. 334 (1993) 159-167.
40. [40] D.S. Knight, J.A. Beal, R.D. Fabre, R.J. Henderson Jr, Catecholamine-containing, dopamine-beta-hydroxylase-immunoreactive perivascular nerve specializations in the rat kidney, Anat. Rec. 225 (1989) 77-86.
41. [41] S.H. Koslow, E. Giacobini, S. Kerpel-Fronius, L. Olson, Cholinergic transmission in the hypoglossal reinnervated nictitating membrane of the cat: an enzymatic, histochemical and physiological study, J. Pharmacol. Exp. Ther. 180 (1972) 664-671.
42. [42] L. Landmesser, Contractile and electrical responses of vagus-innervated frog sartorius muscle, J. Physiol. Lond. 213 (1971) 707-725.
43. [43] J.N. Langley, On the union of cranial autonomic (visceral) fibres with the nerve cells of the superior cervical ganglion, J. Physiol. Lond. 23 (1898) 240-270.
44. [44] S.E. Luff, S.G. Hengstberger, E.M. McLachlan, W.P. Anderson, Two types of sympathetic axon innervating the juxtaglomerular arterioles of the rabbit and rat kidney differ structurally from those supplying other arteries, J. Neurocytol. 20 (1991) 781-795.
45. [45] F. Marzban, P.G. Smith, Conversion of parasympathetic nerve function from pre-junctional inhibition to post-junctional smooth muscle excitation following sympathectomy is associated with formation of presumptive neuroeffector contacts, Soc. Neurosci. Abstr. 22 (1996) 293, (Abstract).
46. [46] A. Mattiasson, K.-E. Andersson, A. Elbadawi, E. Morgan, C. Sjögren, Interaction between adrenergic and cholinergic nerve terminals in the urinary bladder of rabbit, cat and man, J. Urol. 137 (1987) 1017-1019.
47. [47] E.M. McLachlan, S.E. Luff, Sympathetic innervation of renal and extra-renal arterial vessels, Kidney Int. Suppl. 37 (1992) S56-60.
48. [48] K. Messlinger, Functional morphology of nociceptive and other fine sensory endings (free nerve endings) in different tissues, Prog. Brain Res. 113 (1996) 273-298.
49. [49] M.C. Mione, J.F.R. Cavanagh, K.A. Kirkpatrick, G. Burnstock, Plasticity in expression of calcitonin gene-related peptide and substance P immunoreactivity in ganglia and fibres following guanethidine and/or capsaicin denervation, Cell Tissue Res. 268 (1992) 491-504.
50. [50] M.C. Mione, J.F.R. Cavanagh, J. Lincoln, P. Milner, G. Burnstock, Long-term chemical sympathectomy leads to an increase of neuropeptide Y immunoreactivity in cerebrovascular nerves and iris of the developing rat, Neuroscience 34 (1990) 369-378.
51. [51] J.V. Nadler, C.W. Cotman, G.S. Lynch, Histochemical evidence of altered development of cholinergic fibers in the rat dentate gyrus following lesions: I. Time course after complete unilateral entorhial lesion at various ages, J. Comp. Neurol. 171 (1977) 561-588.
52. [52] M. Nomoto, T. Yoshihara, T. Kanda, T. Kaneko, Synapse formation by autonomic nerves in the previously denervated neuromuscular junctions of the feline intrinsic laryngeal muscles, Brain Res. 539 (1991) 276-286.
53. [53] I. Nordenfelt, Choline acetyltransferase in salivary glands of the cat after sympathetic denervation, Q. J. Exp. Physiol. 50 (1965) 57-61.
54. [54] I. Nordenfelt, Cholinesterase in the submaxillary gland of the rat after sympathetic denervation, Q. J. Exp. Physiol. 53 (1968) 6-9.
55. [55] P. Ohlin, C. Perec, Choline acetylase in normal and denervated submaxillary glands of rats after repeated teeth amputations, Acta Physiol. Scand. 69 (1967) 134-139.
56. [56] R.E. Page, The distribution and innervation of the extraocular smooth muscle in the orbit of the rat, Acta Anat. Basel 85 (1973) 10-18.
57. [57] Y.D. Pendry, J. Maclagan, Evidence for inhibition of sympathetic neurotransmission by endogenously released acetylcholine in the guinea-pig trachea, Br. J. Pharmacol. 104 (1991) 817-822.
58. [58] D. Purves, Competitive and non-competitive re-innervation of mammalian sympathetic neurones by native and foreign fibres, J. Physiol. Lond. 261 (1976) 453-475.
59. [59] P.M. Robinson, C. Bell, The localization of acetylcholinesterase at the autonomic neuromuscular junction, J. Cell Biol. 33 (1967) 93-102.
60. [60] F. Schon, M. Ghatei, J.M. Allen, P.K. Mulderry, J.S. Kelly, S.R. Bloom, The effect of sympathectomy on calcitonin gene-related peptide levels in the rat trigeminovascular system, Brain Res. 348 (1985) 197-200.
61. [61] C.E. Sharp, P.G. Smith, Developmental regulation of parasympathetic nerve density by sympathetic innervation, Neuroscience 49 (1992) 229-236.
62. [62] E.J. Simons, P.G. Smith, Sensory and autonomic innervation of the rat eyelid: origins and peptide phenotypes, J. Chem. Neuroanat. 7 (1994) 35-47.
63. [63] P.G. Smith, Role of the sympathetic nervous system in functional maturation of Müller's smooth muscle in the rat, J. Pharmacol. Exp. Ther. 235 (1985) 330-334.
64. [64] P.G. Smith, Functional plasticity in the sympathetic nervous system of the neonatal rat, Exp. Neurol. 91 (1986) 136-146.
65. [65] P.G. Smith, C.L. Beauregard, Conversion of parasympathetic nerve function from pre-junctional inhibition to post-junctional excitation following sympathectomy of rat periorbital smooth muscle, Brain Res. 629 (1993) 319-322.
66. [66] P.G. Smith, J.W. Bruckert, E. Mills, Re-innervation of Müller's smooth muscle by atypical sympathetic pathways following neonatal ganglionectomy in the rat: structural and functional investigations of enhanced neuroplasticity, Neuroscience 23 (1987) 781-793.
67. [67] P.G. Smith, G. Evoniuk, C.W. Poston, E. Mills, Relation between functional maturation of cervical sympathetic innervation and ontogeny of α-noradrenergic smooth muscle contraction in the rat, Neuroscience 8 (1983) 609-616.
68. [68] P.G. Smith, Q. Fan, Sympathetic nerve trajectories to rat orbital targets: role of connective tissue pathways, J. Comp. Neurol. 365 (1996) 69-78.
69. [69] P.G. Smith, T.L. Hoffman, H. Reddy, Sprouting of aberrant neuropeptide Y-immunoreactive sympathetic nerves into neonatally denervated smooth muscle, Regul. Pept. 35 (1991) 103-113.
70. [70] P.G. Smith, H. Reddy, Reorganization of cranial sympathetic pathways following neonatal ganglionectomy in the rat, J. Comp. Neurol. 301 (1990) 490-500.
71. [71] P.G. Smith, H. Reddy, P. Venkataraman, Sympathetic sprouting into neonatally denervated contralateral target: superior cervical ganglion neuronal numbers and sizes, Dev. Brain Res. 53 (1990) 208-214.
72. [72] P.G. Smith, C.E. Sharp, Regulation of parasympathetic nerve density by sympathetic innervation during development, Soc. Neurosci. Abstr. 17 (1991) 216, (Abstract).
73. [73] U. Stenevi, A. Björklund, Growth of vascular sympathetic axons into the hippocampus after lesions of the septo-hippocampal pathway: a pitfall in brain lesion studies, Neurosci. Lett. 7 (1978) 219-224.
74. [74] L. Stjärne, Pre- and post-junctional receptor-mediated cholinergic interactions with adrenergic transmission in guinea-pig vas deferens, Naunyn-Schmiedeberg's Arch. Pharmacol. 288 (1975) 305-310.
75. [75] G. Terenghi, S.-Q. Zhang, W.G. Unger, J.M. Polak, Morphological changes of sensory CGRP-immunoreactive and sympathetic nerves in peripheral tissues following chronic denervation, Histochemistry 86 (1986) 89-95.
76. [76] S. Tyrrell, R.E. Siegel, S.C. Landis, Tyrosine hydroxylase and neuropeptide Y are increased in ciliary ganglia of sympathectomized rats, Neuroscience 47 (1992) 985-998.
77. [77] W.G. Unger, G. Terenghi, S.Q. Zhang, J.M. Polak, Alteration in the histochemical presence of tyrosine hydroxylase and CGRP-immunoreactivities in the eye following chronic sympathetic or sensory denervation, Curr. Eye Res. 7 (1988) 761-769.
78. [78] P.M. Vanhoutte, M.N. Levy, Pre-junctional cholinergic modulation of adrenergic neurotransmission in the cardiovascular system, Am. J. Physiol. 238 (1980) H275-H281.
79. [79] C.L. Vera, J.D. Vial, J.V. Luco, Re-innervation of nictitating membrane of cat by cholinergic fibers, J. Neurophysiol. 20 (1957) 365-373.
80. [80] J.D. Warn, Q. Fan, P.G. Smith, Decreased neuronal nitric oxide synthase-immunoreactivity and NADPH-diaphorase activity in rat pterygopalatine ganglion parasympathetic neurons and cerebrovascular innervation following long-term sympathectomy, Neurosci. Lett. 232 (1997) 25-28.
81. [81] J.D. Warn, P.G. Smith, Parasympathetic VAT and ChAT immunoreactivities are decreased in rat eyelid targets following sympathectomy, J. Auton. Nerv. Syst. 65 (1997) 119, (Abstract).
82. [82] T. Yamashita, R. Honjin, Fine structure, origin, and distribution density of the autonomic nerve endings in the tarsal muscle in the eyelid of the mouse, Cell Tissue Res. 222 (1982) 459-465.
83. [83] S.Q. Zhang, G. Terenghi, W.G. Unger, K.W. Ennis, J. Polak, Changes in substance P- and neuropeptide Y-immunoreactive fibres in rat and guinea-pig irides following unilateral sympathectomy, Exp. Eye Res. 39 (1984) 365-372.