Monosynaptic excitatory connection from the rostral ventrolateral medulla to sympathetic preganglionic neurons revealed by simultaneous recordings

Naoki Oshima, Hiroo Kumagai, Hiroshi Onimaru, Akira Kawai, Paul M. Pilowsky, Kamon Iigaya, Chie Takimoto, Koichi Hayashi, Takao Saruta, Hiroshi Itoh

Research output: Contribution to journalArticle

29 Citations (Scopus)

Abstract

To directly investigate whether a monosynaptic connection exists between neurons in the rostral ventrolateral medulla (RVLM) and sympathetic preganglionic neurons (SPNs), we used simultaneous extracellular recordings of RVLM neurons and whole-cell patch-clamp recordings of SPNs at the Th2 level and analyzed them by spike-triggered averaging. We averaged 200 sweeps of membrane potentials in SPN triggered by the spikes in the RVLM neuron. No clear postsynaptic potentials were detected in the averaged wave of SPNs before angiotensin II (Ang II) superfusion, whereas during superfusion with Ang II (6 μmol/L) on the medulla oblongata side alone excitatory postsynaptic potentials (EPSPs) were clearly found in the SPN of 3 out of 10 pairs at 40±1 ms after the averaged triggering spike in the RVLM neuron. We consider them to be monosynaptic EPSPs, because 1) the averaged EPSPs exhibited a sharp rise time, 2) the onset latency of the averaged EPSPs in the SPNs after the trigger spike in the RVLM was the same as the latency of the antidromic action potentials in the RVLM neurons in response to electrical stimulation of the SPNs, and 3) the amplitude of the averaged EPSPs was over 2 mV. In summary, combining simultaneous recording and spike-triggered averaging allowed us to demonstrate a monosynaptic excitatory connection between a single RVLM neuron and a single SPN in the thoracic spinal cord. Such connections provide the basis for the maintenance of sympathetic tone and the integrative reflex that relays through the RVLM. The results explain the mechanism by which Ang II in the RVLM area increases peripheral sympathetic activity and blood pressure.

Original languageEnglish
Pages (from-to)1445-1454
Number of pages10
JournalHypertension Research
Volume31
Issue number7
DOIs
Publication statusPublished - 2008

Fingerprint

Neurons
Excitatory Postsynaptic Potentials
Angiotensin II
Synaptic Potentials
Medulla Oblongata
Membrane Potentials
Electric Stimulation
Action Potentials
Reflex
Spinal Cord
Thorax
Maintenance
Blood Pressure

Keywords

  • Angiotensin II
  • Brainstem-spinal cord preparation
  • Excitatory postsynaptic potential
  • Spike-triggered averaging
  • Whole-cell patch-clamp technique

ASJC Scopus subject areas

  • Internal Medicine
  • Physiology
  • Cardiology and Cardiovascular Medicine

Cite this

Monosynaptic excitatory connection from the rostral ventrolateral medulla to sympathetic preganglionic neurons revealed by simultaneous recordings. / Oshima, Naoki; Kumagai, Hiroo; Onimaru, Hiroshi; Kawai, Akira; Pilowsky, Paul M.; Iigaya, Kamon; Takimoto, Chie; Hayashi, Koichi; Saruta, Takao; Itoh, Hiroshi.

In: Hypertension Research, Vol. 31, No. 7, 2008, p. 1445-1454.

Research output: Contribution to journalArticle

Oshima, N, Kumagai, H, Onimaru, H, Kawai, A, Pilowsky, PM, Iigaya, K, Takimoto, C, Hayashi, K, Saruta, T & Itoh, H 2008, 'Monosynaptic excitatory connection from the rostral ventrolateral medulla to sympathetic preganglionic neurons revealed by simultaneous recordings', Hypertension Research, vol. 31, no. 7, pp. 1445-1454. https://doi.org/10.1291/hypres.31.1445
Oshima, Naoki ; Kumagai, Hiroo ; Onimaru, Hiroshi ; Kawai, Akira ; Pilowsky, Paul M. ; Iigaya, Kamon ; Takimoto, Chie ; Hayashi, Koichi ; Saruta, Takao ; Itoh, Hiroshi. / Monosynaptic excitatory connection from the rostral ventrolateral medulla to sympathetic preganglionic neurons revealed by simultaneous recordings. In: Hypertension Research. 2008 ; Vol. 31, No. 7. pp. 1445-1454.
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abstract = "To directly investigate whether a monosynaptic connection exists between neurons in the rostral ventrolateral medulla (RVLM) and sympathetic preganglionic neurons (SPNs), we used simultaneous extracellular recordings of RVLM neurons and whole-cell patch-clamp recordings of SPNs at the Th2 level and analyzed them by spike-triggered averaging. We averaged 200 sweeps of membrane potentials in SPN triggered by the spikes in the RVLM neuron. No clear postsynaptic potentials were detected in the averaged wave of SPNs before angiotensin II (Ang II) superfusion, whereas during superfusion with Ang II (6 μmol/L) on the medulla oblongata side alone excitatory postsynaptic potentials (EPSPs) were clearly found in the SPN of 3 out of 10 pairs at 40±1 ms after the averaged triggering spike in the RVLM neuron. We consider them to be monosynaptic EPSPs, because 1) the averaged EPSPs exhibited a sharp rise time, 2) the onset latency of the averaged EPSPs in the SPNs after the trigger spike in the RVLM was the same as the latency of the antidromic action potentials in the RVLM neurons in response to electrical stimulation of the SPNs, and 3) the amplitude of the averaged EPSPs was over 2 mV. In summary, combining simultaneous recording and spike-triggered averaging allowed us to demonstrate a monosynaptic excitatory connection between a single RVLM neuron and a single SPN in the thoracic spinal cord. Such connections provide the basis for the maintenance of sympathetic tone and the integrative reflex that relays through the RVLM. The results explain the mechanism by which Ang II in the RVLM area increases peripheral sympathetic activity and blood pressure.",
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AU - Pilowsky, Paul M.

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