Ultrastructural immunocytochemical localization of μ-opioid receptors in dendritic targets of dopaminergic terminals in the rat caudate-putamen nucleus

H. Wang, A. Moriwaki, J. B. Wang, G. R. Uhl, V. M. Pickel

Research output: Contribution to journalArticle

Abstract

Many motor effects of opiates acting at μ-opioid receptors are thought to reflect functional interactions with dopaminergic inputs to the caudate- putamen nucleus. We examined the cellular and subcellular bases for this interaction in the rat caudate-putamen nucleus by dual immunocytochemical labelling for μ-opioid receptors and tyrosine hydroxylase, a marker mainly for dopamine in this region. μ-Opioid receptor-like immunoreactivity showed a patchy distribution by light microscopy. Within the patches, electron microscopy revealed that immunogold labelling for μ-opioid receptors was mainly distributed along extrasynaptic plasma membranes of medium spiny neurons. In contrast, immunoperoxidase labelling for tyrosine hydroxylase was exclusively located in axons and axon terminals without detectable μ-opioid receptor-like immunoreactivity. Forty-six percent of the total μ-opioid receptor-labelled neuronal profiles (n=1441) were in contact with tyrosine hydroxylase-immunoreactive axons and terminals. These contacts were characterized by closely apposed parallel plasma membrane segments, without well-defined synaptic junctions, or with punctate symmetric specializations. From 639 noted appositions, over 90% were between μ-opioid receptor-labelled dendrites and/or dendritic spines and tyrosine hydroxylase-containing terminals. The dendritic spines containing μ-opioid receptor-like immunoreactivity often received asymmetric synapses characteristic of excitatory inputs from unlabelled terminals. Axon terminals containing μ- opioid receptor-like immunoreactivity formed asymmetric synapses with dendritic spines, or apposed tyrosine hydroxylase-labelled terminals. Our results suggest that, in striatal patch compartments, μ-agonists and dopamine dually modulate the activity of single spiny neurons mainly through changes in their postsynaptic responses to excitatory inputs. In addition, our findings implicate μ-opioid receptors and dopamine in the presynaptic regulation of excitatory neurotransmitter release within the striatal patch compartments.

Original languageEnglish (US)
Pages (from-to)757-771
Number of pages15
JournalNeuroscience
Volume81
Issue number3
DOIs
StatePublished - Sep 26 1997

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Caudate Nucleus
Putamen
Opioid Receptors
Tyrosine 3-Monooxygenase
Dendritic Spines
Presynaptic Terminals
Corpus Striatum
Synapses
Opiate Alkaloids
Dopamine
Cell Membrane
Neurons
Dopamine Agonists
Dendrites
Neurotransmitter Agents
Axons
Microscopy
Electron Microscopy
Light

Keywords

  • Extrasynaptic site
  • Morphine
  • Nigrostriatal afferent
  • Stereotyped behaviour
  • Tyrosine hydroxylase
  • Ultrastructural localization

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Ultrastructural immunocytochemical localization of μ-opioid receptors in dendritic targets of dopaminergic terminals in the rat caudate-putamen nucleus. / Wang, H.; Moriwaki, A.; Wang, J. B.; Uhl, G. R.; Pickel, V. M.

In: Neuroscience, Vol. 81, No. 3, 26.09.1997, p. 757-771.

Research output: Contribution to journalArticle

Wang, H. ; Moriwaki, A. ; Wang, J. B. ; Uhl, G. R. ; Pickel, V. M. / Ultrastructural immunocytochemical localization of μ-opioid receptors in dendritic targets of dopaminergic terminals in the rat caudate-putamen nucleus. In: Neuroscience. 1997 ; Vol. 81, No. 3. pp. 757-771.
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abstract = "Many motor effects of opiates acting at μ-opioid receptors are thought to reflect functional interactions with dopaminergic inputs to the caudate- putamen nucleus. We examined the cellular and subcellular bases for this interaction in the rat caudate-putamen nucleus by dual immunocytochemical labelling for μ-opioid receptors and tyrosine hydroxylase, a marker mainly for dopamine in this region. μ-Opioid receptor-like immunoreactivity showed a patchy distribution by light microscopy. Within the patches, electron microscopy revealed that immunogold labelling for μ-opioid receptors was mainly distributed along extrasynaptic plasma membranes of medium spiny neurons. In contrast, immunoperoxidase labelling for tyrosine hydroxylase was exclusively located in axons and axon terminals without detectable μ-opioid receptor-like immunoreactivity. Forty-six percent of the total μ-opioid receptor-labelled neuronal profiles (n=1441) were in contact with tyrosine hydroxylase-immunoreactive axons and terminals. These contacts were characterized by closely apposed parallel plasma membrane segments, without well-defined synaptic junctions, or with punctate symmetric specializations. From 639 noted appositions, over 90{\%} were between μ-opioid receptor-labelled dendrites and/or dendritic spines and tyrosine hydroxylase-containing terminals. The dendritic spines containing μ-opioid receptor-like immunoreactivity often received asymmetric synapses characteristic of excitatory inputs from unlabelled terminals. Axon terminals containing μ- opioid receptor-like immunoreactivity formed asymmetric synapses with dendritic spines, or apposed tyrosine hydroxylase-labelled terminals. Our results suggest that, in striatal patch compartments, μ-agonists and dopamine dually modulate the activity of single spiny neurons mainly through changes in their postsynaptic responses to excitatory inputs. In addition, our findings implicate μ-opioid receptors and dopamine in the presynaptic regulation of excitatory neurotransmitter release within the striatal patch compartments.",
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AB - Many motor effects of opiates acting at μ-opioid receptors are thought to reflect functional interactions with dopaminergic inputs to the caudate- putamen nucleus. We examined the cellular and subcellular bases for this interaction in the rat caudate-putamen nucleus by dual immunocytochemical labelling for μ-opioid receptors and tyrosine hydroxylase, a marker mainly for dopamine in this region. μ-Opioid receptor-like immunoreactivity showed a patchy distribution by light microscopy. Within the patches, electron microscopy revealed that immunogold labelling for μ-opioid receptors was mainly distributed along extrasynaptic plasma membranes of medium spiny neurons. In contrast, immunoperoxidase labelling for tyrosine hydroxylase was exclusively located in axons and axon terminals without detectable μ-opioid receptor-like immunoreactivity. Forty-six percent of the total μ-opioid receptor-labelled neuronal profiles (n=1441) were in contact with tyrosine hydroxylase-immunoreactive axons and terminals. These contacts were characterized by closely apposed parallel plasma membrane segments, without well-defined synaptic junctions, or with punctate symmetric specializations. From 639 noted appositions, over 90% were between μ-opioid receptor-labelled dendrites and/or dendritic spines and tyrosine hydroxylase-containing terminals. The dendritic spines containing μ-opioid receptor-like immunoreactivity often received asymmetric synapses characteristic of excitatory inputs from unlabelled terminals. Axon terminals containing μ- opioid receptor-like immunoreactivity formed asymmetric synapses with dendritic spines, or apposed tyrosine hydroxylase-labelled terminals. Our results suggest that, in striatal patch compartments, μ-agonists and dopamine dually modulate the activity of single spiny neurons mainly through changes in their postsynaptic responses to excitatory inputs. In addition, our findings implicate μ-opioid receptors and dopamine in the presynaptic regulation of excitatory neurotransmitter release within the striatal patch compartments.

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