123 0090-2977/12/4402-0123 © 2012 Springer Science+Business Media, Inc.
Neurophysiology, Vol. 44, No. 2, 2012
Modulation of Morphine Analgesia and Tolerance
in Rats by NMDA Receptor Antagonists
E. Ozdemir,
1
I. Bagcivan,
2
and S. Gursoy
3
Received December 19, 2011.
The efficacy of opioids in chronic pain treatment is limited because of the development of opioid tolerance.
We investigated the role of N-methyl-D-aspartate (NMDA) receptor antagonists (NMDAR Ants) in
morphine analgesia and tolerance in rats. To induce the morphine tolerance, experimental rats received
morphine (50 mg/kg; subcutaneously) once daily for 3 days. After the last dose of morphine was injected
on day 4 and morphine tolerance was evaluated, analgesic effects of ketamine, dizocilpine (MK-801, a
non-competitive NMDAR Ant), LY235959 (a competitive NMDAR Ant), cis-2,3-piperidinedicarboxylic
acid (PDA, an NMDAR agonist), and morphine were estimated with 30-min-long intervals (0, 30, 60,
90, and 120 min) by the tail-flick and hot-plate algesia tests (n = 6 in each studied group). As was found,
ketamine, MK-801, and LY235959 significantly attenuated the development of morphine tolerance
(P < 0.05). On the other hand, PDA somewhat increased the development of this tolerance, but the
difference was not statistically significant (P > 0.05). Our data indicate that NMDAR Ants attenuate
the development of morphine tolerance, significantly affecting the effects of morphine analgesia in rats.
Keywords: analgesia, morphine, NMDA antagonists, ketamine, MK-801.
1
Departments of Physiology,
1
Pharmacology,
2
and Anesthesiology and
Reanimation,
3
Cumhuriyet University School of Medicine, Sivas, Turkey.
Correspondence should be addressed to E. Ozdemir
(e-mail: ercan_ozdemir@hotmail.com).
INTRODUCTION
The rapid development of tolerance and
dependence limits the usefulness of morphine in
long-term treatment of painful syndromes. Morphine
tolerance is a complex phenomenon, involving the
serotonergic and noradrenergic systems [1, 2].
Recently, it was also demonstrated that the nitric
oxide–cGMP signal pathway plays a pivotal role
in the development of tolerance to the analgesic
effect of morphine [3]. Over the past decade,
much attention in extensive animal studies has
been focused on the potential use of N-methyl-D-
aspartate (NMDA) receptor antagonists (NMDAR
Ants) as adjuvants to opioids [4, 5]. Combinations
of NMDAR Ants and opioid agonists are of clinical
interest because NMDA antagonists may potentiate
opioid analgesia [6].
As was reported, NMDAR Ants either potentiate
[7] or do not affect [8] opioid analgesia in humans.
The exact reasons for the discrepancies are not
clear, but several factors, namely species, strain, the
type of opioid agonist and its dose, the NMDAR Ant
and its dose, route of drug administration, type of
nociceptive stimulus, and injection-to-test interval,
either alone or in combination, might be reasons for
the inconsistent findings [9]. It was reported that
dizocilpine (MK-801) and dextromethorphan (non-
competitive NMDAR Ant) enhanced acute morphine
analgesia in male but not in female mice [10, 11].
The lack of enhancement by dextromethorphan in
females was estrogen-dependent, as ovariectomized
mice showed a male-like enhancement and estrogen
replacement reinstated by the female phenotype
[9]. In contrast, Nemmani et al. suggested that the
competitive NMDA receptor antagonist LY235959
enhanced morphine analgesia equally in both sexes
[11]. Antagonists of the glycine site in the NMDA
receptor complex also produced no effect [12] or
potentiated [13] morphine-induced antinociception
in the tail-flick studies. We found only one
report describing the effect of pretreatment by a
polyamine antagonist (ifenprodil) on morphine
antinociception tested in the hot-plate test [14].
Ifenprodil potentiated and prolonged the morphine
effects. Ifenprodil antinociception was inhibited
by naloxone, suggesting the involvement of opioid
receptors and, perhaps, an additive effect with
morphine.
It is unclear whether the effects of NMDAR
Ants on acute morphine analgesia are related to