Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-26T16:50:13.263Z Has data issue: false hasContentIssue false
  • English
  • Français

Profiles of visuospatial memory dysfunction in opioid-exposed and dependent populations

Published online by Cambridge University Press:  20 November 2018

A. Baldacchino ,
S. Tolomeo ,
D.J. Balfour  and
K Matthews
A. Baldacchino*
Affiliation:
Division of Population and Behavioural Science, School of Medicine, St Andrews University, St Andrews, Fife, UK
S. Tolomeo
Affiliation:
School of Medicine (Neuroscience), Ninewells Hospital & Medical School, University of Dundee, Dundee, Tayside, UK
D.J. Balfour
Affiliation:
School of Medicine (Neuroscience), Ninewells Hospital & Medical School, University of Dundee, Dundee, Tayside, UK
K Matthews
Affiliation:
School of Medicine (Neuroscience), Ninewells Hospital & Medical School, University of Dundee, Dundee, Tayside, UK
*
Author for correspondence: A. Baldacchino, E-mail: amb30@st-andrews.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Chronic opioid exposure is common world-wide, but behavioural performance remains under-investigated. This study aimed to investigate visuospatial memory performance in opioid-exposed and dependent clinical populations and its associations with measures of intelligence and cognitive impulsivity.

Methods

We recruited 109 participants: (i) patients with a history of opioid dependence due to chronic heroin use (n = 24), (ii) heroin users stabilised on methadone maintenance treatment (n = 29), (iii) participants with a history of chronic pain and prescribed tramadol and codeine (n = 28) and (iv) healthy controls (n = 28). The neuropsychological tasks from the Cambridge Neuropsychological Test Automated Battery included the Delayed Matching to Sample (DMS), Pattern Recognition Memory, Spatial Recognition Memory, Paired Associate Learning, Spatial Span Task, Spatial Working Memory and Cambridge Gambling Task. Pre-morbid general intelligence was assessed using the National Adult Reading Test.

Results

As hypothesised, this study identified the differential effects of chronic heroin and methadone exposures on neuropsychological measures of visuospatial memory (p < 0.01) that were independent of injecting behaviour and dependence status. The study also identified an improvement in DMS performance (specifically at longer delays) when the methadone group was compared with the heroin group and also when the heroin group was stabilised onto methadone. Results identified differential effects of chronic heroin and methadone exposures on various neuropsychological measures of visuospatial memory independently from addiction severity measures, such as injecting behaviour and dependence status.

Keywords

Codeinecognitionheroinmethadoneopioidstramadolvisuospatial memory
Type
Original Articles
Information
Psychological Medicine , Volume 49 , Issue 7 , May 2019 , pp. 1174 - 1184
Copyright
Copyright © Cambridge University Press 2018 

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

Ardila, M, Rosselli, E, Matute, O and Inozemtseva, O (2011) Gender differences in cognitive development. Developmental Psychology 47, 984–990.Google Scholar
Awh, E, Vogel, EK and Oh, SH (2006) Interactions between attention and working memory. Neuroscience 139, 201–208.Google Scholar
Bach, P, Vollstädt-Klein, S, Frischknecht, U, Hoerst, M, Kiefer, F, Mann, K, Ende, G and Hermann, D (2012) Diminished brain Functional Magnetic Resonance imaging activation in patients on opiate maintenance despite normal spatial working memory task performance. Clinical Neuropharmacology 35, 153–160.Google Scholar
Baddeley, AD and Hitch, GJ (1974) Working memory. In Bower, GA (ed.), Recent Advances in Learning and Motivation. New York: Academic Press, pp. 47–90.Google Scholar
Baddeley, AD and Logie, RH (1999) Working memory: the multiple component model. In Miyake, A and Shah, P (eds), Models of Working Memory. New York: Cambridge University Press, pp. 29–61.Google Scholar
Baldacchino, A (2011) Procedure for Tolerance Testing (A1), NHS Fife Addiction Services. Fife Area and Drug Therapeutic Committee (ADTC), Fife. https://www.fifeadtc.scot.nhs.uk/media/7032/a1-procedure-for-tolerance-testing-final-april-2011.pdf. Accessed 23rd September 2018.Google Scholar
Baldacchino, A, Balfour, D, Passetti, F, Humphris, G and Matthews, K (2012) The neuropsychological consequences of chronic opioid use: a quantitative review and meta-analysis. Neuroscience and Biobehavioral Review 36, 2056–2068.Google Scholar
Baldacchino, A, Balfour, DJ and Matthews, K (2014) Impulsivity and opioid drugs: differential effects of heroin, methadone and prescribed analgesic medication. Psychological Medicine 8, 1–13.Google Scholar
Baldacchino, A, Armanyous, M, Balfour, D, Humphris, G and Matthews, K (2017) The neuropsychological consequences of chronic methadone use: a quantitative review and meta-analysis. Neuroscience and Biobehavioural Review 73, 23–38.Google Scholar
Bormann, T, Seyboth, M, Umarova, R and Weiller, C (2015) ‘I know your name, but not your number’–patients with verbal short-term memory deficits are impaired in learning sequences of digits. Neuropsychologia 72, 80–86.Google Scholar
Darke, S, Sims, J, McDonald, S and Wickes, W (2000) Cognitive impairment among methadone maintenance patients. Addiction 95, 687–695.Google Scholar
Davis, AM and Inturrisi, CE (1999) D-Methadone blocks morphine tolerance and N-methyl-D-aspartate-induced hyperalgesia. Journal of Pharmacology and Experimental Therapeutics 289, 1048–1053.Google Scholar
Day, M, Langston, R and Morris, RGM (2003) Glutamate-receptor-mediated encoding and retrieval of paired-associate learning. Nature 424, 205–209.Google Scholar
Deeb, TZ, Sharp, D and Hales, TG (2009) Direct subunit-dependent multimodal 5-hydroxytryptamine receptor antagonism by methadone. Molecular Pharmacology 75, 908–917.Google Scholar
Della Sala, S, Gray, C, Baddeley, A, Allamano, N and Wilson, L (1999) Pattern span: a tool for unwelding visuo-spatial memory. Neuropsychologia 37, 1189–1199.Google Scholar
Ekhtiari, H, Rezapour, T, Robin, RL, Aupperle, L and Paulus, MP (2017) Neuroscience-informed psychoeducation for addiction medicine: A neurocognitive perspective. Progress in Brain Research ISSN 0079-6123 https://doi.org/10.1016/bs.pbr.2017.08.013. Accessed 20th January 2018.Google Scholar
Eriksson, J, Vogel, EK, Lansner, A, Bergstrom, F and Nyberg, L (2015) Neurocognitive architecture of working memory. Neuron 88, 33–46.Google Scholar
Ersche, KD, Fletcher, PC, Lewis, SJG, Clark, L, Stocks-Gee, G, London, M, Deakin, JB, Robbins, TW and Sahakian, BJ (2005) Abnormal frontal activations related to decision-making in current and former amphetamine and opiate dependent individuals. Psychopharmacology 180, 612–623.Google Scholar
Ersche, KD, Clark, L, London, M, Robbins, TW and Sahakian, BJ (2006) Profile of executive and memory function associated with amphetamine and opiate dependence. Neuropsychopharmacology 31, 1036–1047.Google Scholar
Fagerstrom, KO and Schneider, NG (1989) Measuring nicotine dependence: a review of the Fagerstrom Tolerance Questionnaire. Journal of Behavioral Medicine 12, 159–182.Google Scholar
Fernandez-Serrano, MJ, Perez-Garcia, M and Verdejo-Garcia, A (2011) What are the specific v. generalised effects of drugs of abuse on neuropsychological performance? Neuroscience and Biobehavioural Reviews 35, 377–406.Google Scholar
Field, A (2009) Discovering Statistics Using SPSS, 3rd Edn. London: SAGE Publications.Google Scholar
Gagnon, B and Bruera, E (1999) Differences in the ratios of morphine to methadone in patients with neuropathic pain versus non-neuropathic pain. Journal of Pain Symptom Management 18, 120–125.Google Scholar
Grevert, P, Masover, B and Goldstein, A (1977) Failure of methadone and levomethadyl acetate (levo-alpha-acetylmethadol, LAAM) maintenance to effect memory. Archives of General Psychiatry 34, 849–853.Google Scholar
Hackman, DA, Farah, MJ and Meaney, MJ (2010) Socioeconomic status and the brain: mechanistic insights from human and animal research. Nature Reviews Neuroscience 11, 651–659.Google Scholar
Hanson, JL, Nacewicz, BM, Sutterer, MJ, Cayo, AA, Schaefer, SM, Rudolph, KD, Shirtcliff, EA, Pollak, SD and Davidson, RJ (2015) Behavioral problems after early life stress, contributions of the hippocampus and amygdala. Biological Psychiatry 77, 314–323.Google Scholar
Henry, PK, Umbricht, A, Kleykamp, BA, Vandrey, R, Strain, EC, Bigelow, GE and Mintzer, MZ (2012) Comparison of cognitive performance in methadone maintenance patients with and without current cocaine dependence. Drug and Alcohol Dependence 124, 167–171.Google Scholar
Hepner, IJ, Homewood, J and Taylor, AJ (2002) Methadone disrupts performance on the working memory version of the morris water task. Physiology and Behavior 76, 41–49.Google Scholar
Hyman, SE (2005) Addiction: a disease of learning and memory. American Journal of Psychiatry 162, 1414–1422.Google Scholar
Hyman, SE, Malenka, RC and Nestler, EJ (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annual Review of Neuroscience 29, 565–598.Google Scholar
Jollant, F, Guillaume, S, Jaussent, I, Castelnau, D, Malafosse, A and Courtet, P (2007) Impaired decision-making in suicide attempters may increase the risk of problems in affective relationships. Journal of Affective Disorders 99, 59–62.Google Scholar
Koob, GF and Volkow, ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35, 217–238.Google Scholar
Krugers, HJ, Arpa, JM, Xiong, H, Kanatsou, S, Lesuis, SL, Korosi, A, Joels, M and Lucassen, PJ (2017) Early life adversity: lasting consequences for emotional learning. Neurobiology of Stress 6, 14–21.Google Scholar
Kübler, A, Murphy, K and Garavan, H (2005) Cocaine dependence and attention switching within and between verbal and visuospatial working memory. European Journal of Neuroscience 21, 1984–1992.Google Scholar
Lin, W-C, Chou, K-H, Chen, H-L, Huang, C-C, Lu, C-H, Li, S-H, Wang, Y-L, Cheng, Y-F, Lin, C-P and Chen, C-C (2012) Structural deficits in the emotion circuit and cerebellum are associated with depression, anxiety and cognitive dysfunction in methadone maintenance patients: a voxel-based morphometric study. Psychiatry Research 201, 89–97.Google Scholar
Lintzeris, N, Mitchell, TB, Bond, A, Nestor, L and Strang, J (2006) Interactions on mixing diazepam with methadone or buprenorphine in maintenance patients. Journal of Clinical Psychopharmacology 26, 274–283.Google Scholar
Loeber, S, Kniest, A, Diehl, A, Mann, K and Croissant, B (2008) Neuropsychological functioning of opiate-dependent patients: a nonrandomized comparison of patients preferring either buprenorphine or methadone maintenance treatment. American Journal of Drug and Alcohol Abuse 34, 584–593.Google Scholar
Mammarella, IC, Pazzaglia, F and Cornoldi, C (2008) Evidence for different components in children's visuospatial working memory. British Journal of Developmental Psychology 26, 337–335.Google Scholar
Marsden, J, Gossop, G, Stewart, D, Best, D, Farrell, M, Lehmann, P, Edwards, C and Strang, J (1998) The maudsley addiction profile (MAP): a brief instrument for assessing treatment outcome. Addiction 93, 1857–1867.Google Scholar
McDonald, S, Darke, S, Kaye, S and Torok, M (2012) Deficits in social perception in opioid maintenance patients, abstinent opioid users and non-opioid users. Addiction 108, 566–574.Google Scholar
McGivern, RF, Adams, A, Handa, RJ and Pineda, JA (2012) Men and women exhibit a differential bias for processing movement versus objects. PLoS ONE 7, e32238 http://dx.doi.org/10.1371/journal.pone.003223. Accessed 20th August 2018.Google Scholar
Miyake, A and Shah, P (1999) Models of Working Memory. Mechanisms of Active Maintenance and Executive Control. Cambridge: Cambridge University Press.Google Scholar
Nelson, HE (1982) National Adult Reading Test (NART): Test Manual. Windsor, UK: NFER. Nelson.Google Scholar
Ornstein, TJ, Iddon, JL, Baldacchino, AM, Sahakian, BJ, London, M, Everitt, BJ and Robbins, TW (2000) Profiles of cognitive dysfunction in chronic amphetamine and heroin abusers. Neuropsychopharmacology 23, 113–126.Google Scholar
Passolunghi, MC and Mammarella, IC (2010) Spatial and visual working memory ability in children with difficulties in arithmetic word problem solving. European Journal of Cognitive Psychology 22, 944–963.Google Scholar
Pasternak, GW (2012) Preclinical pharmacology and opioid combinations. Pain Medicine 13, S4–S11.Google Scholar
Pathan, H and Williams, J (2012) Basic opioid pharmacology: an update. British Journal of Pain 6, 11–16.Google Scholar
Pirastu, M, Fais, R, Messina, M, Bini, V, Spiga, S, Falconieri, D and Diana, M (2006) Impaired decision-making in opiate-dependent subjects: effect of pharmacological therapies. Drug and Alcohol Dependence 83, 163–168.Google Scholar
Prosser, J, Cohen, LJ, Steinfeld, M, Eisenberg, D, London, ED and Galynker, II (2006) Neuropsychological functioning in opiate dependent subjects receiving and following methadone maintenance treatment. Drug and Alcohol Dependence 84, 240–247.Google Scholar
Prosser, J, Eisenberg, D, Davey, E, Steinfeld, M, Cohen, L, London, E and Galynker, I (2008) Character pathology and neuropsychological test performance in remitted opiate dependence. Substance Abuse Treatment, Prevention, and Policy 3, 23.Google Scholar
Rezapour, T, Hatami, J, Farhoudian, A, Sofuoglu, M, Noroozi, A, Daneshmand, R, Samiei, A and Ekhtiari, H (2015) NEuro COgnitive REhabilitation for disease of addiction (NECOREDA) program: from development to trial. Basic and Clinical Neuroscience 6, 291–298.Google Scholar
Richards, M, Jarvis, MJ, Thompson, N and Wadsworth, ME (2003) Cigarette smoking and cognitive decline in midlife: evidence from a prospective birth cohort study. American Journal in Public Health 93, 994–998.Google Scholar
Robbins, TW and Everitt, BJ (2002) Limbic-striatal memory systems and drug addiction. Neurobiology of Learning and Memory 78, 625–636.Google Scholar
Robbins, TW, James, M, Owen, AM, Sahakian, BJ, McInnes, L and Rabbitt, P (1994) Cambridge Neuropsychological Test Automated Battery (CANTAB): a factor analytic study of a large sample of normal elderly volunteers. Dementia (basel, Switzerland) 5, 266–281.Google Scholar
Rounsaville, JB, Jones, C, Novelly, RA and Kleber, A (1982) Neuropsychological functioning in opiate addicts. The Journal of Nervous and Mental Disease 170, 209–216.Google Scholar
Ruiz-Sánchez de León, JM, Pedrero-Pérez, EJ, Rojo-Mota, G, Llanero-Luque, M and Puerta-García, C (2011) A proposal for a protocol of neuropsychological assessment for use in addictions. Revista di Neurologia 53, 483–493.Google Scholar
Sainani, KL (2009) The problem of multiple testing. PM&R 1, 1098–1103.Google Scholar
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E, Hergueta, T, Baker, R and Dunbar, GC (1998) The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry 59, 22–33.Google Scholar
Shmygalev, S, Damm, M, Weckbecker, K, Berghaus, G, Petzke, F and Sabatowski, R (2011) The impact of long-term maintenance treatment with buprenorphine on complex psychomotor and cognitive function. Drug and Alcohol Dependence 117, 190–197.Google Scholar
Soyka, M, Lieb, M, Kagerer, S, Zingg, C, Koller, G, Lehnert, P, Limmer, P, Kuefner, H and Henning-Fast, K (2008) Cognitive functioning during methadone and buprenorphine treatment. Journal of Clinical Psychopharmacology 28, 699–703.Google Scholar
Specka, M, Finkbeiner, T, Lodemann, E, Leifert, K, Kluwig, J and Gastpar, M (2000) Cognitive-motor performance of methadone maintained patients. European Addiction Research 6, 8–19.Google Scholar
Stevens, A, Peschk, I and Schwarz, J (2007) Implicit learning, executive function and hedonic activity in chronic polydrug abusers, currently abstinent polydrug abusers and controls. Addiction 102, 937–946.Google Scholar
Tolomeo, S, Gray, S, Matthews, K, Steele, JD and Baldacchino, A (2016) Multifaceted impairments in impulsivity and brain structural abnormalities in opioid dependence and abstinence. Psychological Medicine 46, 2841–2853.Google Scholar
Tolomeo, S, Matthews, K, Steele, JD and Baldacchino, A (2018) Compulsivity in opioid dependence. Progress in Neuro-Psychopharmacology and Biological Psychiatry 81, 333–339.Google Scholar
Twamley, EW, Palmer, BW, Jeste, PV, Taylor, MJ and Heaton, RK (2006) Transient and executive function working memory in schizophrenia. Schizophrenia Research 87, 185–190.Google Scholar
Wang, GY, Wouldes, TA, Kydd, R, Jensen, M and Russell, B (2014) Neuropsychological performance of methadone-maintained opiate users. Journal of Psychopharmacology 28, 789–799.Google Scholar
Wesson, DR and Ling, W (2003) The clinical opiate withdrawal scale (COWS). Journal of Psychoactive Drugs 35, 253–259.Google Scholar
Westen, D (2006) Implications of research in cognitive neuroscience for psychodynamic psychotherapy. Focus 4, 215–222.Google Scholar
Winer, BJ, Brown, DR and Michels, KM (1991) Statistical Principles in Experimental Design, 3rd Edn. New York: McGraw Hill.Google Scholar
Vassileva, J, Petkova, P, Georgiev, S, Martin, EM, Tersiyski, R, Raycheva, M, Velinov, V and Marinov, P (2007) Impaired decision-making in psychopathic heroin addicts. Drug and Alcohol Dependence 8, 287–289.Google Scholar
Vieweg, VR, Carlyle-Lipps, WF and Fernandez, A (2005) Opioids and methadone equivalents for clinicians. Primary care companion. Journal of Clinical Psychiatry 7, 86–88.Google Scholar
Yan, W-S., Li, Y-H, Xiao, L, Zhua, N, Bechara, A and Sui, N (2014) Working memory and affective decision-making in addiction: A neurocognitive comparison between heroin addicts, pathological gamblers and healthy controls. Drug and Alcohol Dependence 134, 194–200.Google Scholar
Yates, ST (2009) An evaluation of the cognitive functioning of individuals on Methadone Maintenance Treatment and its relation to treatment adherence. A thesis submitted in partial fulfilment of the requirements for the Degree of Doctor of Philosophy in Psychology, University of Waikato, New Zealand.Google Scholar
Yin, LS, Li, ZZ, Pang, LJ, Zhu, CY, Wang, SM, Zhang, L, Tang, WC and Dai, J (2012) Effects of methadone maintenance treatment on working memory in male heroin dependent patients. Zhonghua Yi Xue Za Zhi Journal 92, 464–467.Google Scholar
Zihl, J and von Cramon, D (1979) The contribution of the “second” visual system to directed visual attention in man. Brain 102, 853–856.Google Scholar
Supplementary material: File

Baldacchino et al. supplementary material

Table S1

Download Baldacchino et al. supplementary material(File)
File 15.8 KB