Withdrawal and restoration of central vagal afferents within the dorsal vagal complex following subdiaphragmatic vagotomy

Journal of Comparative Neurology

Volumn 521, Issue 15, 2013, Pages 3584-3599

  Peters, James H ^a   Gallaher, Zachary R ^a   Ryu, Vitaly ^b   Czaja, Krzysztof ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Axotomy; Nucleus of the solitary tract; Synaptic plasticity; Vagus nerve

Indexed keywords

GLUTAMIC ACID;

ANIMAL EXPERIMENT; ARTICLE; BARIATRIC SURGERY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL PLASTICITY; NERVE DEGENERATION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; STOMACH BYPASS; SUBDIAPHRAGMATIC VAGOTOMY; SYNAPSE VESICLE; TISSUE FIXATION; VAGOTOMY; VAGUS NERVE;

AXOTOMY; NUCLEUS OF THE SOLITARY TRACT; SYNAPTIC PLASTICITY; VAGUS NERVE;

ANIMALS; AXONS; BIOTIN; DEXTRANS; DIAPHRAGM; ELECTROPHYSIOLOGICAL PROCESSES; FLUORESCENT DYES; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MALE; NERVE REGENERATION; NEURONS, AFFERENT; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SOLITARY NUCLEUS; SYNAPSES; SYNAPSINS; SYNAPTOPHYSIN; TISSUE FIXATION; TUBULIN; VAGOTOMY; VAGUS NERVE;

EID: 84883005882     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23374     Document Type: Article

References (67)

1. Aldskogius H, Arvidsson J. 1978. Nerve cell degeneration and death in the trigeminal ganglion of the adult rat following peripheral nerve transection. J Neurocytol 7:229-250.
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, Mendelowitz D. 1996. Sensory afferent neurotransmission in caudal nucleus tractus solitarius--common denominators. Chem Senses 21:387-395.
4. Bailey TW, Jin YH, Doyle MW, Smith SM, Andresen MC. 2006. Vasopressin inhibits glutamate release via two distinct modes in the brainstem. J Neurosci 26:6131-6142.
5. Bailey TW, Appleyard SM, Jin YH, Andresen MC. 2008. Organization and properties of GABAergic neurons in solitary tract nucleus (NTS). J Neurophysiol 99:1712-1722.
6. Berthoud HR, Shin AC, Zheng H. 2011. Obesity surgery and gut-brain communication. Physiol Behav 105:106-119.
7. Bowe CM, Evans NH, Vlacha V. 1992. Progressive morphological abnormalities observed in rat spinal motor neurons at extended intervals after axonal regeneration. J Comp Neurol 321:576-590.
8. Brannstrom T, Kellerth JO. 1999. Recovery of synapses in axotomized adult cat spinal motoneurons after reinnervation into muscle. Exp Brain Res 125:19-27.
9. Calhoun ME, Jucker M, Martin LJ, Thinakaran G, Price DL, Mouton PR. 1996. Comparative evaluation of synaptophysin-based methods for quantification of synapses. J Neurocytol 25:821-828.
10. Chen DH. 1978. Qualitative and quantitative study of synaptic displacement in chromatolyzed spinal motoneurons of the cat. J Comp Neurol 177:635-664.
11. Cohen RV, Pinheiro JC, Schiavon CA, Salles JE, Wajchenberg BL, Cummings DE. 2012. Effects of gastric bypass surgery in patients with type 2 diabetes and only mild obesity. Diabetes Care 35:1420-1428.
12. Czaja K, Burns GA, Ritter RC. 2008. Capsaicin-induced neuronal death and proliferation of the primary sensory neurons located in the nodose ganglia of adult rats. Neuroscience 154:621-630.
13. Devor M, Wall PD. 1981. Plasticity in the spinal cord sensory map following peripheral nerve injury in rats. J Neurosci 1:679-684.
14. Doggrell SA, Chan V. 2012. Bariatric surgery or medicine for type 2 diabetes? Expert Opin Pharmacother 13:2249-2253.
15. Doyle MW, Andresen MC. 2001. Reliability of monosynaptic sensory transmission in brain stem neurons in vitro. J Neurophysiol 85:2213-2223.
16. Doyle MW, Bailey TW, Jin YH, Appleyard SM, Low MJ, Andresen MC. 2004. Strategies for cellular identification in nucleus tractus solitarius slices. J Neurosci Methods 137:37-48.
17. Emirandetti A, Simoes GF, Zanon RG, Oliveira AL. 2010. Spinal motoneuron synaptic plasticity after axotomy in the absence of inducible nitric oxide synthase. J Neuroinflammation 7:31.
18. Furness JB, Kunze WA, Clerc N. 1999. Nutrient tasting and signaling mechanisms in the gut. II. The intestine as a sensory organ: neural, endocrine, and immune responses. Am J Physiol 277:G922-G928.
19. Gallaher ZR, Ryu V, Larios RM, Sprunger LK, Czaja K. 2011. Neural proliferation and restoration of neurochemical phenotypes and compromised functions following capsaicin-induced neuronal damage in the nodose ganglion of the adult rat. Front Neurosci 5:12.
20. Gallaher ZR, Ryu V, Herzog T, Ritter RC, Czaja K. 2012. Changes in microglial activation within the hindbrain, nodose ganglia, and the spinal cord following subdiaphragmatic vagotomy. Neurosci Lett 513:31-36.
21. Gazula VR, Strumbos JG, Mei X, Chen H, Rahner C, Kaczmarek LK. 2010. Localization of Kv1.3 channels in presynaptic terminals of brainstem auditory neurons. J Comp Neurol 518:3205-3220.
22. Groves MJ, Christopherson T, Giometto B, Scaravilli F. 1997. Axotomy-induced apoptosis in adult rat primary sensory neurons. J Neurocytol 26:615-624.
23. Groves MJ, An SF, Giometto B, Scaravilli F. 1999. Inhibition of sensory neuron apoptosis and prevention of loss by NT-3 administration following axotomy. Exp Neurol 155:284-294.
24. Herde MK, Friauf E, Rust MB. 2010. Developmental expression of the actin depolymerizing factor ADF in the mouse inner ear and spiral ganglia. J Comp Neurol 518:1724-1741.
25. Hu J, Mata M, Hao S, Zhang G, Fink DJ. 2004. Central sprouting of uninjured small fiber afferents in the adult rat spinal cord following spinal nerve ligation. Eur J Neurosci 20:1705-1712.
26. Hunter DA, Moradzadeh A, Whitlock EL, Brenner MJ, Myckatyn TM, Wei CH, Tung TH, Mackinnon SE. 2007. Binary imaging analysis for comprehensive quantitative histomorphometry of peripheral nerve. J Neurosci Methods 166:116-124.
27. Jinno S, Yamada J. 2011. Using comparative anatomy in the axotomy model to identify distinct roles for microglia and astrocytes in synaptic stripping. Neuron Glia Biol 7:55-66.
28. Kavalali ET, Chung C, Khvotchev M, Leitz J, Nosyreva E, Raingo J, Ramirez DM. 2011. Spontaneous neurotransmission: an independent pathway for neuronal signaling? Physiology (Bethesda) 26:45-53.
29. Kim SK, Nabekura J. 2011. Rapid synaptic remodeling in the adult somatosensory cortex following peripheral nerve injury and its association with neuropathic pain. J Neurosci 31:5477-5482.
30. Laiwand R, Werman R, Yarom Y. 1987. Time course and distribution of motoneuronal loss in the dorsal motor vagal nucleus of guinea pig after cervical vagotomy. J Comp Neurol 256:527-537.
31. Lan CT, Hsu JC, Chang CN, Chuang HL, Ling EA. 2003. Synaptic remodeling in the dorsal motor nucleus of the vagus nerve following vagal-hypoglossal nerve anastomosis in the cat. J Comp Neurol 458:195-207.
32. Lancaster E, Oh EJ, Weinreich D. 2001. Vagotomy decreases excitability in primary vagal afferent somata. J Neurophysiol 85:247-253.
33. Li Y, Owyang C. 2003. Musings on the wanderer: what's new in our understanding of vago-vagal reflexes? V. Remodeling of vagus and enteric neural circuitry after vagal injury. Am J Physiol Gastrointest Liver Physiol 285:G461-G469.
34. Louis-Sylvestre J. 1983. Validation of tests of completeness of vagotomy in rats. J Auton Nerv Syst 9:301-314.
35. McDougall SJ, Peters JH, Andresen MC. 2009. Convergence of cranial visceral afferents within the solitary tract nucleus. J Neurosci 29:12886-12895.
36. Micheva KD, Busse B, Weiler NC, O'Rourke N, Smith SJ. 2010. Single-synapse analysis of a diverse synapse population: proteomic imaging methods and markers. Neuron 68:639-653.
37. Nachman-Clewner M, Townes-Anderson E. 1996. Injury-induced remodelling and regeneration of the ribbon presynaptic terminal in vitro. J Neurocytol 25:597-613.
38. Navarro X. 2009. Chapter 27 neural plasticity after nerve injury and regeneration. Int Rev Neurobiol 87:483-505.
39. Navarro X, Vivo M, Valero-Cabre A. 2007. Neural plasticity after peripheral nerve injury and regeneration. Prog Neurobiol 82:163-201.
40. Peters JH, McDougall SJ, Kellett DO, Jordan D, Llewellyn-Smith IJ, Andresen MC. 2008. Oxytocin enhances cranial visceral afferent synaptic transmission to the solitary tract nucleus. J Neurosci 28:11731-11740.
41. Peters JH, McDougall SJ, Fawley JA, Smith SM, Andresen MC. 2010. Primary afferent activation of thermosensitive TRPV1 triggers asynchronous glutamate release at central neurons. Neuron 65:657-669.
42. Peters JH, McDougall SJ, Fawley JA, Andresen MC. 2011. TRPV1 marks synaptic segregation of multiple convergent afferents at the rat medial solitary tract nucleus. PLoS ONE 6:e25015.
43. Phillips RJ, Powley TL. 2005. Plasticity of vagal afferents at the site of an incision in the wall of the stomach. Auton Neurosci 123:44-53.
44. Phillips RJ, Baronowsky EA, Powley TL. 2000. Regenerating vagal afferents reinnervate gastrointestinal tract smooth muscle of the rat. J Comp Neurol 421:325-346.
45. Phillips RJ, Baronowsky EA, Powley TL. 2003. Long-term regeneration of abdominal vagus: efferents fail while afferents succeed. J Comp Neurol 455:222-237.
46. Powley TL, Fox EA, Berthoud HR. 1987. Retrograde tracer technique for assessment of selective and total subdiaphragmatic vagotomies. Am J Physiol 253:R361-R370.
47. Purves D. 1975. Functional and structural changes in mammalian sympathetic neurones following interruption of their axons. J Physiol 252:429-463.
48. Ramer LM, van Stolk AP, Inskip JA, Ramer MS, Krassioukov AV. 2012. Plasticity of TRPV1-expressing sensory neurons mediating autonomic dysreflexia following spinal cord injury. Front Physiol 3:257.
49. Ronchi G, Ryu V, Fornaro M, Czaja K. 2012. Hippocampal plasticity after a vagus nerve injury in the rat. Neural Regen Res 7:1055-1063.
50. Ryu V, Gallaher Z, Czaja K. 2010. Plasticity of nodose ganglion neurons after capsaicin- and vagotomy-induced nerve damage in adult rats. Neuroscience 167:1227-1238.
51. Schwartz GJ. 2006. Integrative capacity of the caudal brainstem in the control of food intake. Philos Trans R Soc Lond B Biol Sci 361:1275-1280.
52. Shoudai K, Peters JH, McDougall SJ, Fawley JA, Andresen MC. 2010. Thermally active TRPV1 tonically drives central spontaneous glutamate release. J Neurosci 30:14470-14475.
53. Soiza-Reilly M, Commons KG. 2011. Quantitative analysis of glutamatergic innervation of the mouse dorsal raphe nucleus using array tomography. J Comp Neurol 519:3802-3814.
54. Sonoda EY, Gomes da SS, Arida RM, Giglio PN, Margarido NF, Martinez CA, Pansani AP, Maciel RS, Cavalheiro EA, Scorza FA. 2011. Hippocampal plasticity in rats submitted to a gastric restrictive procedure. Nutr Neurosci 14:181-185.
55. Sumner BE, Sutherland FI. 1973. Quantitative electron microscopy on the injured hypoglossal nucleus in the rat. J Neurocytol 2:315-328.
56. Sun T, Xiao HS, Zhou PB, Lu YJ, Bao L, Zhang X. 2006. Differential expression of synaptoporin and synaptophysin in primary sensory neurons and up-regulation of synaptoporin after peripheral nerve injury. Neuroscience 141:1233-1245.
57. Sunico CR, Portillo F, Gonzalez-Forero D, Moreno-Lopez B. 2005. Nitric-oxide-directed synaptic remodeling in the adult mammal CNS. J Neurosci 25:1448-1458.
58. Svensson M, Aldskogius H. 1992. The effect of axon injury on microtubule-associated proteins MAP2, 3 and 5 in the hypoglossal nucleus of the adult rat. J Neurocytol 21:222-231.
59. Svensson M, Tornqvist E, Aldskogius H, Cova JL. 1991. Synaptic detachment from hypoglossal neurons after different types of nerve injury in the cat. J Hirnforsch 32:547-552.
60. Swartz JB, Weinreich D. 2009. Influence of vagotomy on monosynaptic transmission at second-order nucleus tractus solitarius synapses. J Neurophysiol 102:2846-2855.
61. Tandrup T, Woolf CJ, Coggeshall RE. 2000. Delayed loss of small dorsal root ganglion cells after transection of the rat sciatic nerve. J Comp Neurol 422:172-180.
62. Tiraihi T, Rezaie MJ. 2004. Synaptic lesions and synaptophysin distribution change in spinal motoneurons at early stages following sciatic nerve transection in neonatal rats. Brain Res Dev Brain Res 148:97-103.
63. Tseng GF, Hu ME. 1996. Axotomy induces retraction of the dendritic arbor of adult rat rubrospinal neurons. Acta Anat (Basel) 155:184-193.
64. Vestergaard S, Tandrup T, Jakobsen J. 1997. Effect of permanent axotomy on number and volume of dorsal root ganglion cell bodies. J Comp Neurol 388:307-312.
65. White FA, Kocsis JD. 2002. A-fiber sprouting in spinal cord dorsal horn is attenuated by proximal nerve stump encapsulation. Exp Neurol 177:385-395.
66. Wimmer VC, Horstmann H, Groh A, Kuner T. 2006. Donut-like topology of synaptic vesicles with a central cluster of mitochondria wrapped into membrane protrusions: a novel structure-function module of the adult calyx of Held. J Neurosci 26:109-116.
67. Yamada J, Nakanishi H, Jinno S. 2011. Differential involvement of perineuronal astrocytes and microglia in synaptic stripping after hypoglossal axotomy. Neuroscience 182:1-10.