Visceral afferents directly activate catecholamine neurons in the solitary tract nucleus

Suzanne M. Appleyard, Daniel Marks, Kazuto Kobayashi, Hideyuki Okano, Malcolm J. Low, Michael C. Andresen

Research output: Contribution to journalArticle

80 Citations (Scopus)

Abstract

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 (IKA), 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.

Original languageEnglish
Pages (from-to)13292-13302
Number of pages11
JournalJournal of Neuroscience
Volume27
Issue number48
DOIs
Publication statusPublished - 2007 Nov 28

Fingerprint

Visceral Afferents
Solitary Nucleus
Catecholamines
Neurons
Action Potentials
Shock
Presynaptic Receptors
Peptide Receptors
Potassium Channels
Cholecystokinin
Tyrosine 3-Monooxygenase
Evoked Potentials
varespladib methyl

Keywords

  • Autonomic
  • Cardiovascular
  • Food intake
  • NTS
  • Tyrosine hydroxylase
  • Vagus

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Visceral afferents directly activate catecholamine neurons in the solitary tract nucleus. / Appleyard, Suzanne M.; Marks, Daniel; Kobayashi, Kazuto; Okano, Hideyuki; Low, Malcolm J.; Andresen, Michael C.

In: Journal of Neuroscience, Vol. 27, No. 48, 28.11.2007, p. 13292-13302.

Research output: Contribution to journalArticle

Appleyard, Suzanne M. ; Marks, Daniel ; Kobayashi, Kazuto ; Okano, Hideyuki ; Low, Malcolm J. ; Andresen, Michael C. / Visceral afferents directly activate catecholamine neurons in the solitary tract nucleus. In: Journal of Neuroscience. 2007 ; Vol. 27, No. 48. pp. 13292-13302.
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