Differential synaptic inputs to the cell body and proximal dendrites of preganglionic parasympathetic neurons in the rat conus medullaris

Neuroscience

Volumn 157, Issue 3, 2008, Pages 656-665

  Persson, S ^a   Havton, L A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

autonomic; electron microscopy; retrograde tracing; sacral; spinal cord; ultrastructure

Indexed keywords

CHOLERA TOXIN B SUBUNIT; HORSERADISH PEROXIDASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; CONUS MEDULLARIS; DENDRITE; FEMALE; INHIBITORY POSTSYNAPTIC POTENTIAL; NONHUMAN; PARASYMPATHETIC NERVE CELL; PERIKARYON; PREGANGLIONIC NERVE CELL; PRIORITY JOURNAL; RAT; SYNAPTIC POTENTIAL;

ANIMALS; AUTONOMIC FIBERS, PREGANGLIONIC; DENDRITES; FEMALE; HORSERADISH PEROXIDASE; MICROSCOPY, ELECTRON, TRANSMISSION; NEURONS; PRESYNAPTIC TERMINALS; RATS; SPINAL CORD; STATISTICS, NONPARAMETRIC; SYNAPSES;

EID: 56149094189     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.09.017     Document Type: Article

References (55)

1. Alvarez F.J., Villalba R.M., Zerda R., and Schneider S.P. Vesicular glutamate transporters in the spinal cord, with special reference to sensory primary afferent synapses. J Comp Neurol 472 (2004) 257-280
2. Araki I. Inhibitory postsynaptic currents and the effects of GABA on visually identified sacral parasympathetic preganglionic neurons in neonatal rats. J Neurophysiol 72 (1994) 2903-2910
3. Araki I., and de Groat W.C. Unitary excitatory synaptic currents in preganglionic neurons mediated by two distinct groups of interneurons in neonatal rat sacral parasympathetic nucleus. J Neurophysiol 76 (1996) 215-226
4. Birder L.A., Roppolo J.R., Erickson V.L., and de Groat W.C. Increased c-fos expression in spinal lumbosacral projection neurons and preganglionic neurons after irritation of the lower urinary tract in the rat. Brain Res 834 (1999) 55-65
5. Broman J., Anderson S., and Ottersen O.P. Enrichment of glutamate-like immunoreactivity in primary afferent terminals throughout the spinal cord dorsal horn. Eur J Neurosci 5 (1993) 1050-1061
6. Brown H.K., and Nolan M.F. Ultrastructure and quantitative synaptology of the sacral parasympathetic nucleus. J Neurocytol 8 (1979) 167-179
7. Cheng C.L., and de Groat W.C. The role of capsaicin-sensitive afferent fibers in the lower urinary tract dysfunction induced by chronic spinal cord injury in rats. Exp Neurol 187 (2004) 445-454
8. Chung E.A., and Emmanuel A.W. Gastrointestinal symptoms related to autonomic dysfunction following spinal cord injury. Prog Brain Res 152 (2006) 317-333
9. de Groat W.C. Integrative control of the lower urinary tract: preclinical perspective. Br J Pharmacol 147 (2006) 25-40
10. Fremeau Jr. R.T., Vogimaier S., Seal R.P., and Edwards R.H. VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci 27 (2004) 98-103
11. Gibson S.J., Polak J.M., Anand P., Blank M.A., Yiangou Y., Su H.C., Terenghi G., Katagiri T., Morrison J.F., Lumb B.M., et al. A VIP/PHI-containing pathway links urinary bladder and sacral spinal cord. Peptides 7 Suppl 1 (1986) 205-219
12. Hamilton M.O., Papka R.E., O'Donoghue D.L., Vaidya A.M., Williams S.J., Poff C.R., and McNeill D.L. Spinal projection neurons to the laterodorsal pontine tegmental nucleus: relationship to preganglionic neurons and nitric oxide synthase. J Comp Neurol 353 (1995) 1-8
13. Hancock M.B., and Peveto C.A. A preganglionic autonomic nucleus in the dorsal gray commissure of the lumbar spinal cord of the rat. J Comp Neurol 183 (1979) 65-72
14. Havton L.A., and Broman J. Systemic administration of cholera toxin B subunit conjugated to horseradish peroxidase in the adult rat labels preganglionic autonomic neurons, motoneurons, and select primary afferents for light and electron microscopic studies. J Neurosci Methods 149 (2005) 101-109
15. Henry M.A., Westrum L.E., and Johnson L.R. Enhanced ultrastructural visualization of the horseradish peroxidase-tetramethylbenzidine reaction product. J Histochem Cytochem 33 (1985) 1256-1259
16. Hoang T.X., Pikov V., and Havton L.A. Functional reinnervation of the rat lower urinary tract after cauda equina injury and repair. J Neurosci 26 (2006) 8672-8679
17. Kerns J.M., and Peters A. Ultrastructure of a large ventro-lateral dendritic bundle in the rat ventral horn. J Neurocytol 3 (1974) 533-555
18. Leedy M.G., Bresnahan J.C., Mawe G.M., and Beattie M.S. Differences in synaptic inputs to preganglionic neurons in the dorsal and lateral band subdivisions of the cat sacral parasympathetic nucleus. J Comp Neurol 268 (1988) 84-90
19. Liu Y., Sakurai H., Kurokawa K., Yamada H., and Kudo M. Glycine-immunoreactive synapses in the central nucleus of the inferior colliculus. An electron microscopic study in the cat. Neurosci Lett 269 (1999) 183-185
20. Llewellyn-Smith I.J., Martin C.L., Fenwick N.M., Dicarlo S.E., Lujan H.L., and Schreihofer A.M. VGLUT1 and VGLUT2 innervation in autonomic regions of intact and transected rat spinal cord. J Comp Neurol 503 (2007) 741-767
21. Logan S.D., Pickering A.E., Gibson I.C., Nolan M.F., and Spanswick D. Electrotonic coupling between rat sympathetic preganglionic neurones in vitro. J Physiol 495 (1996) 491-502
22. Matsumoto A., Arnold A.P., and Micevych P.E. Gap junctions between lateral spinal motoneurons in the rat. Brain Res 495 (1989) 362-366
23. Matsumoto A., Arnold A.P., Zampighi G.A., and Micevych P.E. Androgenic regulation of gap junctions between motoneurons in the rat spinal cord. J Neurosci 8 (1988) 4177-4183
24. Mawe G.M., Bresnahan J.C., and Beattie M.S. Primary afferent projections from dorsal and ventral roots to autonomic preganglionic neurons in the cat spinal cord: light and electron microscopic observations. Brain Res 290 (1984) 152-157
25. Mawe G.M., Bresnahan J.C., and Beattie M.S. A light and electron microscopic analysis of the sacral parasympathetic nucleus after labelling primary afferent and efferent elements with HRP. J Comp Neurol 250 (1986) 33-57
26. Mesulam M.M. Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26 (1978) 106-117
27. Mesulam M.M., Hegarty E., Barbas H., Carson K.A., Gower E.C., Knapp A.G., Moss M.B., and Mufson E.J. Additional factors influencing sensitivity in the tetramethyl benzidine method for horseradish peroxidase neurohistochemistry. J Histochem Cytochem 28 (1980) 1255-1259
28. Morgan C.W., Ohara P.T., and Scott D.E. Vasoactive intestinal polypeptide in sacral primary sensory pathways in the cat. J Comp Neurol 407 (1999) 381-394
29. Nadelhaft I., and Booth A.M. The location and morphology of preganglionic neurons and the distribution of visceral afferents from the rat pelvic nerve: a horseradish peroxidase study. J Comp Neurol 226 (1984) 238-245
30. Nakamura K., Wu S.X., Fujiyama F., Okamoto K., Hioki H., and Kaneko T. Independent inputs by VGLUT2- and VGLUT3-positive glutamatergic terminals onto rat sympathetic preganglionic neurons. Neuroreport 15 (2004) 431-436
31. Nolan M.F., and Brown H.K. A quantitative ultrastructural analysis of the synaptic population in sacral visceral gray. Exp Neurol 61 (1978) 165-174
32. Oliveira A.L., Hydling F., Olsson E., Shi T., Edwards R.H., Fujiyama F., Kaneko T., Hökfelt T., Cullheim S., and Meister B. Cellular localization of three vesicular glutamate transporter mRNAs and proteins in rat spinal cord and dorsal root ganglia. Synapse 50 (2003) 117-129
33. Olucha F., Martínez-García F., and López-García C. A new stabilizing agent for the tetramethyl benzidine (TMB) reaction product in the histochemical detection of horseradish peroxidase (HRP). J Neurosci Methods 13 (1985) 131-138
34. Örnung G., Ottersen O.P., Cullheim S., and Ulfhake B. Distribution of glutamate-, glycine- and GABA-immunoreactive nerve terminals on dendrites in the cat spinal motor nucleus. Exp Brain Res 118 (1998) 517-532
35. Örnung G., Shupliakov O., Lindå H., Ottersen O.P., Storm-Mathisen J., Ulfhake B., and Cullheim S. Qualitative and quantitative analysis of glycine- and GABA-immunoreactive nerve terminals on motoneuron cell bodies in the cat spinal cord: a postembedding electron microscopic study. J Comp Neurol 365 (1996) 413-426
36. Örnung G., Shupliakov O., Ottersen O.P., Storm-Mathisen J., and Cullheim S. Immunohistochemical evidence for coexistence of glycine and GABA in nerve terminals on cat spinal motoneurones: an ultrastructural study. Neuroreport 5 (1994) 889-892
37. Persson S., Boulland J.L., Aspling M., Larsson M., Fremeau Jr. R.T., Edwards R.H., Storm-Mathisen J., Chaudhry F.A., and Broman J. Distribution of vesicular glutamate transporters 1 and 2 in the rat spinal cord, with a note on the spinocervical tract. J Comp Neurol 497 (2006) 683-701
38. Persson S., and Broman J. Glutamate, but not aspartate, is enriched in trigeminothalamic tract terminals of the rat nucleus submedius. Exp Brain Res 157 (2004) 152-161
39. Peters A., Palay S.L., and Webster HdeF. The fine structure of the nervous system. 3rd ed. (1991), Oxford University Press, New York
40. Pikov V., and Wrathall J.R. Coordination of the bladder detrusor and the external urethral sphincter in a rat model of spinal cord injury: effect of injury severity. J Neurosci 21 (2001) 559-569
41. Ralston III H.J. Analysis of neuronal networks: a review of techniques for labeling axonal projections. J Electron Microsc Tech 15 (1990) 322-331
42. Ramirez-León V., and Ulfhake B. GABA-like immunoreactive innervation and dendro-dendritic contacts in the ventrolateral dendritic bundle in the cat S1 spinal cord segment: an electron microscopic study. Exp Brain Res 97 (1993) 1-12
43. Ranson R.N., Santer R.M., and Watson A.H. The relationship between serotonin, dopamine beta hydroxylase and GABA immunoreactive inputs and spinal preganglionic neurones projecting to the major pelvic ganglion of Wistar rats. Neuroscience 141 (2006) 1935-1949
44. Rash J.E., Yasumura T., and Dudek F.E. Ultrastructure, histological distribution, and freeze-fracture immunocytochemistry of gap junctions in rat brain and spinal cord. Cell Biol Int 22 (1998) 731-749
45. Santer R.M., Dering M.A., Ranson R.N., Waboso H.N., and Watson A.H. Differential susceptibility to ageing of rat preganglionic neurones projecting to the major pelvic ganglion and of their afferent inputs. Auton Neurosci 96 (2002) 73-81
46. Shupliakov O., Örnung G., Brodin L., Ulfhake B., Ottersen O.P., Storm-Mathisen J., and Cullheim S. Immunocytochemical localization of amino acid neurotransmitter candidates in the ventral horn of the cat spinal cord: a light microscopic study. Exp Brain Res 96 (1993) 404-418
47. Thomson T.D., and Franz D.N. Amino acid and monoamine inhibition of sacral parasympathetic preganglionic neurons. Prog Clin Bio Res 68 (1981) 181-189
48. Todd A.J., Hughes D.I., Polgár E., Nagy G.G., Mackie M., Ottersen O.P., and Maxwell D.J. The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur J Neurosci 17 (2003) 13-27
49. Ulfhake B. A morphometric study of the soma, first-order dendrites and proximal axon of cat lumbar alpha-motoneurones intracellularly labelled with HRP. Exp Brain Res 56 (1984) 327-334
50. Vizzard M.A. Alterations in neuropeptide expression in lumbosacral bladder pathways following chronic cystitis. J Chem Neuroanat 21 (2001) 125-138
51. Walberg F. Elongated vesicles in terminal boutons of the central nervous system, a result of aldehyde fixation. Acta Anat 65 (1966) 224-235
52. Wang H.F., Shortland P., Park M.J., and Grant G. Retrograde and transganglionic transport of horseradish peroxidase-conjugated cholera toxin B subunit, wheatgerm agglutinin and isolectin B4 from Griffonia simplicifolia I in primary afferent neurons innervating the rat urinary bladder. Neuroscience 87 (1998) 275-288
53. Wong W.C., and Tan C.K. The fine structure of the intermediolateral nucleus of the spinal cord of the monkey (Macaca fascicularis). J Anat 130 (1980) 263-277
54. Zvarova K., Murray E., and Vizzard M.A. Changes in galanin immunoreactivity in rat lumbosacral spinal cord and dorsal root ganglia after spinal cord injury. J Comp Neurol 475 (2004) 590-603
55. Zvarova K., Dunleavy J.D., and Vizzard M.A. Changes in pituitary adenylate cyclase activating polypeptide expression in urinary bladder pathways after spinal cord injury. Exp Neurol 192 (2005) 46-59