MOR-1-immunoreactive neurons in the dorsal horn of the rat spinal cord

Evidence for nonsynaptic innervation by substance P-containing primary afferents and for selective activation by noxious thermal stimuli

R. C. Spike, Z. Puskár, H. Sakamoto, W. Stewart, C. Watt, A. J. Todd

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Abstract

A direct action of μ-opioid agonists on neurons in the spinal dorsal horn is thought to contribute to opiate-induced analgesia. In this study we have investigated neurons that express the μ-opioid receptor MOR-1 in rat spinal cord to provide further evidence about their role in nociceptive processing. MOR-1-immunoreactive cells were largely restricted to lamina II, where they comprised approximately 10% of the neuronal population. The cells received few contacts from nonpeptidergic unmyelinated afferents, but many from substance P-containing afferents. However, electron microscopy revealed that most of these contacts were not associated with synapses. None of the MOR-1 cells in lamina II expressed the neurokinin 1 receptor; however, the μ-selective opioid peptide endomorphin-2 was present in the majority (62-82%) of substance P axons that contacted them. Noxious thermal stimulation of the foot induced c-Fos expression in approximately 15% of MOR-1 cells in the medial third of the ipsilateral dorsal horn at mid-lumbar level. However, following pinching of the foot or intraplantar injection of formalin very few MOR-1 cells expressed c-Fos, and for intraplantar formalin injection this result was not altered significantly by pretreatment with systemic naloxone. Although these findings indicate that at least some of the neurons in lamina II with MOR-1 are activated by noxious thermal stimulation, the results do not support the hypothesis that the cells have a role in transmitting nociceptive information following acute mechanical or chemical noxious stimuli.

Original languageEnglish
Pages (from-to)1306-1316
Number of pages11
JournalEuropean Journal of Neuroscience
Volume15
Issue number8
DOIs
Publication statusPublished - 2002

Fingerprint

Posterior Horn Cells
Substance P
Hot Temperature
Substantia Gelatinosa
Neurons
Formaldehyde
Opiate Alkaloids
Foot
Neurokinin-1 Receptors
Injections
Opioid Peptides
Opioid Receptors
Naloxone
Synapses
Analgesia
Opioid Analgesics
Axons
Spinal Cord Dorsal Horn
Spinal Cord
Electron Microscopy

Keywords

  • Analgesia
  • c-Fos
  • Endomorphin-2
  • Lamina II
  • Morphine

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

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title = "MOR-1-immunoreactive neurons in the dorsal horn of the rat spinal cord: Evidence for nonsynaptic innervation by substance P-containing primary afferents and for selective activation by noxious thermal stimuli",
abstract = "A direct action of μ-opioid agonists on neurons in the spinal dorsal horn is thought to contribute to opiate-induced analgesia. In this study we have investigated neurons that express the μ-opioid receptor MOR-1 in rat spinal cord to provide further evidence about their role in nociceptive processing. MOR-1-immunoreactive cells were largely restricted to lamina II, where they comprised approximately 10{\%} of the neuronal population. The cells received few contacts from nonpeptidergic unmyelinated afferents, but many from substance P-containing afferents. However, electron microscopy revealed that most of these contacts were not associated with synapses. None of the MOR-1 cells in lamina II expressed the neurokinin 1 receptor; however, the μ-selective opioid peptide endomorphin-2 was present in the majority (62-82{\%}) of substance P axons that contacted them. Noxious thermal stimulation of the foot induced c-Fos expression in approximately 15{\%} of MOR-1 cells in the medial third of the ipsilateral dorsal horn at mid-lumbar level. However, following pinching of the foot or intraplantar injection of formalin very few MOR-1 cells expressed c-Fos, and for intraplantar formalin injection this result was not altered significantly by pretreatment with systemic naloxone. Although these findings indicate that at least some of the neurons in lamina II with MOR-1 are activated by noxious thermal stimulation, the results do not support the hypothesis that the cells have a role in transmitting nociceptive information following acute mechanical or chemical noxious stimuli.",
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T2 - Evidence for nonsynaptic innervation by substance P-containing primary afferents and for selective activation by noxious thermal stimuli

AU - Spike, R. C.

AU - Puskár, Z.

AU - Sakamoto, H.

AU - Stewart, W.

AU - Watt, C.

AU - Todd, A. J.

PY - 2002

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N2 - A direct action of μ-opioid agonists on neurons in the spinal dorsal horn is thought to contribute to opiate-induced analgesia. In this study we have investigated neurons that express the μ-opioid receptor MOR-1 in rat spinal cord to provide further evidence about their role in nociceptive processing. MOR-1-immunoreactive cells were largely restricted to lamina II, where they comprised approximately 10% of the neuronal population. The cells received few contacts from nonpeptidergic unmyelinated afferents, but many from substance P-containing afferents. However, electron microscopy revealed that most of these contacts were not associated with synapses. None of the MOR-1 cells in lamina II expressed the neurokinin 1 receptor; however, the μ-selective opioid peptide endomorphin-2 was present in the majority (62-82%) of substance P axons that contacted them. Noxious thermal stimulation of the foot induced c-Fos expression in approximately 15% of MOR-1 cells in the medial third of the ipsilateral dorsal horn at mid-lumbar level. However, following pinching of the foot or intraplantar injection of formalin very few MOR-1 cells expressed c-Fos, and for intraplantar formalin injection this result was not altered significantly by pretreatment with systemic naloxone. Although these findings indicate that at least some of the neurons in lamina II with MOR-1 are activated by noxious thermal stimulation, the results do not support the hypothesis that the cells have a role in transmitting nociceptive information following acute mechanical or chemical noxious stimuli.

AB - A direct action of μ-opioid agonists on neurons in the spinal dorsal horn is thought to contribute to opiate-induced analgesia. In this study we have investigated neurons that express the μ-opioid receptor MOR-1 in rat spinal cord to provide further evidence about their role in nociceptive processing. MOR-1-immunoreactive cells were largely restricted to lamina II, where they comprised approximately 10% of the neuronal population. The cells received few contacts from nonpeptidergic unmyelinated afferents, but many from substance P-containing afferents. However, electron microscopy revealed that most of these contacts were not associated with synapses. None of the MOR-1 cells in lamina II expressed the neurokinin 1 receptor; however, the μ-selective opioid peptide endomorphin-2 was present in the majority (62-82%) of substance P axons that contacted them. Noxious thermal stimulation of the foot induced c-Fos expression in approximately 15% of MOR-1 cells in the medial third of the ipsilateral dorsal horn at mid-lumbar level. However, following pinching of the foot or intraplantar injection of formalin very few MOR-1 cells expressed c-Fos, and for intraplantar formalin injection this result was not altered significantly by pretreatment with systemic naloxone. Although these findings indicate that at least some of the neurons in lamina II with MOR-1 are activated by noxious thermal stimulation, the results do not support the hypothesis that the cells have a role in transmitting nociceptive information following acute mechanical or chemical noxious stimuli.

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