Withdrawal and restoration of central vagal afferents within the dorsal vagal complex following subdiaphragmatic vagotomy
Open accessAbstract
Vagotomy, a severing of the peripheral axons of the vagus nerve, has been extensively utilized to determine the role of vagal afferents in viscerosensory signaling. Vagotomy is also an unavoidable component of some bariatric surgeries. Although it is known that peripheral axons of the vagus nerve degenerate and then regenerate to a limited extent following vagotomy, very little is known about the response of central vagal afferents in the dorsal vagal complex to this type of damage. We tested the hypothesis that vagotomy results in the transient withdrawal of central vagal afferent terminals from their primary central target, the nucleus of the solitary tract (NTS). Sprague–Dawley rats underwent bilateral subdiaphragmatic vagotomy and were sacrificed 10, 30, or 60 days later. Plastic changes in vagal afferent fibers and synapses were investigated at the morphological and functional levels by using a combination of an anterograde tracer, synapse‐specific markers, and patch‐clamp electrophysiology in horizontal brain sections. Morphological data revealed that numbers of vagal afferent fibers and synapses in the NTS were significantly reduced 10 days following vagotomy and were restored to control levels by 30 days and 60 days, respectively. Electrophysiology revealed transient decreases in spontaneous glutamate release, glutamate release probability, and the number of primary afferent inputs. Our results demonstrate that subdiaphragmatic vagotomy triggers transient withdrawal and remodeling of central vagal afferent terminals in the NTS. The observed vagotomy‐induced plasticity within this key feeding center of the brain may be partially responsible for the response of bariatric patients following gastric bypass surgery. J. Comp. Neurol. 521:3584‐3599, 2013. © 2013 Wiley Periodicals, Inc.
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Subdiaphragmatic vagotomy induced transient withdrawal and restoration of central vagal afferents as well as synaptic plasticity in the NTS.
“For example, subdiaphragmatic vagotomy induced transient withdrawal and restoration of central vagal afferents as well as synaptic plasticity in the NTS (19).”
From Vagus Nerve as Modulator of the Brain–Gut Axis in Psychiatric and Inflammatory Disorders (2018) · cites this paper as [19]
Animal studies have demonstrated a remarkable regeneration capacity of the vagus nerve.
“Animal studies have demonstrated a remarkable regeneration capacity of the vagus nerve.”
From Vagus Nerve as Modulator of the Brain–Gut Axis in Psychiatric and Inflammatory Disorders (2018) · cites this paper as [19]
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Neural plasticity after peripheral nerve injury and regeneration
Navarro, X., Vivó, M., & Valero‐Cabré, A. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.06.005 · Cited by 884 · see citing works
Altschuler, S. M., Bao, X., Bieger, D., Hopkins, D. A., & Miselis, R. R. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902830207 · Cited by 754 · see citing works
Michaela, E., & Elphick, M. R. (2000) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(20000626)422:2 · Cited by 364 · see citing works
Purves, D. (1975) · The Journal of Physiology · doi:10.1113/jphysiol.1975.sp011151 · Cited by 345 · see citing works
Single-Synapse Analysis of a Diverse Synapse Population: Proteomic Imaging Methods and Markers
Micheva, K. D., Busse, B. L., Weiler, N. C., O’Rourke, N. A., & Smith, S. J. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.024 · Cited by 336 · see citing works
Comparative evaluation of synaptophysin-based methods for quantification of synapses
Calhoun, M. E., Jucker, M., Martin, L. J., Thinakaran, G., Price, D. L., & Mouton, P. R. (1996) · Journal of Neurocytology · doi:10.1007/bf02284844 · Cited by 303 · see citing works
II. The intestine as a sensory organ: neural, endocrine, and immune responses
Furness, J. B., Kunze, W., & Clerc, N. (1999) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1999.277.5.g922 · Cited by 300 · see citing works
Plasticity in the spinal cord sensory map following peripheral nerve injury in rats
Devor, M. G., & Wall, P. D. (1981) · Journal of Neuroscience · doi:10.1523/jneurosci.01-07-00679.1981 · Cited by 295 · see citing works
Effects of gastric bypass surgery in patients with type 2 diabetes and only mild obesity
Cohen, R. V., Pinheiro, J. C., Schiavon, C. A., Salles, J. E., Wajchenberg, B. L., & Cummings, D. E. (2012) · Diabetes Care · doi:10.2337/dc11-2289 · Cited by 282 · see citing works
Reliability of Monosynaptic Sensory Transmission in Brain Stem Neurons In Vitro
Doyle, M., & Andresen, M. C. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.5.2213 · Cited by 244 · see citing works
Binary imaging analysis for comprehensive quantitative histomorphometry of peripheral nerve
Hunter, D. A., Moradzadeh, A., Whitlock, E. L., Brenner, M. J., Myckatyn, T. M., Wei, C., Tung, T. H. H., & Mackinnon, S. E. (2007) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2007.06.018 · Cited by 190 · see citing works
Aldskogius, H., & Arvidsson, J. (1978) · Journal of Neurocytology · doi:10.1007/bf01217921 · Cited by 181 · see citing works
Peters, J. H., McDougall, S. J., Fawley, J. A., Smith, S. M., & Andresen, M. C. (2010) · Neuron · doi:10.1016/j.neuron.2010.02.017 · Cited by 181 · see citing works
Self-citationQuantitative electron microscopy on the injured hypoglossal nucleus in the rat
SUMNER, B. E. H., & Sutherland, F. I. (1973) · Journal of Neurocytology · doi:10.1007/bf01104033 · Cited by 176 · see citing works
Chen, D. H. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901770407 · Cited by 140 · see citing works
Oxytocin enhances cranial visceral afferent synaptic transmission to the solitary tract nucleus
Peters, J. H., McDougall, S. J., Kellett, D. O., Jordan, D., Llewellyn-Smith, I. J., & Andresen, M. C. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.3419-08.2008 · Cited by 135 · see citing works
Self-citationKim, S. K., & Nabekura, J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0328-11.2011 · Cited by 120 · see citing works
Chapter 27 Neural Plasticity After Nerve Injury and Regeneration
Navarro, X. (2009) · International review of neurobiology · doi:10.1016/s0074-7742(09)87027-x · Cited by 117 · see citing works
Organization and Properties of GABAergic Neurons in Solitary Tract Nucleus (NTS)
Bailey, T. W., Appleyard, S. M., Jin, Y., & Andresen, M. C. (2008) · Journal of Neurophysiology · doi:10.1152/jn.00038.2008 · Cited by 114 · see citing works
Vasopressin Inhibits Glutamate Release via Two Distinct Modes in the Brainstem
Bailey, T. W., Jin, Y.-H., Doyle, M. W., Smith, S. M., & Andresen, M. C. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5176-05.2006 · Cited by 112 · see citing works
Thermally Active TRPV1 Tonically Drives Central Spontaneous Glutamate Release
Shoudai, K., Peters, J. H., McDougall, S. J., Fawley, J. A., & Andresen, M. C. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2557-10.2010 · Cited by 112 · see citing works
Self-citationRetrograde tracer technique for assessment of selective and total subdiaphragmatic vagotomies
Powley, T. L., Fox, E. A., & Berthoud, H. R. (1987) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1987.253.2.r361 · Cited by 108 · see citing works
Spontaneous Neurotransmission: An Independent Pathway for Neuronal Signaling?
Kavalali, E. T., Chung, C., Khvotchev, M., Leitz, J., Nosyreva, E., Raingo, J., & Ramirez, D. M. O. (2011) · Physiology · doi:10.1152/physiol.00040.2010 · Cited by 104 · see citing works
Axotomy-induced apoptosis in adult rat primary sensory neurons
Groves, M., Christopherson, T., Giometto, B., & Scaravilli, F. (1997) · Journal of Neurocytology · doi:10.1023/a:1018541726460 · Cited by 101 · see citing works
Integrative capacity of the caudal brainstem in the control of food intake
Schwartz, G. J. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1862 · Cited by 100 · see citing works
Wimmer, V. C., Horstmann, H., Groh, A., & Kuner, T. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3268-05.2006 · Cited by 93 · see citing works
Nitric Oxide-Directed Synaptic Remodeling in the Adult Mammal CNS
Sunico, C. R., Portillo, F., González‐Forero, D., & Moreno‐López, B. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4600-04.2005 · Cited by 90 · see citing works
Obesity surgery and gut–brain communication
Berthoud, H., Shin, A. C., & Zheng, H. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.01.023 · Cited by 84 · see citing works
Czaja, K., Burns, G. A., & Ritter, R. C. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.03.055 · Cited by 71 · see citing works
Self-citationStrategies for cellular identification in nucleus tractus solitarius slices
Doyle, M. W., Bailey, T. W., Jin, Y., Appleyard, S. M., Low, M. J., & Andresen, M. C. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2004.02.007 · Cited by 61 · see citing works
Laiwand, R., Werman, R., & Yarom, Y. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902560405 · Cited by 61 · see citing works
Long-term regeneration of abdominal vagus: efferents fail while afferents succeed
Phillips, R. J., Baronowsky, E. A., & Powley, T. L. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10470 · Cited by 59 · see citing works
Ramer, L. M., van Stolk, A. P., Inskip, J. A., et al. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00257 · Cited by 58 · see citing works
Li, Y., & Owyang, C. (2003) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00119.2003 · Cited by 57 · see citing works
Sensory Afferent Neurotransmission in Caudal Nucleus Tractus Solitarius—Common Denominators
Andresen, M. C., & Mendelowitz, D. (1996) · Chemical Senses · doi:10.1093/chemse/21.3.387 · Cited by 57 · see citing works
Localization of Kv1.3 channels in presynaptic terminals of brainstem auditory neurons
Gazula, V., Strumbos, J. G., Mei, X., Chen, H., Rahner, C., & Kaczmarek, L. K. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22393 · Cited by 56 · see citing works
Convergence of Cranial Visceral Afferents within the Solitary Tract Nucleus
McDougall, S. J., Peters, J. H., & Andresen, M. C. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3491-09.2009 · Cited by 54 · see citing works
Self-citationRecovery of synapses in axotomized adult cat spinal motoneurons after reinnervation into muscle
Brännström, T., & Kellerth, J. (1999) · Experimental Brain Research · doi:10.1007/s002210050653 · Cited by 54 · see citing works
Groves, M. J., An, S., Giometto, B., et al. (1999) · Experimental Neurology · doi:10.1006/exnr.1998.6985 · Cited by 51 · see citing works
Rho, M.-J., Cabana, T., & Drew, T. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19971117)388:2 · Cited by 50 · see citing works
Peters, J. H., McDougall, S. J., Fawley, J. A., & Andresen, M. C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025015 · Cited by 50 · see citing works
Self-citationGallaher, Z. R., Ryu, V., Herzog, T., Ritter, R. C., & Czaja, K. (2012) · Neuroscience Letters · doi:10.1016/j.neulet.2012.01.079 · Cited by 47 · see citing works
Self-citationYamada, J., Nakanishi, H., & Jinno, S. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.03.030 · Cited by 45 · see citing works
Sun, T., Xiao, H., Zhou, P.-B., Lu, Y.-J., Bao, L., & Zhang, X. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.05.010 · Cited by 37 · see citing works
Soiza‐Reilly, M., & Commons, K. G. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.22734 · Cited by 37 · see citing works
Vagotomy Decreases Excitability in Primary Vagal Afferent Somata
Lancaster, E., Oh, E. J., & Weinreich, D. M. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.1.247 · Cited by 35 · see citing works
Axotomy Induces Retraction of the Dendritic Arbor of Adult Rat Rubrospinal Neurons
Tseng, G., & Hu, M.-E. (1996) · Cells Tissues Organs · doi:10.1159/000147803 · Cited by 34 · see citing works
Validation of tests of completeness of vagotomy in rats
LOUIS-SYLVESTRE, J. (1983) · Journal of the Autonomic Nervous System · doi:10.1016/0165-1838(83)90149-2 · Cited by 32 · see citing works
Svensson, M. A., & Aldskogius, H. (1992) · Journal of Neurocytology · doi:10.1007/bf01194980 · Cited by 31 · see citing works
Injury-induced remodelling and regeneration of the ribbon presynaptic terminalin vitro
Nachman-Clewner, M., & Townes‐Anderson, E. (1996) · Journal of Neurocytology · doi:10.1007/bf02284827 · Cited by 25 · see citing works
Hu, J., Mata, M. M., Hao, S., et al. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03652.x · Cited by 24 · see citing works
Ryu, V., Gallaher, Z. R., & Czaja, K. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.02.049 · Cited by 24 · see citing works
Self-citationJinno, S., & Yamada, J. (2011) · Neuron Glia Biology · doi:10.1017/s1740925x11000135 · Cited by 24 · see citing works
Hippocampal plasticity after a vagus nerve injury in the rat.
(2012) · PubMed Central · doi:10.3969/j.issn.1673-5374.2012.14.003 · Cited by 23 · see citing works
Gallaher, Z. R., Ryu, V., Larios, R. M., et al. (2011) · Frontiers in Neuroscience · doi:10.3389/fnins.2011.00012 · Cited by 23 · see citing works
Self-citationSynaptic detachment from hypoglossal neurons after different types of nerve injury in the cat.
Svensson, M. A., Törnqvist, E., Aldskogius, H., et al. (1991) · PubMed · Cited by 23 · see citing works
Emirandetti, A., Simões, G. F., Zanon, R. G., & de Oliveira, A. L. R. (2010) · Journal of Neuroinflammation · doi:10.1186/1742-2094-7-31 · Cited by 21 · see citing works
Plasticity of vagal afferents at the site of an incision in the wall of the stomach
Phillips, R. J., & Powley, T. L. (2005) · Autonomic Neuroscience · doi:10.1016/j.autneu.2005.08.009 · Cited by 19 · see citing works
Tiraihi, T., & Rezaie, M. J. (2003) · Developmental Brain Research · doi:10.1016/j.devbrainres.2003.11.002 · Cited by 17 · see citing works
A-Fiber Sprouting in Spinal Cord Dorsal Horn Is Attenuated by Proximal Nerve Stump Encapsulation
White, F. (2002) · Experimental Neurology · doi:10.1006/exnr.2002.7996 · Cited by 14 · see citing works
Herde, M. K., Friauf, E., & Rust, M. B. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22298 · Cited by 11 · see citing works
Bowe, C. M., Evans, N. H., & Vlacha, V. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903210406 · Cited by 10 · see citing works
Swartz, J. B., & Weinreich, D. M. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00168.2009 · Cited by 9 · see citing works
Hippocampal plasticity in rats submitted to a gastric restrictive procedure
Sonoda, E. Y. D. F., da Silva, S. G., Arida, R. M., Giglio, P. N., Margarido, N. F., Martinez, C. A. R., Pansani, A. P., Maciel, R. D. S., Cavalheiro, É. A., & Scorza, F. A. (2011) · Nutritional Neuroscience · doi:10.1179/1476830511y.0000000009 · Cited by 6 · see citing works
Bariatric surgery or medicine for type 2 diabetes?
Doggrell, S. A., & Chan, V. (2012) · Expert Opinion on Pharmacotherapy · doi:10.1517/14656566.2012.721779 · Cited by 5 · see citing works
Lan, C., Hsu, J., Chang, C., et al. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10576 · Cited by 4 · see citing works
Phillips (2000) · doi:10.1002/(sici)1096-9861(20000605)421:3
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- Authors
- Peters, J. H., Gallaher, Z. R., Ryu, V., & Czaja, K.
- Affiliations
- Washington State University (US)
- Georgia State University (US)
- Corresponding author
- Peters, James H.
- Czaja, Krzysztof
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2013-08-23
- Volume
- 521
- Issue
- 15
- Pages
- 3584-3599
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- PMC
- PMC4012858
- OpenAlex
- W1765129194
- Cited by
- 46
- References
- 67
- Citations by year
- 2025: 3 · 2024: 3 · 2023: 3 · 2021: 8 · 2020: 4 · 2019: 2 · 2018: 9 · 2017: 3 · 2016: 3 · 2015: 3 · 2014: 4 · 2012: 1
- FWCI
- 1.87
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK092651)
- Topics
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Keywords
- vagotomy, dorsal vagal complex, nucleus tractus solitarius, subdiaphragmatic vagotomy, glutamate release, synaptic plasticity, bariatric surgery, gastric bypass, feeding center
- MeSH terms
- Animals, Axons, Biotin, Dextrans, Diaphragm, Fluorescent Dyes, Image Processing, Computer-Assisted, Immunohistochemistry, Male, Nerve Regeneration, Neurons, Afferent, Synapses, Tubulin, Vagotomy, Vagus Nerve, Synapsins, Tissue Fixation, Synaptophysin, Rats, Sprague-Dawley, Solitary Nucleus, Patch-Clamp Techniques, Rats, Electrophysiological Phenomena
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