Brain Research, 523 (1990) 51-56 51
Elsevier
BRES 15700
Effect of opioids on acetylcholine release evoked by K ÷ or glutamic
acid from rat neostriatal slices
Ernest Arenas, Jordi Alberch, Ricardo Sanchez Arroyos and Jordi Marsal
Departament de Biologia CeLlular i Anatomia Patolrgica, Facuhat de Medicina, Laboratori de Neurobiologia CeLlular i Molecular,
Universitat de Barcelona, Barcelona (Spain)
(Accepted 23 January 1990)
Key words: Glutamate; Acetylcholine release; Opiate; Naloxone; Tetrodotoxin; Neostriatum
Endogenous acetylcholine (ACh) release from rat striatal slices was measured by a chemiluminescent method. Several opiate agents were
tested for their ability to modulate ACh release evoked by potassium ions (K ÷) or glutamic acid (GLU). Morphine, [D-Ala2,
Gly(ol)5]-enkephalin (DAGO), [D-Ala2,o-LeuS]-enkephalin (DADLE) and [D-PenLD-PenS]-enkephalin (DPDPE) were found to have an
inhibitory effect on K +- or GLU-evoked ACh release. This effect was completely blocked by naloxone, but this antagonist by itself had no
effect on ACh release. The action of/~-opiate agonists (morphine and DAGO) on ACh release evoked by K + was sensitive to tetrodotoxin
(qTX), but that of 6-opiate agonists (DADLE and DPDPE) was insensitive. The release evoked by GLU was abolished in the presence of
TTX. The activation of r-opiate receptor by dynorphin-(1-13) had no effect on K ÷- or GLU-evoked ACh release. It is concluded that/~- and
6-opiate agonists, but not r, exert an inhibitory control on striatal cholinergic interneurons, but with a different mechanism of action or
localization of the receptors. Corticostriatal glutamatergic neurons have an important role in the interaction of the ACh-opioid systems.
INTRODUCTION
The presence of multiple classes of opiate receptors
has been demonstrated in brain,/~-, 6- and r-types have
been extensively studied and defined 12'28. The neostria-
tum contains a large number of enkephalinergic and
dynorphinergic neurons, as well as high density of
receptors for these opiate peptides 3'3°'46. Autoradio-
graphic studies have indicated that r- and 6-binding sites
are homogeneously distributed in the striatum, whereas
g-opiate receptors are more concentrated in patches 3°
complementary to a rich acetylcholinesterase staining
matrix~4,19,25
Acetylcholinesterase intense perikarya of the striatum
are large aspiny neurons that account for approximately
1-8% of all striatal neurons 26'31. Furthermore, these cells
have been identified by choline acetyltransferase immu-
noreactivity as cholinergic interneurons 22'31.
Opioid interactions with cholinergic neurons are
known. However, data on effects of opioid drugs on
acetylcholine (ACh) release are conflicting. Mulder and
coworkers 33 found that the activation of h-receptors
inhibited [14C]ACh release from rat striatal slices, in
contrast with other findings 21. Also p-receptor agonists
have shown different effects on ACh release: facilita-
tory 4'45, inhibitory 4 or no effect 33'44. Thus, it remains to
be definitively established the type(s) of opioid recep-
tor(s) involved in the modulation of ACh release in the
striatum.
The striatum receives a massive input from frontal
cortex and other somatosensory cortices 6'x°, which is
electrophysiologically excitatory in nature 43. The projec-
tions are believed to utilize glutamate (GLU) as a
neurotransmitter. Significant reductions in the levels of
GLU, in its high-affinity uptake and in the K+-evoked
release of GLU have been found in the striatum of rats
with lesions of the cerebral cortex 11. Moreover, elec-
trophysiological studies have revealed that corticostriatal
pathway seems to establish monosynaptic inputs with
neostriatal neurons 23,24. Later, morphological studies
have shown that aspiny dendrites of presumptive cholin-
ergic striatal interneurons receive cortical inputs 17'18.
Furthermore, excitatory amino acids are known to
release ACh from rat striatum 2,27,42.
The aim of the present study was to examine whether
K ÷- or GLU-stimulated ACh release is modulated in a
different manner by p-, 6- and r-opiate agents. Endoge-
nous ACh release was continuously detected by a
chemiluminescent method.
Correspondence: J. Marsal, Department de Biologia Cel.lular i Anatomia Patolbgica, Facultat de Medicina, Universitat de Barcelona,
Casanovas 143, 08036-Barcelona, Spain.
0006-8993/90/$03.50 © 1990 Elsevier Science Publishers B.V. (Biomedical Division)