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Volume 16, Number 22,
Issue of November 15, 1996
pp. 7128-7136
Copyright ©1996 Society for Neuroscience
Local Opioid Withdrawal in Rat Single Periaqueductal Gray Neurons
In Vitro
Received June 13, 1996; revised Aug. 26, 1996; accepted Aug. 30, 1996.
Billy Chieng and
MacDonald J. Christie
Department of Pharmacology, The University of Sydney, NSW 2006, Australia
Opioid dependence in ventrolateral periaqueductal gray (PAG)
neurons was studied by using intracellular recordings from brain
slices. In slices from morphine-dependent rats maintained in morphine
(5 µM) in vitro, action potential
frequencies of opioid-sensitive neurons did not differ from untreated
control neurons but were greater than in control neurons maintained in
morphine in vitro, indicating development of tolerance.
Naloxone (100 nM or 1 µM) depolarized 25 of
51 neurons from morphine-dependent rats maintained in morphine
in vitro, 19 of which previously had been classified as
opioid-sensitive. Action potential frequencies in the presence of
naloxone were greater than in control neurons in the absence of
opioids, as well as in control neurons in the presence of both morphine
and naloxone, demonstrating opioid withdrawal. In slices from control
animals, opioid-induced hyperpolarizations and naloxone-induced
depolarizations (in the presence of morphine) reversed polarity near
expected EK ( 111 ± 3 mV and
113 ± 3 mV, respectively). In contrast, the reversal potential
of naloxone-induced depolarizations was more negative than expected in
neurons from dependent animals (143 ± 9 mV), indicating that
the depolarization was not attributable simply to antagonism of a
K-conductance increase. Naloxone-induced depolarizations were not
inhibited by tetrodotoxin (1 µM), bicuculline (30 µM), 6-cyano-7-nitroquinoxaline-2,3-dione (10 µM), or prazosin (300 nM), suggesting no
involvement of major synaptic neurotransmitters. Clonidine (1 µM) and baclofen (30 µM) overcame
naloxone-induced depolarizations. These results demonstrate development
of both tolerance and withdrawal in PAG neurons and suggest induction
of a novel opioid-sensitive current that could be involved in
withdrawal behavior.
Key words:
periaqueductal gray;
opiate withdrawal;
drug dependence;
morphine;
naloxone;
clonidine;
brain slices
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