Research reportInvolvement of cholinergic neurons in the release of dopamine elicited by stimulation of μ-opioid receptors in striatum
Introduction
There is considerable evidence that striatal dopamine (DA) release is modulated by a variety of convergent inputs either excitatory or inhibitory. Among these inputs, opioidergic and cholinergic neurons seem especially involved.
The neostriatum contains a dense population of opioidergic neurons and also high densities of all three opioid receptor types: μ, δ, κ. The activation of κ-opioid receptors inhibits whereas the activation of μ- or δ-opioid receptors stimulates DA release [4,[8], [9], [10],35].
We have previously reported that the DA release elicited by stimulation of μ-opioid receptors was dependent on neurons whose soma, located in the striatum, may be destroyed by kainic acid [10]. This observation was in agreement with previous studies indicating that μ-opioid receptors are not located on DA nerve endings but on postsynaptic neurons [4,23,30,37]. Among these neurons, cholinergic interneurons might be good candidates. Several studies have indeed evidenced that acetylcholine modulates dopaminergic transmission. This modulation seems complex, involving different types of cholinergic receptors [6,7,12,32,34,39]. Moreover, striatal cholinergic activity appears to be regulated by opioid peptides. In vivo studies demonstrate that a variety of opioid agonists inhibit the acetylcholine release evoked by electric, potassium or glutamate stimulation [3,19,28,31,36,38].
The aim of the present study was to determine, by intrastriatal microdialysis, the involvement of cholinergic interneurons in the modulation of DA release elicited by DAGO, a specific μ-opioid receptor agonist [15]. We assessed the consequence on the modulation of DA release elicited by DAGO of a striatal lesion by AF 64-A, a cholinotoxin, as well as the administration of methoctramine, a M2 muscarinic receptor antagonist.
Section snippets
Animals
The experiments were performed on male Sprague-Dawley rats (260–300 g, Charles River, Saint-Aubin-l`es-Elbeuf, France). They were maintained on a 12 h/12 h light/dark cycle and received food and water ad libitum.
AF 64-A lesion
AF 64-A (ethylcholine mustard aziridinium ion) was prepared from acetylethylcholine mustard hydrochloride (acetyl-AF 64) according to the method described previously [11]. The solution was kept on ice and used less than 2 h following its preparation.
Animals were anesthetized with chloral
Effect of DAGO on striatal extracellular levels of DA and its metabolites in control or AF 64-A lesioned rats
The striatal infusion of DAGO 10−5 M significantly increased DA release in rat striatum (Fig. 1). This effect lasted about 60 min and was maximal in the 20–60 min period following the peptide infusion + 47% vs. controls; n = l; P ≤ 0.01). DAGO 10−5 M failed to modify the levels of DOPAC and HVA (data not shown).The striatal lesion produced by AF 64-A abolished the effect of DAGO 10−5 (Fi = 4.34; n = 7; P ≤ 0.05) (Fig. 1).
Effect of the AF 64-A striatal injection on the uptake of [3H]choline and [3H]dopamine into striatal synaptosomes and on the basal extracellular levels of dopamine, dihydroxyphenylacetic acid and homovanillic acid
Seven days after the striatal injection of AF 64-A (2 × 1 nmol), it was observed a
Discussion
There is considerable in vitro evidence that cholinergic neurons modulate striatal DA transmission. However this modulation appears complex involving both muscarinic and nicotinic receptors [6,12,32,34].
The development of specific ligands for M1- or M2-muscarinic receptors has allowed differentiation of the roles of these receptors which operate in an opposite manner on DA release. In vivo microdialysis experiments showed that the M1-muscarinic receptor stimulation enhanced DA release while
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