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The Journal of Neuroscience, November 28, 2007, 27(48):13292-13302; doi:10.1523/JNEUROSCI.3502-07.2007

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Cellular/Molecular
Visceral Afferents Directly Activate Catecholamine Neurons in the Solitary Tract Nucleus

Suzanne M. Appleyard,¹ Daniel Marks,² Kazuto Kobayashi,⁴ Hideyuki Okano,⁵ Malcolm J. Low,^2,3 and Michael C. Andresen¹

¹Department of Physiology and Pharmacology, ²Center for the Study of Weight Regulation and Associated Disorders, and ³Department of Behavioral Neuroscience, Oregon Health & Science University, Portland, Oregon 97239, ⁴Department of Molecular Genetics, Institute of Biomedical Sciences, Fukushima Medical University, Fukushima 960-1295, Japan, and ⁵Department of Physiology, Keio University School of Medicine, Tokyo 160-8582, Japan

Correspondence should be addressed to Dr. Suzanne M. Appleyard at her present address: Department of Veterinary and Comparative Pharmacology and Physiology, College of Veterinary Medicine, Washington State University, P.O. Box 646520, Pullman, WA 99164. Email: appleyas{at}vetmed.wsu.edu

Brainstem A₂/C₂ neurons are catecholamine (CA) neurons within the solitary tract nucleus (NTS) that influence many homeostatic functions, including cardiovascular reflexes, food intake, and stress. Because NTS is a major interface between sensory visceral afferents and the CNS, NTS CA neurons are ideally suited to coordinate complex responses by their projections to multiple brain regions. To test how NTS CA neurons process visceral afferent information carried by solitary tract (ST) afferents, we identified CA neurons using transgenic mice expressing TH-EGFP (enhanced green fluorescent protein under the control of the tyrosine hydroxylase promoter) and recorded synaptic responses to ST activation in horizontal slices. ST shocks evoked large-amplitude, short-latency, glutamatergic EPSCs (ST-EPSCs) in 90% of NTS CA neurons. Within neurons, ST-EPSCs had constant latency, rarely failed, and depressed substantially at high ST frequencies, indicating that NTS CA neurons receive direct monosynaptic connections from afferent terminals. NTS CA neurons received direct ST inputs from only one or two afferent fibers, with one-half also receiving smaller amplitude indirect inputs. Up to 90% of ST shocks evoked action potentials in NTS CA neurons. However, transmission of sensory afferent information through NTS CA neurons critically depended on the expression of an A-type potassium current (I_KA), which when active attenuated ST-activated action potentials to a 37% success rate. The satiety peptide, cholecystokinin, presynaptically facilitated glutamate transmission in one-half of NTS CA neurons. Thus, NTS CA neurons are directly driven by visceral afferents with output being modulated by presynaptic peptide receptors and postsynaptic potassium channels.

Key words: tyrosine hydroxylase; vagus; NTS; food intake; cardiovascular; autonomic

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Received Aug. 1, 2007; revised Oct. 3, 2007; accepted Oct. 24, 2007.

Correspondence should be addressed to Dr. Suzanne M. Appleyard at her present address: Department of Veterinary and Comparative Pharmacology and Physiology, College of Veterinary Medicine, Washington State University, P.O. Box 646520, Pullman, WA 99164. Email: appleyas{at}vetmed.wsu.edu

This article has been cited by other articles:

				T. W. Bailey, S. M. Appleyard, Y.-H. Jin, and M. C. Andresen Organization and Properties of GABAergic Neurons in Solitary Tract Nucleus (NTS) J Neurophysiol, April 1, 2008; 99(4): 1712 - 1722. [Abstract] [Full Text] [PDF]

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