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Dual ultrastructural localization of enkephalin and tyrosine hydroxylase immunoreactivity in the rat ventral tegmental area: multiple substrates for opiate-dopamine interactions.
J Neurosci. 1992 Apr; 12(4):1335-50.JN

Abstract

Endogenous opiates modulate activity in the mesocorticolimbic dopaminergic system, and this interaction is thought to underlie major aspects of motoric, reward-seeking, and stress-coping behaviors. We sought to determine the ultrastructural substrate for this modulatory action at the level of dopaminergic perikarya in the rat ventral tegmental area (VTA). Using a dual-labeling, immunoperoxidase and immunogold-silver method, we localized antisera directed against leu5-enkephalin (ENK) and the catecholamine-synthesizing enzyme tyrosine hydroxylase (TH) in acrolein-fixed sections through the VTA. ENK-like immunoreactivity (ENK-LI) was visualized within unmyelinated axons and in axon terminals. In terminals, ENK-LI was densely localized to one or more dense-cored vesicles and either densely or lightly detected surrounding small clear vesicles. Immunoreactive dense-cored vesicles were occasionally associated with the presynaptic specialization but were more frequently detected at distant sites along the plasmalemmal surface, often in apposition to astrocytic processes. ENK-immunoreactive terminals formed both symmetric and asymmetric synapses, most frequently on large proximal dendrites. Direct appositions without glial separation were also detected between terminals containing ENK-LI and other ENK-labeled or unlabeled terminals. In contrast to ENK-LI, immunolabeling for TH was primarily detected within perikarya and dendrites in the VTA. Of the ENK-immunoreactive terminals that formed synaptic contacts in single sections, approximately 50-60% were in association with TH-labeled dendrites. The remainder formed synapses on dendrites lacking detectable immunoreactivity for TH. Multiple ENK-immunoreactive terminals occasionally formed convergent synaptic contacts on single TH-labeled or unlabeled dendrites. Furthermore, individual ENK-labeled terminals sometimes formed divergent contacts on two TH-labeled or unlabeled dendrites. When a single ENK-immunoreactive terminal made dual synaptic contacts on TH-labeled dendrites, the latter were usually in close apposition to one another. These findings represent the first ultrastructural demonstration that opioid peptide-containing terminals provide a direct synaptic input to dopaminergic, as well as nondopaminergic, neurons in the VTA. In addition, the morphological evidence suggests that endogenous opioid peptides (1) may be released from nonsynaptic sites, (2) may modulate the release of transmitters from other terminals, and/or (3) may synchronize the activity of multiple neuronal targets in the VTA. These results provide a number of morphological substrates through which opiates may directly or indirectly regulate activity in mesocorticolimbic dopaminergic pathways.

Authors+Show Affiliations

Department of Neurology and Neuroscience, Cornell University Medical College, New York, New York 10021.No affiliation info available

Pub Type(s)

Journal Article
Research Support, U.S. Gov't, P.H.S.

Language

eng

PubMed ID

1348271

Citation

Sesack, S R., and V M. Pickel. "Dual Ultrastructural Localization of Enkephalin and Tyrosine Hydroxylase Immunoreactivity in the Rat Ventral Tegmental Area: Multiple Substrates for Opiate-dopamine Interactions." The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, vol. 12, no. 4, 1992, pp. 1335-50.
Sesack SR, Pickel VM. Dual ultrastructural localization of enkephalin and tyrosine hydroxylase immunoreactivity in the rat ventral tegmental area: multiple substrates for opiate-dopamine interactions. J Neurosci. 1992;12(4):1335-50.
Sesack, S. R., & Pickel, V. M. (1992). Dual ultrastructural localization of enkephalin and tyrosine hydroxylase immunoreactivity in the rat ventral tegmental area: multiple substrates for opiate-dopamine interactions. The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, 12(4), 1335-50.
Sesack SR, Pickel VM. Dual Ultrastructural Localization of Enkephalin and Tyrosine Hydroxylase Immunoreactivity in the Rat Ventral Tegmental Area: Multiple Substrates for Opiate-dopamine Interactions. J Neurosci. 1992;12(4):1335-50. PubMed PMID: 1348271.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Dual ultrastructural localization of enkephalin and tyrosine hydroxylase immunoreactivity in the rat ventral tegmental area: multiple substrates for opiate-dopamine interactions. AU - Sesack,S R, AU - Pickel,V M, PY - 1992/4/1/pubmed PY - 1992/4/1/medline PY - 1992/4/1/entrez SP - 1335 EP - 50 JF - The Journal of neuroscience : the official journal of the Society for Neuroscience JO - J. Neurosci. VL - 12 IS - 4 N2 - Endogenous opiates modulate activity in the mesocorticolimbic dopaminergic system, and this interaction is thought to underlie major aspects of motoric, reward-seeking, and stress-coping behaviors. We sought to determine the ultrastructural substrate for this modulatory action at the level of dopaminergic perikarya in the rat ventral tegmental area (VTA). Using a dual-labeling, immunoperoxidase and immunogold-silver method, we localized antisera directed against leu5-enkephalin (ENK) and the catecholamine-synthesizing enzyme tyrosine hydroxylase (TH) in acrolein-fixed sections through the VTA. ENK-like immunoreactivity (ENK-LI) was visualized within unmyelinated axons and in axon terminals. In terminals, ENK-LI was densely localized to one or more dense-cored vesicles and either densely or lightly detected surrounding small clear vesicles. Immunoreactive dense-cored vesicles were occasionally associated with the presynaptic specialization but were more frequently detected at distant sites along the plasmalemmal surface, often in apposition to astrocytic processes. ENK-immunoreactive terminals formed both symmetric and asymmetric synapses, most frequently on large proximal dendrites. Direct appositions without glial separation were also detected between terminals containing ENK-LI and other ENK-labeled or unlabeled terminals. In contrast to ENK-LI, immunolabeling for TH was primarily detected within perikarya and dendrites in the VTA. Of the ENK-immunoreactive terminals that formed synaptic contacts in single sections, approximately 50-60% were in association with TH-labeled dendrites. The remainder formed synapses on dendrites lacking detectable immunoreactivity for TH. Multiple ENK-immunoreactive terminals occasionally formed convergent synaptic contacts on single TH-labeled or unlabeled dendrites. Furthermore, individual ENK-labeled terminals sometimes formed divergent contacts on two TH-labeled or unlabeled dendrites. When a single ENK-immunoreactive terminal made dual synaptic contacts on TH-labeled dendrites, the latter were usually in close apposition to one another. These findings represent the first ultrastructural demonstration that opioid peptide-containing terminals provide a direct synaptic input to dopaminergic, as well as nondopaminergic, neurons in the VTA. In addition, the morphological evidence suggests that endogenous opioid peptides (1) may be released from nonsynaptic sites, (2) may modulate the release of transmitters from other terminals, and/or (3) may synchronize the activity of multiple neuronal targets in the VTA. These results provide a number of morphological substrates through which opiates may directly or indirectly regulate activity in mesocorticolimbic dopaminergic pathways. SN - 0270-6474 UR - https://www.unboundmedicine.com/medline/citation/1348271/Dual_ultrastructural_localization_of_enkephalin_and_tyrosine_hydroxylase_immunoreactivity_in_the_rat_ventral_tegmental_area:_multiple_substrates_for_opiate_dopamine_interactions_ L2 - http://www.jneurosci.org/cgi/pmidlookup?view=long&pmid=1348271 DB - PRIME DP - Unbound Medicine ER -