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The Journal of Neuroscience, November 5, 2008, 28(45):11731-11740; doi:10.1523/JNEUROSCI.3419-08.2008

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Cellular/Molecular
Oxytocin Enhances Cranial Visceral Afferent Synaptic Transmission to the Solitary Tract Nucleus

James H. Peters,¹ Stuart J. McDougall,¹ Daniel O. Kellett,² David Jordan,²  Ida J. Llewellyn-Smith,³ and Michael C. Andresen¹

¹Department of Physiology and Pharmacology, Oregon Health & Science University, Portland, Oregon 97239-3098, ²Department of Physiology, Royal Free and University College Medical School, University College London, London WC1E 6BT, United Kingdom, and ³Cardiovascular Medicine and Centre for Neuroscience, Flinders University, Bedford Park, South Australia 5042, Australia

Correspondence should be addressed to Dr. James H. Peters, Department of Physiology and Pharmacology, L334, Oregon Health & Science University, 3181 SW Sam Jackson Park Road, Portland, OR 97239-3098. Email: petersj.ohsu{at}gmail.com

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.

Key words: autonomic; brainstem; synaptic; vagal afferents; immunocytochemistry; ultrastructure

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Received July 21, 2008; revised Sept. 29, 2008; accepted Oct. 5, 2008.

Correspondence should be addressed to Dr. James H. Peters, Department of Physiology and Pharmacology, L334, Oregon Health & Science University, 3181 SW Sam Jackson Park Road, Portland, OR 97239-3098. Email: petersj.ohsu{at}gmail.com

Related articles in J. Neurosci.:

Oxytocin Influence on the Nucleus of the Solitary Tract: Beyond Homeostatic Regulation

Kate Karelina and Greg J. Norman
J. Neurosci. 2009 29: 4687-4689. [Full Text]  

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