Tonic control of peripheral cutaneous nociceptors by somatostatin receptors

Susan M. Carlton, Junhui Du, Shengtai Zhou, Richard E. Coggeshall

Research output: Contribution to journalArticle

75 Citations (Scopus)

Abstract

The peptide somatostatin [somatotropin release-inhibiting factor (SRIF)] is widely distributed in the body and exerts a variety of hormonal and neural actions. Several lines of evidence indicate that SRIF is important in nociceptive processing: (1) it is localized in a subset of small-diameter dorsal root ganglion cells; (2) activation of SRIF receptors results in inhibition of both nociceptive behaviors in animals and acute and chronic pain in humans; (3) SRIF inhibits dorsal horn neuronal activity; and (4) SRIF reduces responses of joint mechanoreceptors to noxious rotation of the knee joint. The goal of the present study is to show that cutaneous nociceptors are under the tonic inhibitory control of SRIF. This is accomplished using behavioral and electrophysiological paradigms. In a dose-dependent manner, intraplantar injection of the SRIF receptor antagonist cyclosomatostatin (c-SOM) results in nociceptive behaviors in normal animals and enhancement of nociceptive behaviors in formalin-injected animals, and these actions can be blocked when c-SOM is coapplied with three different SRIF agonists. Furthermore, intraplantar injection of SRIF antiserum also results in nociceptive behaviors. Electrophysiological recordings using an in vitro glabrous skin-nerve preparation show increased nociceptor activity in response to c-SOM, and this increase is blocked by the same three SRIF agonists. Parallel behavioral and electrophysiological studies using the opioid antagonist naloxone demonstrate that endogenous opioids do not maintain a tonic inhibitory control over peripheral nociceptors, nor does opioid receptor antagonism influence peripheral SRIF effects on nociceptors. These findings demonstrate that SRIF receptors maintain a tonic inhibitory control over peripheral nociceptors, and this may contribute to mechanisms that control the excitability of these terminals.

Original languageEnglish (US)
Pages (from-to)4042-4049
Number of pages8
JournalJournal of Neuroscience
Volume21
Issue number11
StatePublished - Jun 1 2001

Fingerprint

Somatostatin Receptors
Nociceptors
Somatostatin
Skin
Animal Behavior
Mechanoreceptors
Injections
Narcotic Antagonists
Acute Pain
Spinal Ganglia
Opioid Receptors
Naloxone
Knee Joint
Chronic Pain
Opioid Analgesics
Formaldehyde
Immune Sera

Keywords

  • Cutaneous
  • Inhibitory peptides
  • Nociception
  • Opioid
  • Primary afferent
  • Sensory neurons

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Carlton, S. M., Du, J., Zhou, S., & Coggeshall, R. E. (2001). Tonic control of peripheral cutaneous nociceptors by somatostatin receptors. Journal of Neuroscience, 21(11), 4042-4049.

Tonic control of peripheral cutaneous nociceptors by somatostatin receptors. / Carlton, Susan M.; Du, Junhui; Zhou, Shengtai; Coggeshall, Richard E.

In: Journal of Neuroscience, Vol. 21, No. 11, 01.06.2001, p. 4042-4049.

Research output: Contribution to journalArticle

Carlton, SM, Du, J, Zhou, S & Coggeshall, RE 2001, 'Tonic control of peripheral cutaneous nociceptors by somatostatin receptors', Journal of Neuroscience, vol. 21, no. 11, pp. 4042-4049.
Carlton SM, Du J, Zhou S, Coggeshall RE. Tonic control of peripheral cutaneous nociceptors by somatostatin receptors. Journal of Neuroscience. 2001 Jun 1;21(11):4042-4049.
Carlton, Susan M. ; Du, Junhui ; Zhou, Shengtai ; Coggeshall, Richard E. / Tonic control of peripheral cutaneous nociceptors by somatostatin receptors. In: Journal of Neuroscience. 2001 ; Vol. 21, No. 11. pp. 4042-4049.
@article{145075c3943a4295ab55014506157962,
title = "Tonic control of peripheral cutaneous nociceptors by somatostatin receptors",
abstract = "The peptide somatostatin [somatotropin release-inhibiting factor (SRIF)] is widely distributed in the body and exerts a variety of hormonal and neural actions. Several lines of evidence indicate that SRIF is important in nociceptive processing: (1) it is localized in a subset of small-diameter dorsal root ganglion cells; (2) activation of SRIF receptors results in inhibition of both nociceptive behaviors in animals and acute and chronic pain in humans; (3) SRIF inhibits dorsal horn neuronal activity; and (4) SRIF reduces responses of joint mechanoreceptors to noxious rotation of the knee joint. The goal of the present study is to show that cutaneous nociceptors are under the tonic inhibitory control of SRIF. This is accomplished using behavioral and electrophysiological paradigms. In a dose-dependent manner, intraplantar injection of the SRIF receptor antagonist cyclosomatostatin (c-SOM) results in nociceptive behaviors in normal animals and enhancement of nociceptive behaviors in formalin-injected animals, and these actions can be blocked when c-SOM is coapplied with three different SRIF agonists. Furthermore, intraplantar injection of SRIF antiserum also results in nociceptive behaviors. Electrophysiological recordings using an in vitro glabrous skin-nerve preparation show increased nociceptor activity in response to c-SOM, and this increase is blocked by the same three SRIF agonists. Parallel behavioral and electrophysiological studies using the opioid antagonist naloxone demonstrate that endogenous opioids do not maintain a tonic inhibitory control over peripheral nociceptors, nor does opioid receptor antagonism influence peripheral SRIF effects on nociceptors. These findings demonstrate that SRIF receptors maintain a tonic inhibitory control over peripheral nociceptors, and this may contribute to mechanisms that control the excitability of these terminals.",
keywords = "Cutaneous, Inhibitory peptides, Nociception, Opioid, Primary afferent, Sensory neurons",
author = "Carlton, {Susan M.} and Junhui Du and Shengtai Zhou and Coggeshall, {Richard E.}",
year = "2001",
month = "6",
day = "1",
language = "English (US)",
volume = "21",
pages = "4042--4049",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "11",

}

TY - JOUR

T1 - Tonic control of peripheral cutaneous nociceptors by somatostatin receptors

AU - Carlton, Susan M.

AU - Du, Junhui

AU - Zhou, Shengtai

AU - Coggeshall, Richard E.

PY - 2001/6/1

Y1 - 2001/6/1

N2 - The peptide somatostatin [somatotropin release-inhibiting factor (SRIF)] is widely distributed in the body and exerts a variety of hormonal and neural actions. Several lines of evidence indicate that SRIF is important in nociceptive processing: (1) it is localized in a subset of small-diameter dorsal root ganglion cells; (2) activation of SRIF receptors results in inhibition of both nociceptive behaviors in animals and acute and chronic pain in humans; (3) SRIF inhibits dorsal horn neuronal activity; and (4) SRIF reduces responses of joint mechanoreceptors to noxious rotation of the knee joint. The goal of the present study is to show that cutaneous nociceptors are under the tonic inhibitory control of SRIF. This is accomplished using behavioral and electrophysiological paradigms. In a dose-dependent manner, intraplantar injection of the SRIF receptor antagonist cyclosomatostatin (c-SOM) results in nociceptive behaviors in normal animals and enhancement of nociceptive behaviors in formalin-injected animals, and these actions can be blocked when c-SOM is coapplied with three different SRIF agonists. Furthermore, intraplantar injection of SRIF antiserum also results in nociceptive behaviors. Electrophysiological recordings using an in vitro glabrous skin-nerve preparation show increased nociceptor activity in response to c-SOM, and this increase is blocked by the same three SRIF agonists. Parallel behavioral and electrophysiological studies using the opioid antagonist naloxone demonstrate that endogenous opioids do not maintain a tonic inhibitory control over peripheral nociceptors, nor does opioid receptor antagonism influence peripheral SRIF effects on nociceptors. These findings demonstrate that SRIF receptors maintain a tonic inhibitory control over peripheral nociceptors, and this may contribute to mechanisms that control the excitability of these terminals.

AB - The peptide somatostatin [somatotropin release-inhibiting factor (SRIF)] is widely distributed in the body and exerts a variety of hormonal and neural actions. Several lines of evidence indicate that SRIF is important in nociceptive processing: (1) it is localized in a subset of small-diameter dorsal root ganglion cells; (2) activation of SRIF receptors results in inhibition of both nociceptive behaviors in animals and acute and chronic pain in humans; (3) SRIF inhibits dorsal horn neuronal activity; and (4) SRIF reduces responses of joint mechanoreceptors to noxious rotation of the knee joint. The goal of the present study is to show that cutaneous nociceptors are under the tonic inhibitory control of SRIF. This is accomplished using behavioral and electrophysiological paradigms. In a dose-dependent manner, intraplantar injection of the SRIF receptor antagonist cyclosomatostatin (c-SOM) results in nociceptive behaviors in normal animals and enhancement of nociceptive behaviors in formalin-injected animals, and these actions can be blocked when c-SOM is coapplied with three different SRIF agonists. Furthermore, intraplantar injection of SRIF antiserum also results in nociceptive behaviors. Electrophysiological recordings using an in vitro glabrous skin-nerve preparation show increased nociceptor activity in response to c-SOM, and this increase is blocked by the same three SRIF agonists. Parallel behavioral and electrophysiological studies using the opioid antagonist naloxone demonstrate that endogenous opioids do not maintain a tonic inhibitory control over peripheral nociceptors, nor does opioid receptor antagonism influence peripheral SRIF effects on nociceptors. These findings demonstrate that SRIF receptors maintain a tonic inhibitory control over peripheral nociceptors, and this may contribute to mechanisms that control the excitability of these terminals.

KW - Cutaneous

KW - Inhibitory peptides

KW - Nociception

KW - Opioid

KW - Primary afferent

KW - Sensory neurons

UR - http://www.scopus.com/inward/record.url?scp=0035370726&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0035370726&partnerID=8YFLogxK

M3 - Article

C2 - 11356891

AN - SCOPUS:0035370726

VL - 21

SP - 4042

EP - 4049

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 11

ER -