Responses of adult human dorsal root ganglion neurons in culture to capsaicin and low pH

Thomas K. Baumann, Kim Burchiel, Susan Ingram, Melissa E. Martenson

Research output: Contribution to journalArticle

54 Citations (Scopus)

Abstract

This study examined the responses of cultured adult human dorsal root ganglion (hDRG) neurons to protons and capsaicin, two substances known to produce pain and hyperalgesia in humans. Both substances were applied to each neuron and responses were examined under both voltage- and current-clamp recording conditions. Sensitivity to protons was tested with rapid acidification of the extracellular fluid from pH 7.35 to 6.0. In neurons nominally clamped near -60 mV, low pH evoked a transient inward current which, in all 40 hDRG neurons tested, was followed by a more sustained inward current. The sustained current was associated with an increase in membrane conductance in 10 neurons, a decrease in 27 neurons, and no overt change in conductance (<10%) in 3 neurons. Current-clamp recordings in the same neurons showed that the proton-induced sustained net inward current caused a prolonged depolarization of the membrane potential in all 40 hDRG neurons. The prolonged depolarization was associated with action potential discharge in 5 neurons. Unlike low pH, capsaicin evoked a sustained net inward current in only a subset of neurons tested (10 nM: 1/4, 30 nM: 4/8, 100 nM: 11/18, and 10 μM: 10/10 neurons tested). The capsaicin-evoked currents were accompanied by an increase in membrane conductance in 15 neurons, a decrease in 2, and no overt change in conductance in 9 neurons. Capsaicin currents, like proton-induced currents, resulted in prolonged depolarizations (10 nM: 0/4, 30 nM: 5/8, 100 nM: 8/18, and 10 μM: 10/10 neurons tested). The depolarization resulted-in the discharge of action potentials in 14 neurons. It is concluded that, while both protons and capsaicin exert excitatory effects on human sensory neurons, multiple membrane mechanisms lead to the depolarization of cultured hDRG neurons by low pH. Inhibition of resting membrane conductances contributes to the responses to low pH in some hDRG neurons.

Original languageEnglish (US)
Pages (from-to)31-38
Number of pages8
JournalPain
Volume65
Issue number1
DOIs
StatePublished - Apr 1996

Fingerprint

Capsaicin
Spinal Ganglia
Neurons
Protons
Membranes
Action Potentials
Hyperalgesia
Extracellular Fluid
Sensory Receptor Cells

Keywords

  • Action potential
  • Capsaicin
  • Chemosensitivity
  • Ganglionectomy
  • Human
  • Pain
  • Patch clamp
  • Protons
  • Spinal ganglion

ASJC Scopus subject areas

  • Clinical Neurology
  • Psychiatry and Mental health
  • Neurology
  • Neuroscience(all)
  • Pharmacology
  • Clinical Psychology

Cite this

Responses of adult human dorsal root ganglion neurons in culture to capsaicin and low pH. / Baumann, Thomas K.; Burchiel, Kim; Ingram, Susan; Martenson, Melissa E.

In: Pain, Vol. 65, No. 1, 04.1996, p. 31-38.

Research output: Contribution to journalArticle

Baumann, Thomas K. ; Burchiel, Kim ; Ingram, Susan ; Martenson, Melissa E. / Responses of adult human dorsal root ganglion neurons in culture to capsaicin and low pH. In: Pain. 1996 ; Vol. 65, No. 1. pp. 31-38.
@article{8dd9b0e0b8654b81955622108633048b,
title = "Responses of adult human dorsal root ganglion neurons in culture to capsaicin and low pH",
abstract = "This study examined the responses of cultured adult human dorsal root ganglion (hDRG) neurons to protons and capsaicin, two substances known to produce pain and hyperalgesia in humans. Both substances were applied to each neuron and responses were examined under both voltage- and current-clamp recording conditions. Sensitivity to protons was tested with rapid acidification of the extracellular fluid from pH 7.35 to 6.0. In neurons nominally clamped near -60 mV, low pH evoked a transient inward current which, in all 40 hDRG neurons tested, was followed by a more sustained inward current. The sustained current was associated with an increase in membrane conductance in 10 neurons, a decrease in 27 neurons, and no overt change in conductance (<10{\%}) in 3 neurons. Current-clamp recordings in the same neurons showed that the proton-induced sustained net inward current caused a prolonged depolarization of the membrane potential in all 40 hDRG neurons. The prolonged depolarization was associated with action potential discharge in 5 neurons. Unlike low pH, capsaicin evoked a sustained net inward current in only a subset of neurons tested (10 nM: 1/4, 30 nM: 4/8, 100 nM: 11/18, and 10 μM: 10/10 neurons tested). The capsaicin-evoked currents were accompanied by an increase in membrane conductance in 15 neurons, a decrease in 2, and no overt change in conductance in 9 neurons. Capsaicin currents, like proton-induced currents, resulted in prolonged depolarizations (10 nM: 0/4, 30 nM: 5/8, 100 nM: 8/18, and 10 μM: 10/10 neurons tested). The depolarization resulted-in the discharge of action potentials in 14 neurons. It is concluded that, while both protons and capsaicin exert excitatory effects on human sensory neurons, multiple membrane mechanisms lead to the depolarization of cultured hDRG neurons by low pH. Inhibition of resting membrane conductances contributes to the responses to low pH in some hDRG neurons.",
keywords = "Action potential, Capsaicin, Chemosensitivity, Ganglionectomy, Human, Pain, Patch clamp, Protons, Spinal ganglion",
author = "Baumann, {Thomas K.} and Kim Burchiel and Susan Ingram and Martenson, {Melissa E.}",
year = "1996",
month = "4",
doi = "10.1016/0304-3959(95)00145-X",
language = "English (US)",
volume = "65",
pages = "31--38",
journal = "Pain",
issn = "0304-3959",
publisher = "Elsevier",
number = "1",

}

TY - JOUR

T1 - Responses of adult human dorsal root ganglion neurons in culture to capsaicin and low pH

AU - Baumann, Thomas K.

AU - Burchiel, Kim

AU - Ingram, Susan

AU - Martenson, Melissa E.

PY - 1996/4

Y1 - 1996/4

N2 - This study examined the responses of cultured adult human dorsal root ganglion (hDRG) neurons to protons and capsaicin, two substances known to produce pain and hyperalgesia in humans. Both substances were applied to each neuron and responses were examined under both voltage- and current-clamp recording conditions. Sensitivity to protons was tested with rapid acidification of the extracellular fluid from pH 7.35 to 6.0. In neurons nominally clamped near -60 mV, low pH evoked a transient inward current which, in all 40 hDRG neurons tested, was followed by a more sustained inward current. The sustained current was associated with an increase in membrane conductance in 10 neurons, a decrease in 27 neurons, and no overt change in conductance (<10%) in 3 neurons. Current-clamp recordings in the same neurons showed that the proton-induced sustained net inward current caused a prolonged depolarization of the membrane potential in all 40 hDRG neurons. The prolonged depolarization was associated with action potential discharge in 5 neurons. Unlike low pH, capsaicin evoked a sustained net inward current in only a subset of neurons tested (10 nM: 1/4, 30 nM: 4/8, 100 nM: 11/18, and 10 μM: 10/10 neurons tested). The capsaicin-evoked currents were accompanied by an increase in membrane conductance in 15 neurons, a decrease in 2, and no overt change in conductance in 9 neurons. Capsaicin currents, like proton-induced currents, resulted in prolonged depolarizations (10 nM: 0/4, 30 nM: 5/8, 100 nM: 8/18, and 10 μM: 10/10 neurons tested). The depolarization resulted-in the discharge of action potentials in 14 neurons. It is concluded that, while both protons and capsaicin exert excitatory effects on human sensory neurons, multiple membrane mechanisms lead to the depolarization of cultured hDRG neurons by low pH. Inhibition of resting membrane conductances contributes to the responses to low pH in some hDRG neurons.

AB - This study examined the responses of cultured adult human dorsal root ganglion (hDRG) neurons to protons and capsaicin, two substances known to produce pain and hyperalgesia in humans. Both substances were applied to each neuron and responses were examined under both voltage- and current-clamp recording conditions. Sensitivity to protons was tested with rapid acidification of the extracellular fluid from pH 7.35 to 6.0. In neurons nominally clamped near -60 mV, low pH evoked a transient inward current which, in all 40 hDRG neurons tested, was followed by a more sustained inward current. The sustained current was associated with an increase in membrane conductance in 10 neurons, a decrease in 27 neurons, and no overt change in conductance (<10%) in 3 neurons. Current-clamp recordings in the same neurons showed that the proton-induced sustained net inward current caused a prolonged depolarization of the membrane potential in all 40 hDRG neurons. The prolonged depolarization was associated with action potential discharge in 5 neurons. Unlike low pH, capsaicin evoked a sustained net inward current in only a subset of neurons tested (10 nM: 1/4, 30 nM: 4/8, 100 nM: 11/18, and 10 μM: 10/10 neurons tested). The capsaicin-evoked currents were accompanied by an increase in membrane conductance in 15 neurons, a decrease in 2, and no overt change in conductance in 9 neurons. Capsaicin currents, like proton-induced currents, resulted in prolonged depolarizations (10 nM: 0/4, 30 nM: 5/8, 100 nM: 8/18, and 10 μM: 10/10 neurons tested). The depolarization resulted-in the discharge of action potentials in 14 neurons. It is concluded that, while both protons and capsaicin exert excitatory effects on human sensory neurons, multiple membrane mechanisms lead to the depolarization of cultured hDRG neurons by low pH. Inhibition of resting membrane conductances contributes to the responses to low pH in some hDRG neurons.

KW - Action potential

KW - Capsaicin

KW - Chemosensitivity

KW - Ganglionectomy

KW - Human

KW - Pain

KW - Patch clamp

KW - Protons

KW - Spinal ganglion

UR - http://www.scopus.com/inward/record.url?scp=0030130917&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0030130917&partnerID=8YFLogxK

U2 - 10.1016/0304-3959(95)00145-X

DO - 10.1016/0304-3959(95)00145-X

M3 - Article

VL - 65

SP - 31

EP - 38

JO - Pain

JF - Pain

SN - 0304-3959

IS - 1

ER -