Oxytocin enhances cranial visceral afferent synaptic transmission to the solitary tract nucleus
Open accessAbstract
Cranial visceral afferents travel via the solitary tract (ST) to contact neurons within the ST nucleus (NTS) and activate homeostatic reflexes. Hypothalamic projections from the paraventricular nucleus (PVN) release oxytocin (OT) to modulate visceral afferent communication with NTS neurons. However, the cellular mechanisms through which OT acts are poorly understood. Here, we electrophysiologically identified second-order NTS neurons in horizontal brainstem slices by their low-jitter, ST-evoked glutamatergic EPSCs. OT increased the frequency of miniature EPSCs in half of the NTS second-order neurons (13/24) but did not alter event kinetics or amplitudes. These actions were blocked by a selective OT receptor antagonist. OT increased the amplitude of ST-evoked EPSCs with no effect on event kinetics. Variance-mean analysis of ST-evoked EPSCs indicated OT selectively increased the release probability of glutamate from the ST afferent terminals. In OT-sensitive neurons, OT evoked an inward holding current and increased input resistance. The OT-sensitive current reversed at the K(+) equilibrium potential. In in vivo studies, NTS neurons excited by vagal cardiopulmonary afferents were juxtacellularly labeled with Neurobiotin and sections were stained to show filled neurons and OT-immunoreactive axons. Half of these physiologically characterized neurons (5/10) showed close appositions by OT fibers consistent with synaptic contacts. Electron microscopy of medial NTS found immunoreactive OT within synaptic boutons. Together, these findings suggest that OT released from PVN axons acts on a subset of second-order neurons within medial NTS to enhance visceral afferent transmission via presynaptic and postsynaptic mechanisms.
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Electron microscopic analysis has revealed dense core vesicles containing AVP- and OT-ir in terminals located in synaptic regions of brain areas such as the habenula, lateral septum, amygdala, supraoptic nuclei, ventromedial hypothalamus, and the nucleus of the solitary tract.
“For example, electron microscopic analysis has revealed dense core vesicles containing AVP- and OT-ir in terminals located in synaptic regions of brain areas such as the habenula, lateral septum, amygdala, supraoptic nuclei, ventromedial hypothalamus and the nucleus of the solitary tract [98; 99; 100; 101; 102; 103; 104].”
From Cross-talk among oxytocin and arginine-vasopressin receptors: Relevance for basic and clinical studies of the brain and periphery (2018) · cites this paper as [100]
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Self-citation
- Authors
- Peters, J. H., McDougall, S. J., Kellett, D. O., Jordan, D., Llewellyn-Smith, I. J., & Andresen, M. C.
- Affiliations
- Oregon Health & Science University (US)
- The Royal Free Hospital (GB)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2008-11-05
- Volume
- 28
- Issue
- 45
- Pages
- 11731-11740
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2585803
- OpenAlex
- W2061040353
- Cited by
- 135
- References
- 45
- Citations by year
- 2026: 5 · 2025: 3 · 2024: 6 · 2023: 4 · 2022: 5 · 2021: 10 · 2020: 8 · 2019: 8 · 2018: 7 · 2017: 8 · 2016: 3 · 2015: 7 · 2014: 14 · 2013: 9 · 2012: 13
- FWCI
- 11.11
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- Flinders Academic Commons (Flinders University) (submittedVersion)
- Funders
- Wellcome Trust (067996)
- British Heart Foundation
- National Institutes of Health
- Medical Research Council
- National Health and Medical Research Council
- National Heart, Lung, and Blood Institute (F32HL088894, R01HL058760, HL-58760, R01HL083115, HL-88894, R01HL105703, R01HL041119)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- oxytocin, solitary tract nucleus, synaptic transmission, paraventricular nucleus, miniature EPSCs, release probability, presynaptic modulation, postsynaptic modulation, synaptic boutons
- MeSH terms
- Analysis of Variance, Animals, Biotin, Cranial Nerves, Dose-Response Relationship, Drug, Electric Stimulation, Hormone Antagonists, Male, Synaptic Transmission, Neurons, Oxytocin, Rats, Sprague-Dawley, Solitary Nucleus, Visceral Afferents, Patch-Clamp Techniques, Excitatory Postsynaptic Potentials, Microscopy, Electron, Transmission, Rats, In Vitro Techniques
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