Cited by 112Neuroscience and Neuropharmacology ResearchNeuropeptides and Animal PhysiologyNeuroscience of respiration and sleep

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Vasopressin Inhibits Glutamate Release via Two Distinct Modes in the Brainstem

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Bailey, T. W., Jin, Y.-H., Doyle, M. W., Smith, S. M., Andresen, M. C.·2006·Journal of Neuroscience

DOI 10.1523/jneurosci.5176-05.2006PMC PMC2680488

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Abstract

The hypothalamus coordinates autonomic responses in part through arginine vasopressin (AVP) released in medial nucleus tractus solitarius (NTS). However, the mechanisms and sites of AVP action within NTS pathways are uncertain. In brainstem slices, we activated solitary tract (ST) primary afferents to release glutamate and tested whether AVP modulated synaptic transmission to second-order neurons. NTS neurons were classified as second order by ST synaptic characteristics or the presence of anterograde tracers from peripheral baroreceptor afferents. Stimulus recruitment curves indicated ST-EPSCs on individual neurons were evoked by stimulation of single ST axons. Variance-mean (V-M) analysis of ST-EPSCs in individual neurons revealed uniformly high release probability (p approximately 0.9) from an average of 19 release sites (N) and a quantal size (q) of 34.0 +/- 4.7 pA. In 26 of 49 neurons, AVP inhibited afferent synaptic transmission. In most neurons, AVP reduced ST-EPSC amplitudes (n = 20) by decreasing p to 0.65, whereas q, N, and conduction times were unaffected. The V1a antagonist SR49059 alone decreased ST-EPSC V and increased M, suggesting tonic AVP actions, and blocked exogenous AVP action (n = 4). In other neurons with identical ST release properties, AVP induced synaptic failures and increased conduction time without altering the V-M relationship of successful ST-EPSCs (n = 6). Interestingly, frequency-depressed ST-EPSCs were not affected by AVP. AVP failed to alter holding or voltage-dependent potassium currents. Thus, AVP regulates NTS neurons by two distinct novel and state-dependent mechanisms: one, an analog, graded presynaptic inhibition of terminal glutamate release and the other, a binary, extraterminal block of conducted excitation.

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Authors: Bailey, T. W., Jin, Y.-H., Doyle, M. W., Smith, S. M., & Andresen, M. C.
Affiliations: Oregon Health & Science University (US)
ORCID: Smith, S. M.
Andresen, M. C.
Venue: Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2006-06-07
Volume: 26
Issue: 23
Pages: 6131-6142
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.5176-05.2006
PMC: PMC2680488
OpenAlex: W1964779574
Cited by: 112
References: 60
Citations by year: 2026: 1 · 2025: 4 · 2024: 1 · 2023: 3 · 2021: 4 · 2020: 3 · 2019: 7 · 2018: 6 · 2017: 5 · 2016: 2 · 2015: 9 · 2014: 6 · 2013: 7 · 2012: 13
FWCI: 3.54
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Neuroscience (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Heart, Lung, and Blood Institute (F32HL070433, HL-56460, HL-70433, HL41119, R01HL041119)
National Institute of Neurological Disorders and Stroke (R01NS043444, NS-43444)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
Keywords: vasopressin, glutamate release, brainstem, presynaptic inhibition, synaptic transmission, release probability, quantal size, synaptic failure, baroreceptor afferents, V1a receptor, hypothalamus, autonomic regulation
MeSH terms: Animals, Arginine Vasopressin, Drug Resistance, Male, Synaptic Transmission, Neurons, Afferent, Pressoreceptors, Probability, Rats, Sprague-Dawley, Receptors, Vasopressin, Solitary Nucleus, Glutamic Acid, Excitatory Postsynaptic Potentials, Rats, In Vitro Techniques

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Vasopressin Inhibits Glutamate Release via Two Distinct Modes in the Brainstem

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