Hostname: page-component-7c8c6479df-8mjnm Total loading time: 0 Render date: 2024-03-28T14:53:35.270Z Has data issue: false hasContentIssue false

Differences in prefrontal blood oxygenation during an acute multitasking stressor in ecstasy polydrug users

Published online by Cambridge University Press:  20 June 2014

C. A. Roberts
Affiliation:
School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, UK
M. A. Wetherell
Affiliation:
Health in Action: Stress Research Group, Department of Psychology, University of Northumbria, Newcastle upon Tyne, UK
J. E. Fisk
Affiliation:
School of Psychology, University of Central Lancashire, Preston, UK
C. Montgomery*
Affiliation:
School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, UK
*
*Address for correspondence: C. Montgomery, School of Natural Sciences and Psychology, Liverpool John Moores University, Byrom Street, Liverpool L3 3AF, UK. (Email: c.a.montgomery@ljmu.ac.uk)

Abstract

Background

Cognitive deficits are well documented in ecstasy (3,4-methylenedioxymethamphetamine; MDMA) users, with such deficits being taken as evidence of dysregulation of the serotonin (5-hydroxytryptamine; 5-HT) system. More recently neuroimaging has been used to corroborate these deficits. The present study aimed to assess multitasking performance in ecstasy polydrug users, polydrug users and drug-naive individuals. It was predicted that ecstasy polydrug users would perform worse than non-users on the behavioural measure and this would be supported by differences in cortical blood oxygenation.

Method

In the study, 20 ecstasy-polydrug users, 17 polydrug users and 19 drug-naive individuals took part. On day 1, drug use history was taken and questionnaire measures were completed. On day 2, participants completed a 20-min multitasking stressor while brain blood oxygenation was measured using functional near infrared spectroscopy (fNIRS).

Results

There were no significant differences between the three groups on the subscales of the multitasking stressor. In addition, there were no significant differences on self-report measures of perceived workload (NASA Task Load Index). In terms of mood, ecstasy users were significantly less calm and less relaxed compared with drug-naive controls. There were also significant differences at three voxels on the fNIRS, indicating decreased blood oxygenation in ecstasy users compared with drug-naive controls at voxel 2 (left dorsolateral prefrontal cortex), voxel 14 and voxel 16 (right dorsolateral prefrontal cortex), and compared with polydrug controls at V14.

Conclusions

The results of the present study provide support for changes in brain activation during performance of demanding tasks in ecstasy polydrug users, which could be related to cerebral vasoconstriction.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ayaz, H (2010). Functional near infrared spectroscopy based brain computer interface . PhD Thesis, Drexel University, Philadelphia, PA.Google Scholar
Ayaz, H, Shewokis, PA, Bunce, S, Izzetoglu, K, Willems, B, Onaral, B (2012). Optical brain monitoring for operator training and mental workload assessment. NeuroImage 59, 3647.CrossRefGoogle ScholarPubMed
Ayaz, H, Shewokis, PA, Curtin, A, Izzetoglu, M, Izzetoglu, K, Onaral, B (2011). Using MazeSuite and functional near infrared spectroscopy to study learning in spatial navigation. Journal of Visualized Experiments 56, e3443.Google Scholar
Benningfield, MM, Cowan, RL (2013). Brain serotonin function in MDMA (ecstasy) users: evidence for persisting neurotoxicity. Neuropsychopharmacology 38, 253255.CrossRefGoogle ScholarPubMed
Bosch, OG, Wagner, M, Jessen, F, Kühn, KU, Joe, A, Seifritz, E, Maier, W, Biersack, HJ, Quednow, BB (2013). Verbal memory deficits are correlated with prefrontal hypometabolism in 18FDG PET of recreational MDMA users. PLOS ONE 8, e61234.CrossRefGoogle ScholarPubMed
Burgess, AP, Venables, L, Jones, H, Edwards, R, Parrott, AC (2011). Event related potential (ERP) evidence for selective impairment of verbal recollection in abstinent recreational methylenedioxymethamphetamine (‘ecstasy’)/polydrug users. Psychopharmacology 216, 545556.CrossRefGoogle ScholarPubMed
Chang, L, Grob, CS, Ernst, T, Itti, L, Mishkin, FS, Jose-Melchor, R, Poland, RE (2000). Effect of ecstasy [3,4-methylenedioxymethamphetamine (MDMA)] on cerebral blood flow: a co-registered SPECT and MRI study. Psychiatry Research 98, 1528.CrossRefGoogle ScholarPubMed
Cui, X, Bray, S, Reiss, AL (2010). Functional near infrared spectroscopy (NIRS) signal improvement based on negative correlation between oxygenated and deoxygenated hemoglobin dynamics. NeuroImage 49, 30393046.CrossRefGoogle ScholarPubMed
Curtis, CE, D'Esposito, M (2003). Persistent activity in the prefrontal cortex during working memory. Trends in Cognitive Sciences 7, 415423.CrossRefGoogle ScholarPubMed
Ehlis, A-C, Bahne, CG, Jacob, CP, Herrmann, MJ, Fallgatter, AJ (2008). Reduced lateral prefrontal activation in adult patients with attention-deficit/hyperactivity disorder (ADHD) during a working memory task: a functional near-infrared spectroscopy (fNIRS) study. Journal of Psychiatric Research 42, 10601067.CrossRefGoogle ScholarPubMed
Erritzoe, D, Frokjaer, VG, Holst, KK, Christoffersen, M, Johansen, SS, Svarer, C, Madsen, J, Rasmussen, PM, Ramsøy, T, Jernigan, TL, Knudsen, GM (2011). In vivo imaging of cerebral serotonin transporter and serotonin2A receptor binding in 3,4-methylenedioxy-methamphetamine (MDMA or ‘ecstasy’) and hallucinogen users. Archives of General Psychiatry 68, 562576.CrossRefGoogle Scholar
Evers, EAT, Cools, R, Clark, L, van der Veen, FM, Jolles, J, Sahakian, BJ, Robbins, TW (2005). Serotonergic modulation of prefrontal cortex during negative feedback in probabilistic reversal learning. Neuropsychopharmacology 30, 11381147.CrossRefGoogle ScholarPubMed
Firbank, M, Okada, E, Delpy, DT (1998). A theoretical study of the signal contribution of regions of the adult head to near-infrared spectroscopy studies of visual evoked responses. NeuroImage 8, 6978.CrossRefGoogle ScholarPubMed
Fisk, JE, Montgomery, C, Hadjiefthyvoulou, F (2011). Visuospatial working memory impairment in current and previous ecstasy/polydrug users. Human Psychopharmacology 26, 313321.CrossRefGoogle ScholarPubMed
Fisk, JE, Montgomery, C, Murphy, P, Wareing, M (2004). Evidence for executive deficits among users of MDMA (ecstasy). British Journal of Psychology 95, 457466.CrossRefGoogle ScholarPubMed
Fox, HC, Parrott, AC, Turner, JJD (2001). Ecstasy use: cognitive deficits related to dosage rather than self-reported problematic use of the drug. Journal of Psychopharmacology 15, 273281.CrossRefGoogle ScholarPubMed
Fox, HC, McLean, A, Turner, JJD, Parrott, AC, Rogers, R, Sahakian, BJ (2002). Neuropsychological evidence of a relatively selective profile of temporal dysfunction in drug-free MDMA (‘ecstasy’) polydrug users. Psychopharmacology 162, 203214.CrossRefGoogle ScholarPubMed
Gouzoulis-Mayfrank, M, Daumann, J (2009). Neurotoxicity of drugs of abuse – the case of methylenedioxy amphetamines (MDMA, ecstasy), and amphetamines. Dialogues in Clinical Neuroscience 11, 305317.CrossRefGoogle Scholar
Green, AR, Cross, AJ, Goodwin, GM (1995). Review of the pharmacology and clinical pharmacology of 3,4-methylenedioxy-methamphetamine (MDMA or ‘Ecstasy’). Psychopharmacology 119, 247260.CrossRefGoogle Scholar
Green, AR, Mechan, AO, Elliot, JM, O'Shea, E, Colado, MI (2003). The pharmacology and clinical pharmacology of 3,4-methylenedioxy-methamphetamine (MDMA, ‘ecstasy’). Pharmacological Reviews 55, 463508.CrossRefGoogle Scholar
Hart, SG, Staveland, LE (1988). Development of NASA-TLX (Task Load Index): results of empirical and theoretical research. In Human Mental Workload (ed. Hancock, P. A. and Meshkati, N.) pp. 239250 North Holland Press: Amsterdam.Google Scholar
Hoshi, Y, Kobayashi, N, Tamura, M (2001). Interpretation of near-infrared signals: a study with newly developed perfused rat brain model. Journal of Applied Physiology 90, 16571662.CrossRefGoogle ScholarPubMed
Izzetoglu, K, Bunce, S, Onaral, B, Pourrezaei, K, Chance, B (2004). Functional optical brain imaging using near-infrared during cognitive tasks. International Journal of Human-Computer Interaction 17, 211227.CrossRefGoogle Scholar
Jager, G, de Win, MML, van der Tweel, I, Schilt, T, Kahn, RS, van den Brink, W, van Ree, JM, Ramsey, NF (2008). Assessment of cognitive brain function in ecstasy users and contributions of other drugs of abuse: results from an fMRI study. Neuropsychopharmacology 33, 247258.CrossRefGoogle ScholarPubMed
Kalechstein, AD, De La Garza, R II, Mahoney, JJ III, Fantegrossi, WE, Newton, TF (2007). MDMA use and neurocognition: a meta-analytic review. Psychopharmacology 189, 531537.CrossRefGoogle ScholarPubMed
Kanayama, G, Rogowska, J, Pope, HG, Gruber, SA, Yurglun-Todd, DA (2004). Spatial working memory in heavy cannabis users: a functional magnetic resonance imaging study. Psychopharmacology 176, 239247.CrossRefGoogle ScholarPubMed
Kish, SJ, Lerch, J, Furukawa, Y, Tong, J, McCluskey, T, Wilkins, D, Houle, S, Meyer, J, Mundo, E, Wilson, AA, Rusjan, PM, Saint-Cyr, JA, Guttman, M, Collins, DL, Shapiro, C, Warsh, JJ, Boileau, I (2010). Decreased cerebral cortical serotonin transporter binding in ecstasy users: a positron emission tomography/[11C]DASB and structural brain imaging study. Brain 133, 17791797.CrossRefGoogle Scholar
Leff, DR, Elwell, CE, Orihuela-Espina, F, Atallah, L, Delpy, DT, Darzi, AW, Yang, GY (2008). Changes in prefrontal cortical behaviour depend upon familiarity on a bimanual co-ordination task: an fNIRS study. NeuroImage 39, 805813.CrossRefGoogle ScholarPubMed
Leff, DR, Orihuela-Espina, F, Elwell, CE, Athanasiou, T, Delpy, DT, Darzi, AW, Yand, G-Z (2011). Assessment of the cerebral cortex during motor task behaviours in adults: a systematic review of functional near infrared spectroscopy (fNIRS) studies. NeuroImage 54, 29222936.CrossRefGoogle ScholarPubMed
McCann, UD, Ridenour, A, Shaham, Y, Ricaurte, GA (1994). Serotonin neurotoxicity after 3,4-methelenedioxymethamphetamine (MDMA; ‘ecstasy’): a controlled study in humans. Neuropsychopharmacology 10, 129138.CrossRefGoogle Scholar
McDowell, DM, Kleber, HD (1994). MDMA: its history and pharmacology. Psychiatric Annals 24, 127130.CrossRefGoogle Scholar
Montgomery, C, Fisk, JE (2008). Ecstasy-related deficits in the updating component of executive processes. Human Psychopharmacology 23, 495511.CrossRefGoogle ScholarPubMed
Montgomery, C, Fisk, JE, Newcombe, R, Murphy, PN (2005). The differential effects of ecstasy/polydrug use on executive components: shifting, inhibition, updating and access to semantic memory. Psychopharmacology 182, 262276.CrossRefGoogle ScholarPubMed
Montgomery, C, Hatton, PN, Fisk, JE, Ogden, RS, Jansari, A (2010). Assessing the functional significance of ecstasy-related memory deficits using a virtual paradigm. Human Psychopharmacology 25, 318325.CrossRefGoogle ScholarPubMed
Parrott, AC (2004). Is ecstasy MDMA? A review of the proportion of ecstasy tablets containing MDMA, their dosage levels, and the changing perceptions of purity. Psychopharmacology (Berlin) 173, 234241.CrossRefGoogle ScholarPubMed
Parrott, AC (2013). MDMA, serotonergic neurotoxicity, and the diverse functional deficits of recreational ‘ecstasy’ users. Neuroscience and Biobehavioral Reviews 37, 14661484.CrossRefGoogle ScholarPubMed
Parrott, AC, Lasky, J (1998). Ecstasy (MDMA) effects upon mood and cognition: before, during and after a Saturday night dance. Psychopharmacology 139, 261268.CrossRefGoogle ScholarPubMed
Parrott, AC, Sisk, E, Turner, JJD (2000). Psychobiological problems in heavy ‘ecstasy’ (MDMA) polydrug users. Drug and Alcohol Dependence 60, 105110.Google ScholarPubMed
Pazos, A, Prosbit, A, Palacios, JM (1987). Serotonin receptors in the human brain – III. Autoradiographic mapping of serotonin-1 receptors. Neuroscience 21, 97122.CrossRefGoogle ScholarPubMed
Raven, J, Raven, JC, Court, HH (1998). Manual for Raven's Progressive Matrices and Vocabulary Scales. Oxford Psychologists Press: Oxford, UK.Google Scholar
Reneman, L, Habraken, JBA, Majoie, CBL, Booij, J, den Heeten, GJ (2000). MDMA (‘ecstasy’) and its association with cerebrovascular accidents: preliminary findings. American Journal of Neuroradiology 21, 10011007.Google ScholarPubMed
Reneman, L, Schilt, T, de Win, MM, Booij, J, Schmand, B, van den Brink, W, Bakker, O (2006). Memory function and serotonin transporter promoter gene polymorphism in ecstasy (MDMA) users. Psychopharmacology 20, 389399.CrossRefGoogle ScholarPubMed
Robbins, TW, Arnsten, AF (2009). The neuropsychopharmacology of fronto-executive function: monoaminergic modulation. Annual Review of Neuroscience 32, 267287.CrossRefGoogle ScholarPubMed
Roberts, C, Fairclough, S, Fisk, JE, Tames, F, Montgomery, C (2013 a). Electrophysiological indices of response inhibition in human polydrug users. Journal of Psychopharmacology 27, 779789.CrossRefGoogle ScholarPubMed
Roberts, CA, Fairclough, SF, Fisk, JE, Tames, F, Montgomery, C (2013 b). ERP evidence suggests executive dysfunction in ecstasy polydrug users. Psychopharmacology 3, 375388.CrossRefGoogle Scholar
Rodgers, J (2000). Cognitive performance amongst recreational users of ‘ecstasy’. Psychopharmacology 151, 1924.CrossRefGoogle ScholarPubMed
Rodgers, J, Buchanan, T, Scoley, AB, Heffernan, TM, Ling, J, Parrott, AC (2003). Patterns of drug use and the influence of gender on self reports of memory ability in ecstasy users: a web based study. Journal of Psychopharmacology 17, 389396.CrossRefGoogle ScholarPubMed
Sankoh, AJ, Huque, MF, Dubey, SD (1997). Some comments on frequently used multiple endpoint adjustment methods in clinical trials. Statistics in Medicine 16, 25292542.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Schecklmann, M, Ehlis, AC, Plichta, MM, Romanos, J, Heine, M, Boreatti-Hümmer, A, Jacob, C, Falgatter, AJ (2008). Diminished prefrontal oxygenation with normal and above-average verbal fluency performance in adult ADHD. Journal of Psychiatric Research 43, 98106.CrossRefGoogle ScholarPubMed
Scholey, AB, Owen, L, Gates, J, Rodgers, J, Buchanan, T, Ling, J, Heffernan, T, Swan, P, Stough, C, Parrott, AC (2011). Hair MDMA samples are consistent with reported ecstasy use: findings from a study investigating effects of Ecstasy on mood and memory. Neuropsychobiology 63, 1521.CrossRefGoogle ScholarPubMed
Taussky, P, O'Neal, B, Daugherty, WP, Luke, S, Thorpe, D, Pooley, RA, Evans, C, Hanel, RA, Freeman, WD (2012). Validation of frontal near-infrared spectroscopy as noninvasive bedside monitoring for regional cerebral blood flow in brain-injured patients. Neurosurgical Focus 32, E2.CrossRefGoogle ScholarPubMed
Wareing, M, Murphy, PN, Fisk, JE (2004). Visuospatial memory impairments in users of MDMA (‘ecstasy’). Psychopharmacology 173, 391397.CrossRefGoogle ScholarPubMed
Wetherell, MA, Atherton, K, Grainger, J, Brosnan, R, Scholey, AB (2012). The effects of multitasking on psychological stress reactivity in recreational users of cannabis and MDMA. Human Psychopharmacology: Clinical and Experimental 27, 167176.CrossRefGoogle ScholarPubMed
Wetherell, MA, Sidgreaves, MC (2005). Short communication: secretory immunoglobulin – a reactivity following increases in workload intensity using the Defined Intensity Stressor Simulation (DISS). Stress and Health 21, 99106.CrossRefGoogle Scholar
Zakzanis, KK, Campbell, Z, Jovanovski, D (2007). The neuropsychology of ecstasy (MDMA) use: a quantitative review. Human Psychopharmacology: Clinical and Experimental 22, 427435.CrossRefGoogle ScholarPubMed