Morphological and electrophysiological features of motor neurons and putative interneurons in the dorsal vagal complex of rats and mice

Brain Research

Volumn 1291, Issue , 2009, Pages 40-52

  Gao, Hong ^a,d   Glatzer, Nicholas R ^a   Williams, Kevin W ^b   Derbenev, Andrei V ^a,d   Liu, Dan ^a   Smith, Bret N ^a,b,c,d  

^a Tulane University   (United States)

^b TULANE UNIVERSITY   (United States)

^c TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF KENTUCKY   (United States)

Author keywords

GABA; Morphology; Patch clamp; PRV; Solitarius; Vagus

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; FLUOROGOLD;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN STEM; CELL STRUCTURE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; INTERNEURON; MALE; MOTONEURON; MOUSE; NONHUMAN; PATCH CLAMP; PREGANGLIONIC NERVE; PRIORITY JOURNAL; RAT; SOLITARY TRACT NUCLEUS; VAGUS NERVE DORSAL NUCLEUS;

ANIMALS; AXONS; BRAIN STEM; CELL COUNT; DENDRITES; DENDRITIC SPINES; FLUORESCENT DYES; GAMMA-AMINOBUTYRIC ACID; IMAGE PROCESSING, COMPUTER-ASSISTED; INTERNEURONS; LYSINE; MALE; MEMBRANE POTENTIALS; MICE; MICE, TRANSGENIC; MOTOR NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; STOMACH; SYNAPSES; VAGUS NERVE;

DASHEEN MOSAIC VIRUS; MUS; MUS MUSCULUS; RATTUS; SUID HERPESVIRUS 1;

EID: 69249209643     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.07.024     Document Type: Article

References (55)

1. Bailey T.W., Appleyard S.M., Jin Y.H., and Andresen M.C. Organization and properties of GABAergic neurons in solitary tract nucleus (NTS). J. Neurophysiol. 99 (2008) 1712-1722
2. Banfield B.W., Kaufman J.D., Randall J.A., and Pickard G.E. Development of pseudorabies virus strains expressing red fluorescent proteins: new tools for multisynaptic labeling applications. J. Virol. 77 (2003) 10106-10112
3. Blessing W.W. Distribution of glutamate decarboxylase-containing neurons in rabbit medulla oblongata with attention to intramedullary and spinal projections. Neuroscience 37 (1990) 171-185
4. Blessing W.W., Oertel W.H., and Willoughby J.O. Glutamic acid decarboxylase immunoreactivity is present in perikarya of neurons in nucleus tractus solitarius of rat. Brain Res. 322 (1984) 346-350
5. Browning K.N., Renehan W.E., and Travagli R.A. Electrophysiological and morphological heterogeneity of rat dorsal vagal neurones which project to specific areas of the gastrointestinal tract. J. Physiol. 517 Pt 2 (1999) 521-532
6. Browning K.N., Coleman F.H., and Travagli R.A. Characterization of pancreas-projecting rat dorsal motor nucleus of vagus neurons. Am. J. Physiol. Gastrointest. Liver Physiol. 288 (2005) G950-G955
7. Campbell R.E., Tour O., Palmer A.E., Steinbach P.A., Baird G.S., Zacharias D.A., and Tsien R.Y. A monomeric red fluorescent protein. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 7877-7882
8. Card J.P. Exploring brain circuitry with neurotropic viruses: new horizons in neuroanatomy. Anat. Rec. 253 6 (1998) 176-185
9. Card J.P., Rinaman L., Schwaber J.S., Miselis R.R., Whealy M.E., Robbins A.K., and Enquist L.W. Neurotropic properties of pseudorabies virus: uptake and transneuronal passage in the rat central nervous system. J. Neurosci. 10 (1990) 1974-1994
10. Card J.P., Rinaman L., Lynn R.B., Lee B.H., Meade R.P., Miselis R.R., and Enquist L.W. Pseudorabies virus infection of the rat central nervous system: ultrastructural characterization of viral replication, transport, and pathogenesis. J. Neurosci. 13 6 (1993) 2515-2539
11. Ch'ng T.H., Spear P.G., Struyf F., and Enquist L.W. Glycoprotein D-independent spread of pseudorabies virus infection in cultured peripheral nervous system neurons in a compartmented system. J. Virol. 81 (2007) 10742-10757
12. Davis S.F., Williams K.W., Xu W., Glatzer N.R., and Smith B.N. Selective enhancement of synaptic inhibition by hypocretin (orexin) in rat vagal motor neurones: implications for autonomic regulation. J. Neurosci. 23 (2003) 3844-3854
13. Davis S.F., Derbenev A.V., Williams K.W., Glatzer N.R., and Smith B.N. Convergent excitatory and inhibitory local circuit input to the rat dorsal motor nucleus of the vagus originating from the nucleus tractus solitarius. Brain Res. 1017 (2004) 208-217
14. Derbenev, A.V., Stuart, T.C., Smith, B.N., 2004. Cannabinoids suppress synaptic input to neurones of the rat dorsal motor nucleus of the vagus nerve. J. Physiol. 559(Pt 3):923-38. Epub 2004 Jul 22, 2004.
15. Enquist L.W., Husak P.J., Banfield B.W., and Smith G.A. Infection and spread of alphaherpesviruses in the nervous system. Adv. Virus Res. 51 (1998) 237-347
16. Fox E.A., and Powley T.L. Morphology of identified preganglionic neurons in the dorsal motor nucleus of the vagus. J. Comp. Neurol. 322 1 (1992) 79-98
17. Fogel R., Zhang X., and Renehan W.E. 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 1 (1996) 78-91
18. Fong A.Y., Stornetta R.L., Foley C.M., and Potts J.T. Immunohistochemical localization of GAD67-expressing neurons and processes in the rat brainstem: subregional distribution in the nucleus tractus solitarius. J. Comp. Neurol. 493 2 (2005) 274-290
19. Gillis, R.A., Quest, J.A., Pagani, F.D., and Norman, W.P., 1989 Control centers in the central nervous system for regulating gastrointestinal motility. In: Handbook of Physiology. The Gastrointestinal System. Motility and Circulation. Bethesda, MD: Am. Physiol. Soc, 1989, sect. 6, vol. I, pt. 1, chapt. 17, p. 621-683.
20. Glatzer N.R., and Smith B.N. Modulation of synaptic transmission in the rat nucleus of the solitary tract by endomorphin-1. J. Neurophysiol. 93 5 (2005) 2530-2540
21. Glatzer N.R., Hasney C.P., Bhaskaran M.D., and Smith B.N. Synaptic and morphological properties in vitro of premotor rat nucleus tractus solitarius neurones labelled transneuronally from the stomach. J. Comp. Neurol. 464 (2003) 525-539
22. Glatzer N.R., Derbenev A.V., Banfield B.W., and Smith B.N. Endomorphin-1 modulates intrinsic inhibition in the dorsal vagal complex. J. Neurophysiol. 98 (2007) 1591-1599
23. Grabauskas G., and Moises H.C. Gastrointestinal-projecting neurones in the dorsal motor nucleus of the vagus exhibit direct and viscerotopically organized sensitivity to orexin. J. Physiol. 549 (2003) 37-56
24. Grabauskas G., Zhou S.Y., Das S., Lu Y., Owyang C., and Moises H.C. Prolactin-releasing peptide affects gastric motor function in rat by modulating synaptic transmission in the dorsal vagal complex. J. Physiol. 561 (2004) 821-839
25. Guillery R.W. On counting and counting errors. J. Comp. Neurol. 447 (2002) 1-7
26. Herman M.A., Cruz M.T., Sahibzada N., Verbalis J., and Gillis R.A. GABA signaling in the nucleus tractus solitarius sets the level of activity in dorsal motor nucleus of the vagus cholinergic neurons in the vagovagal circuit. Am. J. Physiol. Gastrointest. Liver Physiol. 296 (2009) G101-G111
27. Huang X.F., Tork I., and Paxinos G. Dorsal motor nucleus of the vagus nerve: a cyto- and chemoarchitectonic study in the human. J. Comp. Neurol. 330 (1993) 158-182
28. Irnaten M., Neff R.A., Wang J., Loewy A.D., Mettenleiter T.C., and Mendelowitz D. Activity of cardiorespiratory networks revealed by transsynaptic virus expressing GFP. J. Neurophysiol. 85 (2001) 435-438
29. Izzo P.N., Sykes R.M., and Spyer K.M. gamma-Aminobutyric acid immunoreactive structures in the nucleus tractus solitarius: a light and electron microscopic study. Brain Res. 591 (1992) 69-78
30. Jarvinen M.K., and Powley T.L. Dorsal motor nucleus of the vagus neurons: a multivariate taxonomy. J. Comp. Neurol. 403 (1999) 359-377
31. Jons A., and Mettenleiter T.C. Green fluorescent protein expressed by recombinant pseudorabies virus as an in vivo marker for viral replication. J. Virol. Methods 66 (1997) 283-292
32. Kawai Y., and Senba E. Electrophysiological and morphological characterization of cytochemically-defined neurons in the caudal nucleus of tractus solitarius of the rat. Neuroscience 89 (1999) 1347-1355
33. Leong S.K., and Ling E.A. Labelling neurons with fluorescent dyes administered via intravenous, subcutaneous or intraperitoneal route. J. Neurosci. Methods 32 (1990) 15-23
34. McLean J.H., and Hopkins D.A. A light and electron microscopic study of the dorsal motor nucleus of the vagus nerve in the cat. J. Comp. Neurol. 195 (1981) 157-175
35. McLean J.H., and Hopkins D.A. Ultrastructural identification of labeled neurons in the dorsal motor nucleus of the vagus nerve following injections of horseradish peroxidase into the vagus nerve and brainstem. J. Comp. Neurol. 206 (1982) 243-252
36. Oliva A.A., Jiang M., Lam T., Smith K.L., and Swann J.W. Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J. Neurosci. 20 (2000) 3354-3368
37. Paxinos G., Carrive P., Wang H., and Wang P. Chemoarchitectonic atlas of the rat brainstem (1999), Academic Press, San Diego
38. Pickard G.E., Smeraski C.A., Tomlinson C.C., Banfield B.W., Kaufman J., Wilcox C.L., Enquist L.W., and Sollars P.J. 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 (2002) 2701-2710
39. Rinaman L., Card J.P., and Enquist L.W. Spatiotemporal responses of astrocytes, ramified microglia, and brain macrophages to central neuronal infection with pseudorabies virus. J. Neurosci. 13 (1993) 685-702
40. Rogers R.C., McTigue D.M., and Herman G.E. Vagal control of digestion: modulation by central neuronal and peripheral endocrine factors. Neurosci. Biobehav. Rev. 20 (1996) 57-66
41. Smith B.N., Dou P., Barber W.D., and Dudek F.E. Vagally evoked synaptic currents in the immature rat nucleus tractus solitarii in an intact in vitro preparation. J. Physiol. (Lond) 512 (1998) 149-162
42. Smith B.N., Banfield B.W., Smeraski C.A., Wilcox C.L., Dudek F.E., and Enquist L.W. Pickard GE. 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 (2000) 9264-9269
43. Smith B.N., Davis S.F., van den Pol A.N., and Xu W. Selective enhancement of excitatory synaptic activity in the rat nucleus tractus solitarius by hypocretin 2. Neuroscience 115 (2002) 707-714
44. Strack A.M., Sawyer W.B., Platt K.B., and Loewy A.D. CNS cell groups regulating the sympathetic outflow to adrenal gland as revealed by transneuronal cell body labeling with pseudorabies virus. Brain Res. 491 (1989) 274-296
45. Streefland C., Maes F.W., and Bohus B. Autonomic brainstem projections to the pancreas: a retrograde transneuronal viral tracing study in the rat. J. Auton. Nerv. Syst. 74 (1998) 71-81
46. Tanaka I., Ezure K., and Kondo M. Distribution of glycine transporter 2 mRNA-containing neurons in relation to glutamic acid decarboxylase mRNA-containing neurons in rat medulla. Neurosci. Res. 47 (2003) 139-151
47. Travagli R.A., and Rogers R.C. Receptors and transmission in the brain-gut axis: potential for novel therapies. V. Fast and slow extrinsic modulation of dorsal vagal complex circuits. Am. J. Physiol. Gastrointest. Liver Physiol. 281 (2001) G595-G601
48. Travagli R.A., Gillis R.A., Rossiter C.D., and Vicini S. Glutamate and GABA-mediated synaptic currents in neurons of the rat dorsal motor nucleus of the vagus. Am. J. Physiol. 260 (1991) G531-G536
49. Travagli R.A., Hermann G.E., Browning K.N., and Rogers R.C. Brainstem circuits regulating gastric function. Annu. Rev. Physiol. 68 (2006) 279-305
50. Valenzuela I.M., Browning K.N., and Travagli R.A. Morphological differences between planes of section do not influence the electrophysiological properties of identified rat dorsal motor nucleus of the vagus neurons. Brain Res. 1003 (2004) 54-60
51. Wang J., Irnaten M., Neff R.A., Venkatesan P., Evans C., Loewy A.D., Mettenleiter T.C., and Mendelowitz D. Synaptic and neurotransmitter activation of cardiac vagal neurons in the nucleus ambiguus. Ann. N.Y. Acad. Sci. 940 (2001) 237-246
52. Williams K.W., and Smith B.N. Rapid inhibition of neural excitability in the nucleus tractus solitarii by leptin: implications for ingestive behaviour. J. Physiol. (Lond) 573 (2006) 395-412
53. Williams K.W., Zsombok A., and Smith B.N. Rapid inhibition of neurons in the dorsal motor nucleus of the vagus by leptin. Endocrinology 148 (2007) 1868-1881
54. Zhang X., Renehan W.E., and Fogel R. Neurons in the vagal complex of the rat respond to mechanical and chemical stimulation of the GI tract. Am. J. Physiol. 274 (1998) G331-G341
55. Zhang X., Jiang C., Tan Z., and Fogel R. Vagal motor neurons in rats respond to noxious and physiological gastrointestinal distention differentially. Eur. J. Neurosci. 16 (2002) 2027-2038