Characterization of synapses in the rat subnucleus centralis of the nucleus tractus solitarius

Tanja Babic, Jason Ambler, Kirsteen N. Browning, R. Alberto Travagli

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

The nucleus tractus solitarius (NTS) receives subdiaphragmatic visceral sensory information via vagal A- or C-fibers. We have recently shown that, in contrast to cardiovascular NTS medialis neurons, which respond to either purinergic or vanilloid agonists, the majority of esophageal NTS centralis (cNTS) neurons respond to vanilloid agonists, whereas a smaller subset responds to both vanilloid and purinerigic agonists. The present study aimed to further investigate the neurochemical and synaptic characteristics of cNTS neurons using whole cell patchclamp, single cell RT-PCR and immunohistochemistry. Excitatory postsynaptic currents (EPSCs) were evoked in cNTS by tractus solitarius stimulation, and in 19 of 64 neurons perfusion with the purinergic agonist ab-methylene ATP (ab MeATP) increased the evoked EPSC amplitude significantly. Furthermore, neurons with ab MeATP-responsive synaptic inputs had different probabilities of release compared with nonresponsive neurons. Single cell RT-PCR revealed that 8 of 13 ab MeATP-responsive neurons expressed metabotropic glutamate receptor 8 (mGluR8) mRNA, which our previous studies have suggested is a marker of glutamatergic neurons, whereas only 3 of 13 expressed glutamic acid dehydroxylase, a marker of GABAergic neurons. A significantly lower proportion of ab MeATP-nonresponsive neurons expressed mGluR8 (2 of 30 neurons), whereas a greater proportion expressed glutamic acid dehydroxylase (12 of 30 neurons). Esophageal distension significantly increased the number of colocalized mGluR8- and c-Fos-immunoreactive neurons in the cNTS from 8.0 ± 4% to 20 ± 2.5%. These data indicate that cNTS comprises distinct neuronal subpopulations that can be distinguished based on their responses to purinergic agonists and that these subpopulations have distinct neurochemical and synaptic characteristics, suggesting that integration of sensory inputs from the esophagus relies on a discrete organization of synapses between vagal afferent fibers and cNTS neurons.

Original languageEnglish (US)
Pages (from-to)466-474
Number of pages9
JournalJournal of neurophysiology
Volume113
Issue number2
DOIs
StatePublished - Jan 15 2015

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Solitary Nucleus
Synapses
Neurons
Purinergic Agonists
Adenosine Triphosphate
Excitatory Postsynaptic Potentials
Glutamic Acid
GABAergic Neurons
Polymerase Chain Reaction
Unmyelinated Nerve Fibers
Esophagus

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Physiology

Cite this

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title = "Characterization of synapses in the rat subnucleus centralis of the nucleus tractus solitarius",
abstract = "The nucleus tractus solitarius (NTS) receives subdiaphragmatic visceral sensory information via vagal A- or C-fibers. We have recently shown that, in contrast to cardiovascular NTS medialis neurons, which respond to either purinergic or vanilloid agonists, the majority of esophageal NTS centralis (cNTS) neurons respond to vanilloid agonists, whereas a smaller subset responds to both vanilloid and purinerigic agonists. The present study aimed to further investigate the neurochemical and synaptic characteristics of cNTS neurons using whole cell patchclamp, single cell RT-PCR and immunohistochemistry. Excitatory postsynaptic currents (EPSCs) were evoked in cNTS by tractus solitarius stimulation, and in 19 of 64 neurons perfusion with the purinergic agonist ab-methylene ATP (ab MeATP) increased the evoked EPSC amplitude significantly. Furthermore, neurons with ab MeATP-responsive synaptic inputs had different probabilities of release compared with nonresponsive neurons. Single cell RT-PCR revealed that 8 of 13 ab MeATP-responsive neurons expressed metabotropic glutamate receptor 8 (mGluR8) mRNA, which our previous studies have suggested is a marker of glutamatergic neurons, whereas only 3 of 13 expressed glutamic acid dehydroxylase, a marker of GABAergic neurons. A significantly lower proportion of ab MeATP-nonresponsive neurons expressed mGluR8 (2 of 30 neurons), whereas a greater proportion expressed glutamic acid dehydroxylase (12 of 30 neurons). Esophageal distension significantly increased the number of colocalized mGluR8- and c-Fos-immunoreactive neurons in the cNTS from 8.0 ± 4{\%} to 20 ± 2.5{\%}. These data indicate that cNTS comprises distinct neuronal subpopulations that can be distinguished based on their responses to purinergic agonists and that these subpopulations have distinct neurochemical and synaptic characteristics, suggesting that integration of sensory inputs from the esophagus relies on a discrete organization of synapses between vagal afferent fibers and cNTS neurons.",
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Characterization of synapses in the rat subnucleus centralis of the nucleus tractus solitarius. / Babic, Tanja; Ambler, Jason; Browning, Kirsteen N.; Travagli, R. Alberto.

In: Journal of neurophysiology, Vol. 113, No. 2, 15.01.2015, p. 466-474.

Research output: Contribution to journalArticle

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