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When possible, females were tested in estrus-diestrus pairs, so that the amount of handling between the two groups was approximately equal. Each rat was tested only once. Twenty-three and a half hr later, rats were tested on the tail withdrawal assay to obtain a baseline latency. Then morphine was injected s. For example, 3. Then 2. Then 4. Rats were overdosed with Equithesin. Then 0. In each experiment, data from rats that had cannula placements outside of vPAG defined as ventrolateral PAG and dorsal raphe nucleus , and data from rats that were tested with two doses or fewer Experiment 1 before the cannula became occluded, were not included in the statistical analyses.

Data were included only from rats that were confirmed to be in either diestrus-1 or estrus before and after testing. T-tests with Bonferroni adjustments were used for post-hoc comparisons. Figure 1 shows individual placements, mapped according to magnitude of effect. There were no clear differences in antinociception between rats with vlPAG vs.

DRN cannula placements; thus, data from these two areas were combined for further analysis of sex differences. Cannula placements, Experiment 1 morphine microinjections. For clarity, female placements are marked primarily on the left and male placements are marked on the right side of the brain maps actual cannula placements were all on the right. Analysis of combined data showed that there were no significant sex differences in control saline tail withdrawal latencies: averaged across the time course, latencies were 6.

There was also no significant sex difference in the time course of antinociception after microinjections of morphine to vPAG data not shown ; latency data were therefore transformed to AUC values. Post-hoc analysis showed that all doses of morphine except 0.

Antinociceptive and locomotor effects of morphine microinjected into vPAG in male and female rats. Bottom panel : Effect of intra-vPAG morphine on spontaneous locomotor activity measured min post-injection. Figure 2 bottom panel shows locomotor activity measured min post-injection in rats with vPAG cannula placements. There was no significant difference in locomotion between males and females following saline administration, although females tended to be slightly more active.

There were no significant sex differences in maximal morphine-induced immobility, however, the lowest dose of morphine, 0. Thus, morphine was more potent but equally efficacious in males compared to females. Interestingly, morphine produced a U-shaped dose-effect curve in both sexes, with greater decreases in locomotor activity at the lower than at the higher doses.

Thus, Experiment 2 was conducted to determine whether the antinociceptive effect of morphine microinjected into the vPAG differs when females are in estrus vs. That is, rats tested during estrus were relatively resistant to the antinociceptive effects of morphine administered to the vPAG.

Antinociceptive and locomotor effects of 1. Bottom panel : Effect of intra-vPAG saline or morphine on spontaneous locomotor activity measured min post-injection. In control rats those receiving intra-site saline , s. Thus, similar to Experiment 1, most females in Experiment 3 were in diestrus-1 at the time of testing.

Antagonism of systemic s. The present study examined sex differences in morphine-induced antinociception and immobility mediated by the vPAG. Morphine was, however, more potent in males than in females in producing immobility.

Because most females in Experiment 3 were in diestrus-1 — a stage at which females are very similar to males in their morphine sensitivity — this result suggests that mu opioid receptor density is probably lower even in diestrus females compared to males. In rodent models of antinociception, systemically administered mu opioid agonists are often reported to be more potent in males than in females [ 2 , 10 , 11 , 38 ], although this is not always the case [e.

The persistence of sex differences in antinociception when opioids are administered i. Thus, sex differences in opioid antinociception are probably caused by one or more pharmacodynamic factors, such as sexually dimorphic brain loci at which opioids act.

Site-specific opioid administration to areas of the descending pain modulatory system has been examined by several groups. Similarly, Krzanowska and Bodnar [ 31 ] reported that at doses of 2. Recently, Murphy and colleagues [ 55 ] also showed that intra-vPAG morphine was more potent in male than female rats against persistent inflammatory pain.

In contrast, another previous study [ 27 ] as well as the present one shows no significant sex difference in antinociception after intra-PAG morphine microinjection, and Tershner and colleagues [ 53 ] reported that in anesthetized rats, DAMGO microinjected into vPAG was more potent in females compared to males.

The present study suggests that the extent to which sex differences in opioid antinociception mediated by the PAG are observed depend on estrous stage and availability of mu opioid receptors at the time of testing. Female rats have been shown to be least sensitive to the antinociceptive effects of systemically administered mu opioid agonists approximately 24 hr after plasma gonadal steroids peak [ 3 , 5 , 45 , 50 , 51 ], that is, during vaginal estrus.

Experiment 2 of the present study suggests that the same is true when morphine is administered directly into the vPAG. Bodnar and colleagues report similar findings [ 47 ]. Two of the previous studies in which females were significantly less sensitive than males to site-specific morphine also had more estrus females than in Experiment 1 of the present study: Bodnar and colleagues [ 30 - 32 ] tested cycling female rats only during estrus, and in the Boyer et al.

Boyer, personal communication. Estrous stage of female rats was not reported in the Tershner et al. If females in these studies were predominantly in diestrus at the time of testing, the present results suggest that opioid antinociception would not be significantly greater in males than females. One additional factor that may be important is the use of anesthesia.

We recently observed that an anesthetic dose of pentobarbital enhanced morphine antinociception to a significantly greater extent in female compared to male rats [ 13 ] — thus it is possible that the observation of greater DAMGO antinociception in females in the Tershner et al. Previous studies have shown that mu opioid agonists microinjected into the PAG [ 30 , 39 ] and RVM [ 6 ] affect locomotor activity in rats. In the present study morphine was more potent in its locomotor depressant effect in male compared to female rats, as reported previously for site-specific and systemic mu opioid agonists [ 6 , 30 , 49 ].

As with antinociception, sex differences were probably limited by the fact that females in Experiment 1 were predominantly in diestrus at the time of testing; Experiment 2 suggests that morphine-induced immobility is attenuated in estrus relative to diestrus females. The hyperactivity that was also observed in some rats resulting in a U-shaped dose-effect curve has been reported previously after morphine microinjection to dorsal and lateral regions of the PAG in rats [ 39 , 46 ], but it cannot be determined from these data whether that behavioral effect differs by sex or estrous stage.

Experiment 3 showed that 1. A previous study in male rats showed that naloxone methobromide microinjected to the PAG attenuated antinociception induced by a single s. The antagonism experiment in the present study confirms that activation of mu opioid receptors in the vPAG plays an important role in antinociception produced by systemic morphine in both male and female rats.

The relatively greater antagonism observed in females compared to males suggests that females — even those in diestrus — have a smaller reserve of functional mu opioid receptors than do males. This finding corroborates the recent report of reduced mu opioid receptor expression in the vPAG of female compared to male rats [ 55 ]. We previously observed a similar sex difference in antagonism of s. Thus, it appears that females in any stage of the estrous cycle may have a smaller mu opioid receptor reserve than do males; however, this difference may not be great enough to result in significant sex differences in opioid antinociception with relatively high efficacy agonists like morphine, unless females are tested in estrus or a significant fraction of mu receptors are made unavailable in this case, via irreversible antagonist treatment.

Previous studies comparing opioid agonists that vary in efficacy also support the hypothesis that differential opioid receptor density underlies sex differences in opioid antinociception. Picker and colleagues have demonstrated that sex differences in opioid antinociception increase in magnitude as the efficacy of the agonist decreases [ 4 , 11 , 52 ].

Because low to intermediate efficacy agonists must activate more receptors than high efficacy agonists to produce antinociception, the functional significance of small sex differences in opioid receptor density would be magnified when testing lower efficacy agonists.

It is possible that the mechanism underlying decreased opioid sensitivity in estrus females also relates to supraspinal opioid receptor availability. Although it is not yet known whether PAG mu opioid receptor density fluctuates in females across the estrous cycle, this has been demonstrated in other brain areas such as hypothalamus [ 21 , 36 ]. Therefore, perhaps any factor that decreases supraspinal opioid receptor availability e.

In summary, the present findings confirm that the midbrain PAG is important in morphine-induced antinociception and immobility in male and female rats. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

National Center for Biotechnology Information , U. Behav Brain Res. Author manuscript; available in PMC Feb Scott A. Bernal , a Michael M. Morgan , b and Rebecca M. Michael M. Rebecca M. Author information Copyright and License information Disclaimer.

Copyright notice. See other articles in PMC that cite the published article. Abstract Given the findings that 1 systemic opioid antinociception varies by estrous stage in females, and 2 the magnitude of sex differences in opioid antinociception is negatively correlated with opioid agonist efficacy, we hypothesized that sex differences in the function of the descending pain modulatory system are likely influenced by estrous stage in females and by the number of available opioid receptors therein.

Introduction Sex differences in opioid antinociception have been observed in mice [ 7 , 38 ], rats [ 2 , 9 - 11 ], monkeys [ 40 ] and humans [ 19 - 21 ]. Materials and methods 2. Results 3. Open in a separate window. Figure 1. Figure 2. Figure 3. Figure 4. Discussion The present study examined sex differences in morphine-induced antinociception and immobility mediated by the vPAG. References 1.

Antagonism of stimulation-produced analgesia by naloxone, a narcotic antagonist. Sex-related differences in the effects of morphine and stress on visceral pain. Ovarian steroids and modulation of morphine-induced analgesia and catalepsy in female rats.

Eur J Pharmacol. Sex and rat strain determine sensitivity to kappa opioid-induced antinociception. Alterations in brain opiate receptor mechanisms on proestrous afternoon. Microinjection of morphine into the rostral ventromedial medulla produces greater antinociception in male compared to female rats. Brain Res. Effect of adrenal and sex hormones on opioid analgesia and opioid receptor regulation. Pharmacol Biochem Behav. Gender differences in the reinforcing properties of morphine.

Gender-related differences in the antinociceptive properties of morphine. J Pharmacol Exp Ther. Sex-related differences in the antinociceptive effects of opioids: importance of rat genotype, nociceptive stimulus intensity, and efficacy at the rat mu opioid receptor. Craft RM. Potentiation of morphine antinociception by pentobarbital in female vs. Sex differences in discriminative stimulus effects of morphine in the rat.

Behav Pharm. Sex differences in pain and analgesia: the role of gonadal hormones. Eur J Pain. Neuroscience and Biobehavioral Reviews. A comprehensive review". Progress in Neurobiology. Hoboken, N. J Neurosci. Archived from the original PDF on Retrieved Anatomy of the midbrain. Corpora quadrigemina : Inferior colliculus Brachium Superior colliculus Brachium.

Pretectal area. Spinotectal tract Central tegmental tract. Tectospinal tract. Periaqueductal gray Raphe nuclei dorsal. Ventral tegmental area Rostromedial tegmental nucleus Pedunculopontine nucleus. Red nucleus Rostral interstitial nucleus of medial longitudinal fasciculus Parabrachial area. Interpeduncular nucleus Midbrain reticular formation.

Cerebral aqueduct. Pars compacta Pars reticulata. Superior cerebellar peduncle Decussation Interpeduncular fossa. Authority control TA98 : A Categories : Midbrain Pain. Hidden categories: CS1 maint: multiple names: authors list Articles with short description Short description matches Wikidata Use American English from January All Wikipedia articles written in American English All articles with unsourced statements Articles with unsourced statements from September Wikipedia articles with TA98 identifiers.

Namespaces Article Talk. Views Read Edit View history. Help Learn to edit Community portal Recent changes Upload file. Download as PDF Printable version. Wikimedia Commons. Anatomical terms of neuroanatomy [ edit on Wikidata ]. TA98 : A

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