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Volume 16, Number 16, Issue of August 15, 1996 pp. 5037-5048
Copyright ©1996 Society for Neuroscience

Ultrastructural Evidence for Prominent Distribution of the µ-Opioid Receptor at Extrasynaptic Sites on Noradrenergic Dendrites in the Rat Nucleus Locus Coeruleus

Received Feb. 6, 1996; revised May 9, 1996; accepted May 21, 1996.

Elisabeth J. Van Bockstaele¹, Eric E. O. Colago¹, Peter Cheng¹, Akiyoshi Moriwaki², George R. Uhl², and Virginia M. Pickel¹

¹ Department of Neurology and Neuroscience, Cornell University Medical College, New York, New York 10021, and ² National Institute on Drug Abuse, Division of Intramural Research Program, Addiction Research Center, Baltimore, Maryland 21224

Physiological studies have indicated that agonists at the µ-opioid receptor (µOR), such as morphine or the endogenous peptide methionine⁵-enkephalin, can markedly decrease the spontaneous activity of noradrenergic neurons in the locus coeruleus (LC). Messenger RNA and protein for µOR are also densely expressed by LC neurons. During opiate withdrawal, increased discharge rates of LC neurons coincide with the expression of behavioral features associated with the opiate withdrawal syndrome. To better define the cellular sites for the physiological activation of µOR in the LC and its relation to afferent terminals, we examined the ultrastructural localization of µOR immunoreactivity in sections dually labeled for the catecholamine-synthesizing enzyme tyrosine hydroxylase (TH). Immunogold-silver labeling for µOR (i-µOR) was localized to parasynaptic and extrasynaptic portions of the plasma membranes of perikarya and dendrites, many of which also contained immunolabeling for TH. The dendrites containing exclusively i-µOR were more numerous in the rostral pole of the LC. The i-µOR in dendrites with and without detectable TH immunoreactivity were usually postsynaptic to unlabeled axon terminals containing heterogeneous types of synaptic vesicles and forming asymmetric synaptic specializations characteristic of excitatory-type synapses. These results provide the first direct ultrastructural evidence that µOR is strategically localized to modulate the postsynaptic excitatory responses of catecholamine-containing neurons in the LC.

Key words: norepinephrine; drug abuse; enkephalin; opiate; morphine; excitatory amino acid

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