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Figure 1. C-F, The Brodmann areas are labeled on brain sections having increased serotonin 2A BP ND in MDMA users after adjusting for age, use of birth control, and estrogen level in the representative clusters from the right hemisphere A and bilateral superior B regions. Figure 2. Right hemisphere A and bilateral superior B regions in which lifetime use of 3,4-methylenedioxymethamphetamine MDMA correlates positively with the serotonin 2A receptor nondisplaceable binding potential serotonin 2A BP ND in the MDMA user group after adjusting for use of birth control, estrogen level, and age Table 4. Scatterplots are rank data to account for the nonparametric distribution of lifetime MDMA use x-axis; minimum-maximum use, mg and the adjusted predicted rank data for serotonin 2A BP ND y-axis; adjusted for age, use of birth control, and estrogen level and using fluorine 18—labeled setoperone as the tracer. The rank of lifetime use was calculated as the product of the average use per episode and the number of use episodes. Arch Gen Psychiatry. Whether MDMA produces chronic reductions in serotonin signaling in humans remains controversial. Objective To determine whether MDMA use is associated with chronic reductions in serotonin signaling in the cerebral cortex of women as reflected by increased serotonin 2A receptor levels. Case participants were abstinent from MDMA use for at least 90 days as verified by analysis of hair samples. The serotonin 2A receptor levels in the cerebral cortex were determined using serotonin 2A -specific positron emission tomography with radioligand fluorine 18—labeled setoperone as the tracer. In contrast, there were no regions in which MDMA use was inversely associated with receptor levels. Serotonin 2A receptor levels correlate positively with lifetime MDMA use and do not decrease with abstinence. These results suggest that MDMA use produces chronic serotonin neurotoxicity in humans. Given the broad role of serotonin in human brain function, the possibility for therapeutic MDMA use, and the widespread recreational popularity of this drug, these results have critical public health implications. In animals, MDMA spares the cell bodies of brainstem serotonin neurons. Although the ability of some MDMA dosing regimens to produce chronic serotonin axon loss is clear, 9 the evidence for MDMA-induced chronic reductions in serotonin signaling in humans remains equivocal. However, there is little evidence for the use of MDMA as a psychotherapeutic agent and a great deal of evidence to support neurocognitive deficits in recreational MDMA users. Consistent evidence for chronic reductions in serotonin signaling in individuals who use MDMA as a recreational drug derives from nuclear imaging measures of the presynaptic axonal serotonin transporter as a surrogate marker for serotonin axon integrity. In contrast to the presynaptic serotonin transporter, the postsynaptic serotonin 2A receptor may have advantages as an assay of ongoing serotonin signaling because serotonin 2A receptors reflect presynaptic agonist signaling. Serotonin 2A receptor levels decrease in the face of increased agonist stimulation, 23 , 24 and the release of MDMA-induced serotonin acutely decreases serotonin 2A levels in some brain regions of rats. Erritzoe and colleagues 26 examined both serotonin 2A receptor binding and serotonin transporter binding in humans who recently used MDMA and hallucinogens and were characterized as either MDMA-preferring users or hallucinogen-preferring users. Overall, there was a slight tendency for lower serotonin 2A receptor levels in the MDMA- and hallucinogen-preferring users than in the controls, but no differences in serotonin 2A binding were seen between the 2 drug-using groups, despite widespread reductions in the serotonin transporter level that were restricted to the MDMA-preferring users. In addition to the need to determine whether MDMA use is associated with chronic serotonin loss in humans, more evidence is needed regarding the effects of MDMA on women. Sex has been shown to influence toxicity to drugs of abuse. The evidence to date suggests that human recreational MDMA use may lead to chronic alterations in cortical serotonin function. To determine whether MDMA use is associated with chronic changes in serotonin signaling as reflected by serotonin 2A receptor levels, we used fluorine 18 18 F —labeled setoperone 33 positron emission tomography PET to assay cerebral cortical serotonin 2A receptors in long-abstinent female MDMA polydrug users and controls. We estimated receptor levels as the nondisplaceable binding potential BP ND , which reflects receptors available to bind \[ 18 F\]setoperone. In line with the observations of Reneman and colleagues, 25 we hypothesized that long-abstinent MDMA users would have increased serotonin 2A receptor levels in the cortex and that greater lifetime MDMA exposure would predict greater serotonin 2A receptor levels. Data from 1 female MDMA user was excluded because it was found by analysis of hair samples that she had recently used cocaine. We recruited control participants in parallel with MDMA users by advertising in the local media, in flyers, and by word of mouth requesting participants who had used ecstasy, marijuana, or other recreational drugs. Participants were compensated for their time. Our study was approved by the Vanderbilt University institutional review board and conformed to the World Medical Association's Declaration of Helsinki. Participants were screened by telephone for inclusion and exclusion criteria, and those who met the provisional enrollment criteria were additionally screened in person. White women 18 to 25 years of age who did not use drugs of abuse within 2 weeks of enrollment were eligible for inclusion in our study. Participants were required to have regular menstrual cycles or use oral hormonal contraceptives. For all participants, their last exposure to cocaine, lysergic acid diethylamide, and other amphetamines had to be at least 90 days prior to enrollment in our study. These use and abstinence criteria were chosen on the basis of our earlier fMRI studies and on the basis of the literature reviewed regarding the time frame of serotonin 2A receptor changes following MDMA exposure. The exclusion criteria were having general medical conditions or endocrine abnormalities; having contraindications to PET or MRI scanning; having a lifetime history of Axis I psychiatric diagnoses, except for drug-induced mood disorder 1 MDMA user met criteria for a history of substance-induced hypomania ; being currently dependent or having been previously dependent on a substance other than nicotine or caffeine; positive urine drug screen within 2 weeks of the PET scan, and alcohol use within 72 hours of the PET scan; use of psychoactive or vasoactive medications within 6 weeks of enrollment; and head injury with loss of consciousness greater than 20 minutes. Participants were screened for drug use, cotinine, and pregnancy twice a week for at least 2 weeks and until completing the PET scan. Participants with positive drug or pregnancy test results were excluded from our study. Participants provided their history of drug use in a self-reported drug use questionnaire, 34 , 36 , 37 using a time-line follow-back method. Twenty-four hours prior to PET scanning, we assayed serum estrogen levels. Urine drug and cotinine tests were performed prior to the PET scan for all participants to reconfirm drug abstinence and self-reported nicotine exposure. An alcohol breathalyzer Intoximeters was used to confirm recent abstinence from alcohol. A hair sample was obtained to perform a drug analysis of prolonged abstinence up to 90 days United States Drug Testing Laboratories. Hair specimens that are used to measure exposure to MDMA correlate well with self-reports. All other participants tested negative for drug use within the day exposure window. The tracer \[ 18 F\]setoperone has been used by a number of investigators to study cortical serotonin 2A receptor levels in depression, 48 , 49 schizophrenia, 50 , 51 and Alzheimer disease 52 and to measure the effects of antipsychotic and antidepressant medications 53 , 54 on serotonin 2A receptor levels. The binding of \[ 18 F\]setoperone to serotonin 2 receptors in the cortex largely reflects serotonin 2A receptors, with there being an affinity for serotonin 2A vs serotonin 2C receptors of Serial scans of increasing lengths were started immediately after the intravenous injection of 7. Eight second scans, six second scans, five 1-minute scans, two 2. The PET images were preprocessed as previously reported elsewhere. This algorithm registers images by computing a transformation that maximizes the mutual information between the images. This algorithm is fully automatic and does not require any type of manual preprocessing. The very low levels of serotonin 2A receptors in the cerebellum do not invalidate the use of the cerebellum as a reference region for estimating serotonin 2 receptor levels in the cortex. Prior reports indicate that use of birth control, estrogen level, 70 and age 71 affect serotonin 2A receptor expression. We used multivariable regression within SPM5 to test for the effects of confounding factors use of birth control, estrogen level, and age on serotonin 2A BP ND. Therefore, subsequent between- and within-group analyses were adjusted for use of birth control, estrogen level, and age. Because \[ 18 F\]setoperone is not specific to serotonin 2A binding outside of the cortex, 33 we used the Wake Forest University Pickatlas tool version 2. Because we had no firm a priori hypotheses regarding which cortical regions would be most strongly affected by MDMA, we chose to perform a whole cortex regression analysis as opposed to a region-of-interest analysis. This approach was also chosen to avoid potential partial volume effects inherent in a region-of-interest analysis if the effect of interest is confined to a portion of the region of interest. As within SPM5, data were adjusted for use of birth control, estrogen level, and age. This 2-step approach, first to identify areas differing between groups in serotonin 2A binding within SPM and then to extract that data for further analysis, was used to ensure that the association of MDMA use with greater serotonin 2A binding potential was not explained by other drug use or other factors, such as the duration of drug abstinence. Therefore, we used multivariable regression analysis to assess the relationship between lifetime MDMA use in units of milligrams of ecstasy and receptor levels within the MDMA user group. We controlled for confounding factors age, use of birth control, and estrogen level. Data on the demographics and lifetime drug use of the participants are summarized in Table 1. MDMA users had increased serotonin 2A BP ND in 5 cortical clusters Figure 1 ; Table 2 that were mainly localized to the occipitoparietal, temporal, occipitotemporal-parietal, frontal, and frontoparietal regions but also included limbic areas. The greatest between-group difference in serotonin 2A BP ND was found in the temporal cluster Table 3 , where serotonin 2A receptor availability was Regions having increased serotonin 2A binding potential involved more brain regions in the right hemisphere than in the left. This was notable for the right frontal regions Table 2. In contrast, there were no regions in which lifetime MDMA use was statistically significantly associated with lower serotonin 2A receptor availability. To ensure that the observed association of lifetime MDMA use with serotonin 2A BP ND was not driven by exposure to other drugs of abuse, we conducted analyses examining the association of regional serotonin 2A BP ND with other drug use, including nicotine. The current findings reveal that female MDMA users have chronic changes in cortical serotonin function that consist of greater serotonin 2A receptor levels and increasing serotonin 2A receptor levels with increasing MDMA use. We hypothesized that MDMA users would have increased cortical serotonin 2A BP ND , a finding consistent with MDMA-induced chronic reductions in cortical serotonin synaptic neurotransmission leading to compensatory upregulation of the serotonin 2A receptors. Although the results support our hypothesis, the interpretation of these findings must remain speculative because we did not measure brain serotonin levels and because factors other than MDMA-induced serotonin axon loss may account for the current findings. Although the current observations are consistent with chronically reduced serotonin levels in the cerebral cortex, this interpretation is limited by the fact that the serotonin 2A receptor has not been sufficiently validated as a measure of serotonin denervation, and it is also possible that chronic reductions in cortical serotonin neurotransmission might occur in the absence of serotonin axon loss. Increased serotonin 2A BP ND could theoretically be due to a combination of compensatory receptor upregulation and reduced competition for synaptic serotonin with \[ 18 F\]setoperone. However, acute tryptophan depletion has been associated with decreased serotonin 2A receptor binding in humans in broad regions of the cortex using \[ 18 F\]setoperone 77 and in the frontal cortex using the highly selective serotonin 2A ligand carbon 11—labeled MDL Our findings are consistent with those of Reneman and colleagues 25 regarding increased serotonin 2A receptor levels in the occipital cortex of abstinent MDMA users; however, our study of a cohort of female MDMA users extends the findings to multiple cortical regions, demonstrates that there is a lack of recovery with extended abstinence, and strengthens the argument for specificity to MDMA exposure by demonstrating a dose-response effect. Several factors including a homogenous female cohort, verified abstinence, improved kinetic properties and tracer kinetic modeling, and possible increases in resolution \[although partially offset by the degree of smoothing\] afforded by PET may have permitted us to detect broader effects. A recent report 26 used \[ 18 F\]altanserin to examine the serotonin 2A receptor levels and carbon 11—labeled 3-amino\[2-\[ di methyl amino methyl\]phenyl\]sulfanylbenzonitrile \[ 11 C\]DASB to examine the serotonin transporter levels in MDMA-preferring and hallucinogen-preferring drug users and controls. Because both hallucinogens and MDMA have serotonin 2A agonist effects, Erritzoe and colleagues 26 predicted that the serotonin 2A receptor levels would be lower in recent hallucinogen and MDMA users than in controls. However, use of MDMA or hallucinogens was not clearly associated with lower serotonin 2A receptor binding, despite reductions in the serotonin transporter binding in the MDMA-preferring group. In a subset analysis of users with longer periods of MDMA abstinence that more closely paralleled those of the users in the study by Reneman and colleagues, 25 Erritzoe and colleagues 26 were unable to detect chronic increases in serotonin 2A binding, and they considered that this was potentially due to the opposing effects of hallucinogen use on receptor regulation or to the reduced serotonin transporter binding and associated changes in serotonin transmission. Concern for the possibility of residual acute effects of recent MDMA use led to our choice of a minimum day abstinence from MDMA and other drugs potentially influencing the serotonin 2A receptor levels as a requirement for enrollment. Although we did not find evidence to suggest that receptor levels decrease with increasing abstinence from MDMA, it is possible that the serotonin 2A receptor levels might have normalized in our cohort with a greater period of abstinence. The basis for the pattern of findings is unclear. It is possible that serotonin axons in some brain regions are more vulnerable to the effects of MDMA or that regional differences in serotonin 2A receptors account for the findings. There was considerable overlap between regions having increased serotonin 2A levels in MDMA users and regions showing a positive association of serotonin 2A BP ND and lifetime ecstasy use, suggesting that MDMA exposure may account for the findings in both analyses. Although we did not detect differences in depression or anxiety, 84 , 85 impulsivity, or novelty seeking between MDMA users and controls, the cross-sectional study method that we used cannot rule out the possibility that preexisting differences in brain function, personality, or behavior 86 , 87 might predispose to MDMA use and might also be associated with altered serotonin function. Some evidence suggests that memory impairment persists in abstinent MDMA users, despite the potential for recovery of the serotonin transporter. However, the relationship between memory, the serotonin 2A receptor, and the serotonin transporter may prove complex because McCann and colleagues 89 reported that verbal memory correlated more strongly with serotonin transporter levels in controls than in MDMA users and because preliminary data suggested that verbal memory was negatively correlated with serotonin 2A receptors in MDMA users. Because MDMA users have been reported to have impairments in neurocognition, 12 sleep, 90 and altered pain processing, 91 as well as increased sleep apnea, 92 studies assessing the relationship of serotonin function with these conditions are warranted. We applied strict inclusion criteria to our cohort and restricted our study to female users to maximize cohort homogeneity and to isolate the effects of MDMA on serotonin 2A receptors. We controlled for factors associated with receptor binding in our cohort estrogen level, use of birth control, and age , but the number of variables that we adjusted for was large relative to our sample size. Therefore, we may not have fully accounted for the influence of these variables in the overall model. Because we studied healthy women, we cannot generalize these findings to men or individuals with anxiety or depression. However, we consider it likely that similar processes operate in men and that the association of MDMA use with serotonin 2A levels is likely to be equally evident, if not more so, in those more vulnerable to psychiatric disorders. Given the major role that serotonin plays in anxiety and mood disorders, coupled with evidence from some studies that MDMA users have higher rates of anxiety and depression, 84 , 85 additional studies that examine serotonin 2A receptor status in a broader range of cohorts are warranted. Although we did not find strong evidence that drug use was higher in the MDMA users, this is likely in part due to sample size limitations. However, we did not detect a significant association between other drug use and serotonin 2A receptor levels, and it therefore seems unlikely that other drug exposure accounts for the current findings. We did not assess MDMA users to determine why they stopped using MDMA, creating the possibility that we recruited a group of participants who stopped using MDMA owing to negative effects and who potentially were more vulnerable to toxicity. Although we excluded participants who had been diagnosed and treated for psychiatric conditions such as depression, it is possible that some participants had prior exposure to non-recreational drugs that could potentially affect the serotonin 2A receptor levels. Although we interpret our findings as consistent with reduced cortical serotonin signaling, we did not obtain additional measures of cortical serotonin signaling, such as cerebrospinal fluid serotonin metabolite levels. MDMA is a fascinating drug that acutely affects psychological processes and social behaviors. Acute MDMA use produces a sense of improved mood and well-being 94 and enhances sociability. Human MDMA plasma concentrations increase greatly when multiple dosages are taken within a narrow time window, 96 and animal studies have demonstrated that MDMA's serotonin toxicity is dependent on the dose and the presence of hyperthermia. In conclusion, our findings indicate that human MDMA use is associated with long-lasting changes in serotonin 2A receptor availability that do not decrease with drug abstinence. Our results suggest that MDMA produces chronic alterations in cortical serotonin signaling that is possibly reflective of MDMA-induced neurotoxicity in humans. Given the broad role that serotonin plays in human brain function, the possibility for therapeutic MDMA use, and the widespread recreational popularity of this drug, our results have critical implications for human MDMA users. Correspondence: Ronald L. Submitted for Publication: May 5, ; final revision received August 23, ; accepted October 12, Published Online: December 5, View Large Download. Table 1. Table 2. 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Effects of dose, sex, and long-term abstention from use on toxic effects of MDMA ecstasy on brain serotonin neurons. Br J Psychiatry. Am J Psychiatry. Paradoxical trafficking and regulation of 5-HT 2A receptors by agonists and antagonists. Brain Res Bull. Biological basis of sex differences in drug abuse: preclinical and clinical studies. Clin Pharmacokinet. Gender differences in the subjective effects of MDMA. Gender, personality, and serotonin-2A receptor binding in healthy subjects. Psychiatry Res. Sex difference in 5HT2 receptor in the living human brain. Neurosci Lett. A method for the in vivo investigation of the serotonergic 5-HT2 receptors in the human cerebral cortex using positron emission tomography and 18F-labeled setoperone. J Neurochem. Human ecstasy use is associated with increased cortical excitability: an fMRI study. Pharmacol Biochem Behav. 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Analyses of \[ 18 F\] altanserin bolus injection PET data: I, consideration of radiolabeled metabolites in baboons. Rapid synthesis of \[ 18 F\]setoperone by microwave heating and simple purification. Midbrain dopamine receptor availability is inversely associated with novelty-seeking traits in humans. J Neurosci. Mesolimbic dopamine reward system hypersensitivity in individuals with psychopathic traits. Nat Neurosci. The interrelationship of dopamine D2-like receptor availability in striatal and extrastriatal brain regions in healthy humans: a principal component analysis of \[18F\]fallypride binding. Multimodality image registration by maximization of mutual information. Multi-modal volume registration by maximization of mutual information. Med Image Anal. Mutual information matching in multiresolution contexts. Image Vis Comput. Comparison of methods for analysis of clinical \[11C\]raclopride studies. J Cereb Blood Flow Metab. Estimation of neocortical serotonin-2 receptor binding potential by single-dose fluorinesetoperone kinetic PET data analysis. J Nucl Med. Estimation of binding potential for the 5HT2 receptor ligand \[18F\]setoperone by a noninvasive reference region graphical method. Widespread increases of cortical serotonin type 2A receptor availability after hormone therapy in euthymic postmenopausal women. Fertil Steril. Age-related decline of serotonin transporters in living human brain of healthy males. Life Sci. Molecular and cellular mechanisms of ecstasy-induced neurotoxicity: an overview. Mol Neurobiol. Distinct morphologic classes of serotonergic axons in primates exhibit differential vulnerability to the psychotropic drug 3,4-methylenedioxymethamphetamine. Lyles J, Cadet JL. Brain Res Brain Res Rev. Extended characterisation of the serotonin 2A 5-HT 2A receptor-selective PET radiotracer 11 C-MDL in humans: quantitative analysis, test-retest reproducibility, and vulnerability to endogenous 5-HT tone \[published online ahead of print July 18, \]. Neuroimage Google Scholar. Acute and chronic tryptophan depletion differentially regulate central 5-HT1A and 5-HT 2A receptor binding in the rat. Prefrontal serotonergic denervation induces increase in the density of 5-HT2A receptors in adult rat prefrontal cortex. Neurochem Res. Brain Res. Regional central serotonin-2 receptor binding and phosphoinositide turnover in rats with 5,7-dihydroxytryptamine lesions. Drug Alcohol Depend Google Scholar. Harv Rev Psychiatry. Morgan MJ. Drug Alcohol Depend. Mood, cognition and serotonin transporter availability in current and former ecstasy MDMA users: the longitudinal perspective. Biol Psychiatry. Br J Clin Pharmacol. See More About Radiology. Save Preferences. Privacy Policy Terms of Use. This Issue. Views 14, Citations View Metrics. X Facebook More LinkedIn. Original Article. Christina R. Watkins, BA ; Mary S. Ansari, PhD ; Ronald M. Kessler, MD ; Ronald M. Cowan, MD, PhD. Inclusion criteria. Exclusion criteria. Pet scanning. Image and data analysis. Between-group analysis. Within-group analysis. Within-group analysis of mdma dose effects. Within-group analysis of polydrug use effects. Back to top Article Information. Financial Disclosure: None reported. Access your subscriptions. Access through your institution. Add or change institution. Free access to newly published articles. Purchase access. Rent article Rent this article from DeepDyve. Sign in to access free PDF. Save your search. Customize your interests. Create a personal account or sign in to:. Privacy Policy. Make a comment.

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