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Volume 17, Number 7, Issue of April 1, 1997 pp. 2585-2594
Copyright ©1997 Society for Neuroscience

µ-Opioid Receptors Are Localized to Extrasynaptic Plasma Membranes of GABAergic Neurons and Their Targets in the Rat Nucleus Accumbens

Received Dec. 9, 1996; revised Jan. 14, 1997; accepted Jan. 16, 1997.

Adena L. Svingos¹, Akiyoshi Moriwaki², Jia Bei Wang², George R. Uhl², and Virginia M. Pickel¹

¹ Division of Neurobiology, Department of Neurology and Neuroscience, Cornell University Medical Center, New York, New York 10021, and ² Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health, Bethesda, Maryland 20892, and Departments of Neurology and Neuroscience, Johns Hopkins University, Baltimore, Maryland 21224

The activation of µ-opioid receptors in the nucleus accumbens (Acb) produces changes in locomotor and rewarding responses that are believed to involve neurons, including local -aminobutyric acid (GABA)ergic neurons. We combined immunogold-silver detection of an antipeptide antiserum against the cloned µ-opioid receptor (MOR) and immunoperoxidase labeling of an antibody against GABA to determine the cellular basis for the proposed opioid modulation of GABAergic neurons in the rat Acb. MOR-like immunoreactivity (MOR-LI) was localized prominently to plasma membranes of neurons having morphological features of both spiny and aspiny cells, many of which contained GABA. Of 351 examples of profiles that contained MOR-LI and GABA labeling, 65% were dendrites. In these dendrites, MOR-LI was seen mainly along extrasynaptic portions of the plasma membrane apposed to unlabeled terminals and/or glial processes. Dually labeled dendrites often received convergent input from GABAergic terminals and/or from unlabeled terminals forming asymmetric excitatory-type synapses. Of all profiles that contained both MOR and GABA immunoreactivity, 28% were axon terminals. MOR-containing GABAergic terminals and terminals separately labeled for MOR or GABA formed synapses with unlabeled dendrites and also with dendrites containing MOR or GABA. Our results indicate that MOR agonists could modulate the activity of GABA neurons in the Acb via receptors located mainly at extrasynaptic sites on dendritic plasma membranes. MOR ligands also could alter the release of GABA onto target dendrites that contain GABA and/or respond to opiate stimulation.

Key words: -aminobutyric acid; striatum; enkephalin; opiate; ultrastructure; electron microscopy; morphine

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