Synaptic and morphologic properties in vitro of premotor rat nucleus tractus solitarius neurons labeled transneuronally from the stomach

Journal of Comparative Neurology

Volumn 464, Issue 4, 2003, Pages 525-539

  Glatzer, Nicholas R ^a   Hasney, Christian P ^a   Bhaskaran, Muthu D ^a   Smith, Bret N ^a,b  

^a Tulane University   (United States)

^b TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Gastric; GFP; Parasympathetic; Patch clamp; Pseudorabies virus; Vagus

Indexed keywords

BIOCYTIN; GREEN FLUORESCENT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CHOLINERGIC SYSTEM; DENDRITE; IN VITRO STUDY; MALE; MORPHOLOGY; NERVE CELL; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; SOLITARY TRACT NUCLEUS; STOMACH; SYNAPSE; VAGUS NERVE; VOLTAGE CLAMP;

ANIMALS; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIALS; GREEN FLUORESCENT PROTEINS; HERPESVIRUS 1, SUID; INDICATORS AND REAGENTS; LUMINESCENT PROTEINS; LYSINE; MALE; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; PSEUDORABIES; RATS; RATS, SPRAGUE-DAWLEY; SOLITARY NUCLEUS; STOMACH; SYNAPSES; TIME FACTORS;

EID: 0041419671     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10831     Document Type: Article

References (62)

1. Agarwal SK, Calaresu FR. 1990. Reciprocal connections between nucleus tractus solitarii and rostral ventrolateral medulla. Brain Res 523:305-308.
2. Altschuler SM, Bao XM, Bieger D, Hopkins DA, Miselis RR. 1989. Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol 283:248-268.
3. Andresen MC, Yang MY. 1990. Non-NMDA receptors mediate sensory afferent synaptic transmission in medial nucleus tractus solitarius. Am J Physiol 259:H1307-H1311.
4. Andresen MC, Doyle MW, Jin YH, Bailey TW. 2001. Cellular mechanisms of baroreceptor integration at the nucleus tractus solitarius. Ann N Y Acad Sci 940:132-141.
5. Barber WD, Yuan CS, Cammarata BJ. 1990. Vagal interactions on brain stem neurons receiving input from the proximal stomach in cats. Am J Physiol 258:G321-G327.
6. Bonham AC, Coles SK, McCrimmon DR. 1993. Pulmonary stretch receptor afferents activate excitatory amino acid receptors in the nucleus tractus solitarii in rats. J Physiol 464:725-745.
7. Browning KN, Renehan WE, Travagli RA. 1999. Electrophysiological and morphological heterogeneity of rat dorsal vagal neurones which project to specific areas of the gastrointestinal tract. J Physiol 517:521-532.
8. Buckmaster PS, Dudek FE. 1997. Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J Comp Neurol 385:385-404.
9. Buijs RM, Chun SJ, Niijima A, Romijn HJ, Nagai K. 2001. Parasympathetic and sympathetic control of the pancreas: a role for the suprachiasmatic nucleus and other hypothalamic centers that are involved in the regulation of food intake. J Comp Neurol 431:405-423.
10. Card JP, Rinaman L, Schwaber JS, Miselis RR, Whealy ME, Robbins AK, Enquist LW. 1990. Neurotropic properties of pseudorabies virus: uptake and transneuronal passage in the rat central nervous system. J Neurosci 10:1974-1994.
11. Card JP, Rinaman L, Lynn RB, Lee BH, Meade RP, Miselis RR, Enquist LW. 1993. Pseudorabies virus infection of the rat central nervous system: ultrastructural characterization of viral replication, transport, and pathogenesis. J Neurosci 13:2515-2539.
12. Champagnat J, Denavit-Saubie M, Grant K, Shen KF. 1986. Organization of synaptic transmission in the mammalian solitary complex, studied in vitro. J Physiol 381:551-573.
13. Chen CY, Ling EH, Horowitz JM, Bonham AC. 2002. Synaptic transmission in nucleus tractus solitarius is depressed by group II and III but not group I presynaptic metabotropic glutamate receptors in rats. J Physiol 538:773-786.
14. Davis SF, Williams KW, Xu W, Glatzer NR, Smith BN. 2003. Selective enhancement of synaptic inhibition by hypocretin (orexin) in rat vagal motor neurons: implications for autonomic regulation. J Neurosci 23: 3844-3854.
15. Dekin MS, Getting PA. 1987. In vitro characterization of neurons in the ventral part of the nucleus tractus solitarius. I. Identification of neuronal types and repetitive firing properties. J Neurophysiol 58:195-214.
16. Dekin MS, Getting PA, Johnson SM. 1987. In vitro characterization of neurons in the ventral part of the nucleus tractus solitarius. II. Ionic basis for repetitive firing patterns. J Neurophysiol 58:215-229.
17. Deuchars J, Li YW, Kasparov S, Paton JF. 2000. Morphological and electrophysiological properties of neurones in the dorsal vagal complex of the rat activated by arterial baroreceptors. J Comp Neurol 417:233-249.
18. Doyle MW, Andresen MC. 2001. Reliability of monosynaptic sensory transmission in brain stem neurons in vitro. J Neurophysiol 85:2213-2223.
19. Felder RB, Mifflin SW. 1988. Modulation of carotid sinus afferent input to nucleus tractus solitarius by parabrachial nucleus stimulation. Circ Res 63:35-49.
20. Fogel R, Zhang X, Renehan WE. 1996. Relationships between the morphology and function of gastric and intestinal distention-sensitive neurons in the dorsal motor nucleus of the vagus. J Comp Neurol 364:78-91.
21. Fortin G, Champagnat J. 1993. Spontaneous synaptic activities in rat nucleus tractus solitarius neurons in vitro: evidence for re-excitatory processing. Brain Res 630:125-135.
22. Fukuda J, Kurata T. 1981. Loss of membrane excitability after herpes simplex virus infection in tissue-cultured nerve cells from adult mammals. Brain Res 211:235-241.
23. Guillery RW. 2002. On counting and counting errors. J Comp Neurol 447:1-7.
24. Hestrin S, Nicoll RA, Perkel DJ, Sah P. 1990. Analysis of excitatory synaptic action in pyramidal cells using whole-cell recording from rat hippocampal slices. J Physiol 422:203-225.
25. Inglis FM, Furia F, Zuckerman KE, Strittmatter SM, Kalb RG. 1998. The role of nitric oxide and NMDA receptors in the development of motor neuron dendrites. J Neurosci 18:10493-10501.
26. Irnaten M, Wang J, Mendelowitz D. 2001. Firing properties of identified superior laryngeal neurons in the nucleus ambiguus in the rat. Neurosci Lett 303:1-4.
27. Jons A, Mettenleiter TC. 1997. Green fluorescent protein expressed by recombinant pseudorabies virus as an in vivo marker for viral replication. J Virol Methods 66:283-292.
28. Kalia M, Sullivan JM. 1982. Brainstem projections of sensory and motor components of the vagus nerve in the rat. J Comp Neurol 211:248-265.
29. Kawai Y, Senba E. 1996. Organization of excitatory and inhibitory local networks in the caudal nucleus of tractus solitarius of rats revealed in in vitro slice preparation. J Comp Neurol 373:309-321.
30. Kawai Y, Senba E. 2000. Postnatal differentiation of local networks in the nucleus of the tractus solitarius. Neuroscience 100:109-114.
31. King MS, Bradley RM. 1994. Relationship between structure and function of neurons in the rat rostral nucleus tractus solitarii. J Comp Neurol 344:50-64.
32. Kiraly M, Dolivo M. 1982. Alteration of the electrophysiological activity in sympathetic ganglia infected with a neurotropic virus. I. Presynaptic origin of the spontaneous bioelectric activity. Brain Res 240:43-54.
33. la Fleur SE, Kalsbeek A, Wortel J, Buijs RM. 2000. Polysynaptic neural pathways between the hypothalamus, including the suprachiasmatic nucleus, and the liver. Brain Res 871:50-56.
34. Loewy AD, Haxhiu MA. 1993. CNS cell groups projecting to pancreatic parasympathetic preganglionic neurons. Brain Res 620:323-330.
35. Mayer ML, James MH, Russell RJ, Kelly JS, Wise JC, Pasternak CA. 1985. Spontaneous electrical activity induced by herpes virus infection in rat sensory neuron cultures. Brain Res 341:360-364.
36. Miles R. 1986. Frequency dependence of synaptic transmission in nucleus of the solitary tract in vitro. J Neurophysiol 55:1076-1090.
37. Paton JF, Li YW, Deuchars J, Kasparov S. 2000. Properties of solitary tract neurons receiving inputs from the sub-diaphragmatic vagus nerve. Neuroscience 95:141-153.
38. Paxinos G, Carrive P, Wang H, Wang P. 1999. Chemoarchitectonic atlas of the rat brainstem. San Diego: Academic Press.
39. Pickard GE, Smeraski CA, Tomlinson CC, Banfield BW, Kaufman J, Wilcox CL, Enquist LW, Sollars PJ. 2002. Intravitreal injection of the attenuated pseudorabies virus PRV Bartha results in infection of the hamster suprachiasmatic nucleus only by retrograde transsynaptic transport via autonomic circuits. J Neurosci 22:2701-2710.
40. Renehan WE, Jin Z, Zhang X, Schweitzer L. 1994. Structure and function of gustatory neurons in the nucleus of the solitary tract. I. A classification of neurons based on morphological features. J Comp Neurol 347:531-544.
41. Renehan WE, Jin Z, Zhang X, Schweitzer L. 1996. Structure and function of gustatory neurons in the nucleus of the solitary tract: II. Relationships between neuronal morphology and physio]ogy. J Comp Neurol 367:205-221.
42. Rinaman L, Card JP, Schwaber JS, Miselis RR. 1989. Ultrastructural demonstration of a gastric monosynaptic vagal circuit in the nucleus of the solitary tract in rat. J Neurosci 9:1985-1996.
43. Rinaman L, Card JP, Enquist LW. 1993. Spatiotemporal responses of astrocytes, ramified microglia, and brain macrophages to central neuronal infection with pseudorabies virus. J Neurosci 13:685-702.
44. Rogers RC, McCann MJ. 1993. Intramedu]lary connections of the gastric region in the solitary nucleus: a biocytin histochemical tracing study in the rat. J Auton Nerv Syst 42:119-130.
45. Russ JC. 2000. Practical stereology. New York: Plenum.
46. Sawchenko PE, Swanson LW. 1982. The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res 257:275-325.
47. Schweitzer L, Renehan WE. 1997. The use of cluster analysis for cell typing. Brain Res Brain Res Protoc 1:100-108.
48. Seagard JL, Dean C, Hopp FA. 1999. Role of glutamate receptors in transmission of vagal cardiac input to neurones in the nucleus tractus solitarii in dogs. J Physiol 520:243-253.
49. Shapiro RE, Miselis RR. 1985. The central organization of the vagus nerve innervating the stomach of the rat. J Comp Neurol 238:473-488.
50. Smith BN, Armstrong WE. 1990. Tuberal supraoptic neurons. I. Morphological and electrophysiological characteristics observed with intracellular recording and biocytin filling in vitro. Neuroscience 38:469-483.
51. Smith BN, Banfield BW, Smeraski CA, Wilcox CL, Dudek FE, Enquist LW, Pickard GE. 2000. Pseudorabies virus expressing enhanced green fluorescent protein: a tool for in vitro electrophysiological analysis of transsynaptically labeled neurons in identified central nervous system circuits. Proc Natl Acad Sci U S A 97:9264-9269.
52. Smith BN, Dou P, Barber WD, Dudek FE. 1998. Vagally evoked synaptic currents in the immature rat nucleus tractus solitarii in an intact in vitro preparation. J Physiol 512:149-162.
53. Smith BN, Davis SF, van den Pol AN, Xu W. 2002. Selective enhancement of excitatory synaptic activity in the rat nucleus tractus solitarius by hypocretin 2. Neuroscience 115:707-714.
54. Spyer KM, Donoghue S, Felder RB, Jordan D. 1984. Processing of afferent inputs in cardiovascular control. Clin Exp Hypertens A 6:173-184.
55. Standish A, Enquist LW, Miselis RR, Schwaber JS. 1995. Dendritic morphology of cardiac related medullary neurons defined by circuit-specific infection by a recombinant pseudorabies virus expressing beta-galactosidase. J Neurovirol 1:359-368.
56. Stern JE, Armstrong WE. 1998. Reorganization of the dendritic trees of oxytocin and vasopressin neurons of the rat supraoptic nucleus during lactation. J Neurosci 18:841-853.
57. Strack AM, Sawyer WB, Hughes JH, Platt KB, Loewy AD. 1989. A general pattern of CNS innervation of the sympathetic outflow demonstrated by transneuronal pseudorabies viral infections. Brain Res 491:156-162.
58. Travagli RA, Gillis RA, Rossiter CD, Vicini S. 1991. Glutamate and GABA-mediated synaptic currents in neurons of the dorsal motor nucleus of the vagus. Am J Physiol 260:G531-G536.
59. Vincent A, Tell F. 1999. Postnatal development of rat nucleus tractus solitarius neurons: morphological and electrophysiological evidence. Neuroscience 93:293-305.
60. Zhang W, Mifflin SW. 1993. Excitatory amino acid receptors within NTS mediate arterial chemoreceptor reflexes in rats. Am J Physiol 265(Pt 2):H770-H773.
61. Zhang X, Fogel R, Renehan WE. 1995. Relationships between the morphology and function of gastric- and intestine-sensitive neurons in the nucleus of the solitary tract. J Comp Neurol 363:37-52.
62. Zhang X, Renehan WE, Fogel R. 1998. Neurons in the vagal complex of the rat respond to mechanical and chemical stimulation of the GI tract. Am J Physiol 274:G331-G341.