The DOI matches its Crossref record; 3 of the 3 references it cites were found in a registry or an index.
Gastric neurons in the nucleus tractus solitarius are selective to the orientation of gastric electrical stimulation
Open accessPublished version of a preprint
Abstract
Objective. Gastric electrical stimulation (GES) is a bioelectric intervention for gastroparesis, obesity, and other functional gastrointestinal disorders. In a potential mechanism of action, GES activates the nerve endings of vagal afferent neurons and induces the vago-vagal reflex through the nucleus tractus solitarius (NTS) in the brainstem. However, it is unclear where and how to stimulate in order to optimize the vagal afferent responses. Approach. To address this question with electrophysiology in rats, we applied mild electrical currents to two serosal targets on the distal forestomach with dense distributions of vagal intramuscular arrays (IMAs) that innervated the circular and longitudinal smooth muscle layers. During stimulation, we recorded single and multi-unit responses from gastric neurons in NTS and evaluated how the recorded responses depended on the stimulus orientation and amplitude. Main results. We found that NTS responses were highly selective to the stimulus orientation for a range of stimulus amplitudes. The strongest responses were observed when the applied current flowed in the same direction as the IMAs in parallel with the underlying smooth muscle fibers. Our results suggest that gastric neurons in NTS may encode the orientation-specific activity of gastric smooth muscles relayed by vagal afferent neurons. Significance. This finding suggests that the orientation of GES is critical to effective engagement of vagal afferents and should be considered in light of the structural phenotypes of vagal terminals in the stomach.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Different forces (distension, contraction, stroking) applied to the stomach wall activate both the vagal and the spinal splanchnic nerves.
“Different forces (distension, contraction, stroking) applied to the stomach wall activate both the vagal 167-169 and the spinal splanchnic 170,171 nerves,”
From Interoceptive rhythms in the brain (2023) · cites this paper as [169]
The Introduction (page not available) says vagal afferent terminals in the stomach wall include mechanoreceptors that report smooth-muscle stretch, supporting a response to at least one kind of mechanical force. It does not establish that distension, contraction, and stroking each activate vagal nerves. The spinal splanchnic portion of the sentence has separate citations and is not attributed to this source. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Sensory neurons that detect stretch and nutrients in the digestive system
Williams, E. K., Chang, R. B., Strochlic, D. E., Umans, B. D., Lowell, B. B., & Liberles, S. D. (2016) · Cell · doi:10.1016/j.cell.2016.05.011 · Cited by 645
Browning, K. N., & Travagli, R. A. (2014) · Comprehensive Physiology · doi:10.1002/cphy.c130055 · Cited by 541
Vagal circuitry mediating cephalic-phase responses to food
Powley, T. L. (2000) · Appetite · doi:10.1006/appe.1999.0279 · Cited by 98
Self-citation
Flagged first, then by citations
Research works printed but not linked: 55
- Abell, 2003, Gastric electrical stimulation for medically refractory gastroparesis, Gastroenterology, 125, 421, 10.1016/S0016-5085(03)00878-3 · DOI
- Ahmed, 2020, Anodal block permits directional vagus nerve stimulation, Sci. Rep., 10, 9221, 10.1038/s41598-020-66332-y · DOI
- Andermann, 2017, Toward a wiring diagram understanding of appetite control, Neuron, 95, 757, 10.1016/j.neuron.2017.06.014 · DOI
- Babic, 2014, The role of vagal neurocircuits in the regulation of nausea and vomiting, Eur. J. Pharmacol., 722, 38, 10.1016/j.ejphar.2013.08.047 · DOI · Paper page
- Berthoud, 1997, Distribution and structure of vagal afferent intraganglionic laminar endings (IGLEs) in the rat gastrointestinal tract, Anat. Embryol., 195, 183, 10.1007/s004290050037 · DOI
- Berthoud, 1992, Vagal afferent innervation of the rat fundic stomach: morphological characterization of the gastric tension receptor, J. Comp. Neurol., 319, 261, 10.1002/cne.903190206 · DOI
- Brindley, 1980, A technique for anodally blocking large nerve fibres through chronically implanted electrodes, J. Neurol. Neurosurg. Psychiatr., 43, 1083, 10.1136/jnnp.43.12.1083 · DOI
- Brookes, 2013, Extrinsic primary afferent signalling in the gut, Nat. Rev. Gastroenterol. Hepatol., 10, 286, 10.1038/nrgastro.2013.29 · DOI
- Browning, 2021, Central neurocircuits regulating food intake in response to gut inputs—preclinical evidence, Nutrients, 13, 908, 10.3390/nu13030908 · DOI
- Carabotti, 2015, The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems, Ann. Gastroenterol., 28, 203
- Carmagnola, 2005, Mechanoreceptors of the proximal stomach and perception of gastric distension, Am. J. Gastroenterol., 100, 1704, 10.1111/j.1572-0241.2005.41350.x · DOI
- Chen, 2004, Mechanisms of action of the implantable gastric stimulator for obesity, Obes. Surg., 14, S28, 10.1007/BF03342135 · DOI
- Cheng, 2021, Strategies to refine gastric stimulation and pacing protocols: experimental and modeling approaches, Front. Neurosci., 15, 10.3389/fnins.2021.645472 · DOI
- Du, 2009, Effects of electrical stimulation on isolated rodent gastric smooth muscle cells evaluated via a joint computational simulation and experimental approach, Am. J. Physiol.-Gastrointestinal Liver Physiol., 297, G672, 10.1152/ajpgi.00149.2009 · DOI
- Forster, 2001, Gastric pacing is a new surgical treatment for gastroparesis, Am. J. Surg., 182, 676, 10.1016/S0002-9610(01)00802-9 · DOI
- Furness, 2020, The identification of neuronal control pathways supplying effector tissues in the stomach, Cell and Tissue Research, 382, 433, 10.1007/s00441-020-03294-7 · DOI
- Furness, 2013, The gut as a sensory organ, Nat. Rev. Gastroenterol. Hepatol., 10, 729, 10.1038/nrgastro.2013.180 · DOI
- Furness, 2018, The first brain: species comparisons and evolutionary implications for the enteric and central nervous systems, Neurogastroenterol. Motility, 30, 10.1111/nmo.13234 · DOI
- Gottfried‐Blackmore, 2020, Open-label pilot study: non-invasive vagal nerve stimulation improves symptoms and gastric emptying in patients with idiopathic gastroparesis, Neurogastroenterol. Motility, 32, 10.1111/nmo.13769 · DOI
- Han, 2018, A neural circuit for gut-induced reward, Cell, 175, 665, 10.1016/j.cell.2018.08.049 · DOI
- Hasler, 2009, Methods of gastric electrical stimulation and pacing: a review of their benefits and mechanisms of action in gastroparesis and obesity, Neurogastroenterol. Motility, 21, 229, 10.1111/j.1365-2982.2009.01277.x · DOI
- Hocking, 1992, Human gastric myoelectric activity and gastric emptying following gastric surgery and with pacing, Gastroenterology, 103, 1811, 10.1016/0016-5085(92)91439-B · DOI
- Holtmann, 2014, The stomach–brain axis, Best Pract. Res. Clin. Gastroenterol., 28, 967, 10.1016/j.bpg.2014.10.001 · DOI
- Jones, 1995, Heart rate responses to selective stimulation of cardiac vagal C fibres in anaesthetized cats, rats and rabbits, J. Physiol., 489, 203, 10.1113/jphysiol.1995.sp021042 · DOI
- Kelly, 1972, Pacing the canine stomach with electric stimulation, Am. J. Physiol.-Legacy Content, 222, 588, 10.1152/ajplegacy.1972.222.3.588 · DOI
- Lal, 2015, Gastric electrical stimulation with the enterra system: a systematic review, Gastroenterol. Res. Pract., 2015, 1, 10.1155/2015/762972 · DOI
- Levinthal, 2017, Systematic review and meta-analysis: gastric electrical stimulation for gastroparesis, Auton. Neurosci., 202, 45, 10.1016/j.autneu.2016.03.004 · DOI
- Levinthal, 2020, Multiple areas of the cerebral cortex influence the stomach, Proc. Nat. Acad. Sci. USA, 117, 13078, 10.1073/pnas.2002737117 · DOI · Paper page
- Li, 2010, Cellular effects of gastric electrical stimulation on antral smooth muscle cells in rats, Am. J. Physiol.-Regul. Integr. Comp. Physiol., 298, R1580, 10.1152/ajpregu.00024.2010 · DOI
- Lu, 2020, Acute effects of vagus nerve stimulation parameters on gastric motility assessed with magnetic resonance imaging, Neurogastroenterol. Motility, 32, 10.1111/nmo.13853 · DOI
- Lu, 2017, Contrast enhanced magnetic resonance imaging of gastric emptying and motility in rats, IEEE Trans. Biomed. Eng., 64, 2546, 10.1109/TBME.2017.2737559 · DOI
- Mayer, 2011, Gut feelings: the emerging biology of gut–brain communication, Nat. Rev. Neurosci., 12, 453, 10.1038/nrn3071 · DOI · Paper page
- Mayer, 2006, Modulation of the brain–gut axis as a therapeutic approach in gastrointestinal disease, Aliment. Pharmacol. Ther., 24, 919, 10.1111/j.1365-2036.2006.03078.x · DOI
- McCallum, 1998, Gastric pacing improves emptying and symptoms in patients with gastroparesis, Gastroenterology, 114, 456, 10.1016/S0016-5085(98)70528-1 · DOI
- McCallum, 2010a, Mechanisms of symptomatic improvement after gastric electrical stimulation in gastroparetic patients, Neurogastroenterol. Motility, 22, 161, 10.1111/j.1365-2982.2009.01389.x · DOI
- McCallum, 2010b, Gastric electrical stimulation with Enterra therapy improves symptoms from diabetic gastroparesis in a prospective study, Clin. Gastroenterol. Hepatol., 8, 947, 10.1016/j.cgh.2010.05.020 · DOI
- O’Grady, 2009, High-frequency gastric electrical stimulation for the treatment of gastroparesis: a meta-analysis, World J. Surg., 33, 1693, 10.1007/s00268-009-0096-1 · DOI
- Payne, 2019, Bioelectric neuromodulation for gastrointestinal disorders: effectiveness and mechanisms, Nat. Rev. Gastroenterol. Hepatol., 16, 89, 10.1038/s41575-018-0078-6 · DOI
- Penagini, 2004, Mechanoreceptors of the proximal stomach: role in triggering transient lower esophageal sphincter relaxation, Gastroenterology, 126, 49, 10.1053/j.gastro.2003.10.045 · DOI
- Phillips, 2000, Tension and stretch receptors in gastrointestinal smooth muscle: re-evaluating vagal mechanoreceptor electrophysiology, Brain Res. Rev., 34, 1, 10.1016/S0165-0173(00)00036-9 · DOI
- Powley, 2016, Vagal intramuscular arrays: the specialized mechanoreceptor arbors that innervate the smooth muscle layers of the stomach examined in the rat, J. Comp. Neurol., 524, 713, 10.1002/cne.23892 · DOI
- Powley, 2019, Vagal innervation of the stomach reassessed: brain-gut connectome uses smart terminals, Ann. NY Acad. Sci., 1454, 14, 10.1111/nyas.14138 · DOI
- Powley, 2002, I. Morphology and topography of vagal afferents innervating the GI tract, Am. J. Physiol.-Gastrointestinal Liver Physiol., 283, G1217, 10.1152/ajpgi.00249.2002 · DOI
- Powley, 2011, Vagal afferent innervation of the proximal gastrointestinal tract mucosa: chemoreceptor and mechanoreceptor architecture, J. Comp. Neurol., 519, 644, 10.1002/cne.22541 · DOI
- Qin, 2005, Gastric electrical stimulation modulates neuronal activity in nucleus tractus solitarii in rats, Auton. Neurosci., 119, 1, 10.1016/j.autneu.2005.01.007 · DOI
- Rijkhoff, 1997, Selective detrusor activation by electrical sacral nerve root stimulation in spinal cord injury, J. Urol., 157, 1504, 10.1016/S0022-5347(01)65032-8 · DOI
- Rogers, 1995, Vagovagal reflex control of digestion: afferent modulation by neural and endoneurocrine factors, Am. J. Physiol.-Gastrointestinal Liver Physiol., 268, G1, 10.1152/ajpgi.1995.268.1.G1 · DOI · Paper page
- Tan, 2021, Stomach region stimulated determines effects on duodenal motility in rats, Am. J. Physiol. Regul. Integr. Comp. Physiol., 320, R331, 10.1152/ajpregu.00111.2020 · DOI
- Tang, 2006, Central mechanisms of gastric electrical stimulation involving neurons in the paraventricular nucleus of the hypothalamus in rats, Obes. Surg., 16, 344, 10.1381/096089206776116372 · DOI
- Tomita, 1966, Electrical responses of smooth muscle to external stimulation in hypertonic solution, J. Physiol., 183, 450, 10.1113/jphysiol.1966.sp007876 · DOI
- Travagli, 2016, Vagal neurocircuitry and its influence on gastric motility, Nat. Rev. Gastroenterol. Hepatol., 13, 389, 10.1038/nrgastro.2016.76 · DOI · Paper page
- Travagli, 2006, Brainstem circuits regulating gastric function, Annu. Rev. Physiol., 68, 279, 10.1146/annurev.physiol.68.040504.094635 · DOI · Paper page
- Wang, 2000, Topographic inventories of vagal afferents in gastrointestinal muscle, J. Comp. Neurol., 421, 302, 10.1002/(SICI)1096-9861(20000605)421:3<302::AID-CNE2>3.0.CO;2-N · DOI
- Whitehead, 1988, Neuronal architecture of the nucleus of the solitary tract in the hamster, J. Comp. Neurol., 276, 547, 10.1002/cne.902760409 · DOI
- Yin, 2008, Implantable gastric electrical stimulation: ready for prime time?, Gastroenterology, 134, 665, 10.1053/j.gastro.2008.01.068 · DOI
Cited by
Sorted by citations
Interoceptive rhythms in the brain
Engelen, T., Solcà, M., & Tallon-Baudry, C. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01425-1 · Cited by 207
The vagus nerve mediates the stomach-brain coherence in rats
Cao, J., Wang, X., Chen, J., Zhang, N., & Liu, Z. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119628 · Cited by 25
Self-citation
Metadata
- Authors
- Cao, J., Wang, X., Powley, T. L., & Liu, Z.
- Affiliations
- University of Michigan (US)
- Purdue University West Lafayette (US)
- Corresponding author
- Cao, Jiayue
- Wang, Xiaokai
- Powley, Terry L
- Liu, Zhongming
- Venue
- Journal of Neural Engineering
- Publisher
- IOP Publishing
- Published
- 2021-10-01
- Volume
- 18
- Issue
- 5
- Pages
- 056066
- ISSN
- 1741-2552 (ISSN-L)
- 1741-2560
- PMC
- PMC8625070
- OpenAlex
- W3205863227
- Cited by
- 10
- References
- 3
- Citations by year
- 2026: 2 · 2025: 1 · 2023: 4 · 2022: 3
- FWCI
- 1.60
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- Locations
- Journal of Neural Engineering (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Center for Complementary and Integrative Health (AT011665)
- NIH Office of the Director (OD023847)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK131524)
- Topics
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neural Engineering
- Keywords
- gastric electrical stimulation, nucleus tractus solitarius, vagal afferent neurons, stimulus orientation, gastric smooth muscle, vago-vagal reflex, gastroparesis, functional gastrointestinal disorders
- MeSH terms
- Animals, Electric Stimulation, Neurons, Stomach, Vagus Nerve, Solitary Nucleus, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review