Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-26T06:20:11.629Z Has data issue: false hasContentIssue false

Neural substrates of impulsive decision making modulated by modafinil in alcohol-dependent patients

Published online by Cambridge University Press:  05 March 2014

L. Schmaal*
Affiliation:
Amsterdam Institute for Addiction Research, Department of Psychiatry, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands Department of Psychiatry, VU University Medical Center, Amsterdam, The Netherlands
A. E. Goudriaan
Affiliation:
Amsterdam Institute for Addiction Research, Department of Psychiatry, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands Arkin Mental Health Institute, Amsterdam, The Netherlands
L. Joos
Affiliation:
Collaborative Antwerp Psychiatric Research Institute (CAPRI), Department of Psychiatry, University of Antwerp, Antwerp, Belgium
G. Dom
Affiliation:
Collaborative Antwerp Psychiatric Research Institute (CAPRI), Department of Psychiatry, University of Antwerp, Antwerp, Belgium Psychiatric Center Alexian Brothers, Boechout, Belgium
T. Pattij
Affiliation:
Department of Anatomy and Neurosciences, Neuroscience Campus Amsterdam, VU University Medical Center, Amsterdam, The Netherlands
W. van den Brink
Affiliation:
Amsterdam Institute for Addiction Research, Department of Psychiatry, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
D. J. Veltman
Affiliation:
Department of Psychiatry, VU University Medical Center, Amsterdam, The Netherlands
*
*Address for correspondence: Dr L. Schmaal, Department of Psychiatry, VU University Medical Center, PO Box 74077, 1070 BB Amsterdam, The Netherlands. (Email: lianschmaal@gmail.com)

Abstract

Background

Impulsive decision making is a hallmark of frequently occurring addiction disorders including alcohol dependence (AD). Therefore, ameliorating impulsive decision making is a promising target for the treatment of AD. Previous studies have shown that modafinil enhances cognitive control functions in various psychiatric disorders. However, the effects of modafinil on delay discounting and its underlying neural correlates have not been investigated as yet. The aim of the current study was to investigate the effects of modafinil on neural correlates of impulsive decision making in abstinent AD patients and healthy control (HC) subjects.

Method

A randomized, double-blind, placebo-controlled, within-subjects cross-over study using functional magnetic resonance imaging (fMRI) was conducted in 14 AD patients and 16 HC subjects. All subjects participated in two fMRI sessions in which they either received a single dose of placebo or 200 mg of modafinil 2 h before the session. During fMRI, subjects completed a delay-discounting task to measure impulsive decision making.

Results

Modafinil improved impulsive decision making in AD pateints, which was accompanied by enhanced recruitment of frontoparietal regions and reduced activation of the ventromedial prefrontal cortex. Moreover, modafinil-induced enhancement of functional connectivity between the superior frontal gyrus and ventral striatum was specifically associated with improvement in impulsive decision making.

Conclusions

These findings indicate that modafinil can improve impulsive decision making in AD patients through an enhanced coupling of prefrontal control regions and brain regions coding the subjective value of rewards. Therefore, the current study supports the implementation of modafinil in future clinical trials for AD.

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

Abe, M, Hanakawa, T, Takayama, Y, Kuroki, C, Ogawa, S, Fukuyama, H (2007). Functional coupling of human prefrontal and premotor areas during cognitive manipulation. Journal of Neuroscience 27, 34293438.CrossRefGoogle ScholarPubMed
Anderson, AL, Reid, MS, Li, SH, Holmes, T, Shemanski, L, Slee, A, Smith, EV, Kahn, R, Chiang, N, Vocci, F, Ciraulo, D, Dackis, C, Roache, JD, Salloum, IM, Somoza, E, Urschel, HC 3rd, Elkashef, AM (2009). Modafinil for the treatment of cocaine dependence. Drug and Alcohol Dependence 104, 133139.CrossRefGoogle ScholarPubMed
APA (1994). Diagnostic and Statistical Manual of Mental Disorders, 4th edn. American Psychiatric Press: Washington, DC.Google Scholar
Baarendse, PJ, Vanderschuren, LJ (2012). Dissociable effects of monoamine reuptake inhibitors on distinct forms of impulsive behavior in rats. Psychopharmacology (Berlin) 219, 313326.CrossRefGoogle ScholarPubMed
Babor, TF, Kranzler, HR, Lauerman, RJ (1989). Early detection of harmful alcohol consumption: comparison of clinical, laboratory, and self-report screening procedures. Addictive Behaviors 14, 139157.CrossRefGoogle ScholarPubMed
Bickel, WK, Jones, BA, Landes, RD, Christensen, DR, Jackson, L, Mancino, M (2010). Hypothetical intertemporal choice and real economic behavior: delay discounting predicts voucher redemptions during contingency-management procedures. Experimental and Clinical Psychopharmacology 18, 546552.CrossRefGoogle ScholarPubMed
Bickel, WK, Pitcock, JA, Yi, R, Angtuaco, EJ (2009). Congruence of BOLD response across intertemporal choice conditions: fictive and real money gains and losses. Journal of Neuroscience 29, 88398846.CrossRefGoogle ScholarPubMed
Bjork, JM, Hommer, DW, Grant, SJ, Danube, C (2004). Impulsivity in abstinent alcohol-dependent patients: relation to control subjects and type 1-/type 2-like traits. Alcohol 34, 133150.CrossRefGoogle ScholarPubMed
Bohn, MJ, Krahn, DD, Staehler, BA (1995). Development and initial validation of a measure of drinking urges in abstinent alcoholics. Alcoholism: Clinical and Experimental Research 19, 600606.CrossRefGoogle ScholarPubMed
Brett, M, Anton, J-L, Valabreque, R, Poline, J-B (2002). Region of interest analysis using an SPM toolbox [Abstract]. Presented at the 8th International Conference on Functional Mapping of the Human Brain, 2–6 June 2002, Sendai, Japan. (Available on CD-ROM in NeuroImage, vol. 16, no. 2.).Google Scholar
Broos, N, Diergaarde, L, Schoffelmeer, AN, Pattij, T, De Vries, TJ (2012 a). Trait impulsive choice predicts resistance to extinction and propensity to relapse to cocaine seeking: a bidirectional investigation. Neuropsychopharmacology 37, 13771386.CrossRefGoogle ScholarPubMed
Broos, N, Schmaal, L, Wiskerke, J, Kostelijk, L, Lam, T, Stoop, N, Weierink, L, Ham, J, De Geus, EJC, Schoffelmeer, ANM, Van den Brink, W, Veltman, DJ, De Vries, TJ, Pattij, T, Goudriaan, AE (2012 b). The relationship between impulsive choice and impulsive action: a cross-species translational study. PLOS ONE 7, e37781.CrossRefGoogle Scholar
Buckner, RL, Andrews-Hanna, JR, Schacter, DL (2008). The brain's default network: anatomy, function, and relevance to disease. Annals of the New York Acadamy of Sciences 1124, 138.CrossRefGoogle ScholarPubMed
Calzavara, R, Mailly, P, Haber, SN (2007). Relationship between the corticostriatal terminals from areas 9 and 46, and those from area 8A, dorsal and rostral premotor cortex and area 24c: an anatomical substrate for cognition to action. European Journal of Neuroscience 26, 20052024.CrossRefGoogle ScholarPubMed
Claus, ED, Kiehl, KA, Hutchison, KE (2011). Neural and behavioral mechanisms of impulsive choice in alcohol use disorder. Alcoholism: Clinical and Experimental Research 35, 12091219.CrossRefGoogle ScholarPubMed
Cools, R, Barker, RA, Sahakian, BJ, Robbins, TW (2001). Enhanced or impaired cognitive function in Parkinson's disease as a function of dopaminergic medication and task demands. Cerebral Cortex 11, 11361143.CrossRefGoogle ScholarPubMed
Cools, R, Barker, RA, Sahakian, BJ, Robbins, TW (2003). l-Dopa medication remediates cognitive inflexibility, but increases impulsivity in patients with Parkinson's disease. Neuropsychologia 41, 14311441.CrossRefGoogle ScholarPubMed
Cools, R, D'Esposito, M (2011). Inverted-U-shaped dopamine actions on human working memory and cognitive control. Biological Psychiatry 69, e113e125.CrossRefGoogle ScholarPubMed
Dean, AC, Sevak, RJ, Monterosso, JR, Hellemann, G, Sugar, CA, London, ED (2011). Acute modafinil effects on attention and inhibitory control in methamphetamine-dependent humans. Journal of Studies on Alcohol and Drugs 72, 943953.CrossRefGoogle ScholarPubMed
Diergaarde, L, Pattij, T, Poortvliet, I, Hogenboom, F, De Vries, W, Schoffelmeer, AN, De Vries, TJ (2008). Impulsive choice and impulsive action predict vulnerability to distinct stages of nicotine seeking in rats. Biological Psychiatry 63, 301308.CrossRefGoogle ScholarPubMed
Evenden, JL (1999). Varieties of impulsivity. Psychopharmacology (Berlin) 146, 348361.CrossRefGoogle ScholarPubMed
Ferraro, L, Antonelli, T, O'Connor, WT, Tanganelli, S, Rambert, FA, Fuxe, K (1998). The effects of modafinil on striatal, pallidal and nigral GABA and glutamate release in the conscious rat: evidence for a preferential inhibition of striato-pallidal GABA transmission. Neuroscience Letters 253, 135138.CrossRefGoogle ScholarPubMed
Finke, K, Dodds, CM, Bublak, P, Regenthal, R, Baumann, F, Manly, T, Müller, U (2010). Effects of modafinil and methylphenidate on visual attention capacity: a TVA-based study. Psychopharmacology (Berlin) 210, 317329.CrossRefGoogle ScholarPubMed
Ghahremani, DG, Tabibnia, G, Monterosso, J, Hellemann, G, Poldrack, RA, London, ED (2011). Effect of modafinil on learning and task-related brain activity in methamphetamine-dependent and healthy individuals. Neuropsychopharmacology 36, 950959.CrossRefGoogle ScholarPubMed
Golde, M, von Cramon, DY, Schubotz, RI (2010). Differential role of anterior prefrontal and premotor cortex in the processing of relational information. NeuroImage 49, 28902900.CrossRefGoogle ScholarPubMed
Gossop, M, Keaney, F, Stewart, D, Marshall, EJ, Strang, J (2002). A Short Alcohol Withdrawal Scale (SAWS): development and psychometric properties. Addiction Biology 7, 3743.CrossRefGoogle Scholar
Greely, H, Sahakian, B, Harris, J, Kessler, RC, Gazzaniga, M, Campbell, P, Farah, MJ (2008). Towards responsible use of cognitive-enhancing drugs by the healthy. Nature 456, 702705.CrossRefGoogle ScholarPubMed
Green, L, Myerson, J, Lichtman, D, Rosen, S, Fry, A (1996). Temporal discounting in choice between delayed rewards: the role of age and income. Psychology and Aging 11, 7984.CrossRefGoogle ScholarPubMed
Hanakawa, T, Honda, M, Sawamoto, N, Okada, T, Yonekura, Y, Fukuyama, H, Shibasaki, H (2002). The role of rostral Brodmann area 6 in mental-operation tasks: an integrative neuroimaging approach. Cerebral Cortex 12, 11571170.CrossRefGoogle ScholarPubMed
Hanlon, CA, Wesley, MJ, Stapleton, JR, Laurienti, PJ, Porrino, LJ (2011). The association between frontal-striatal connectivity and sensorimotor control in cocaine users. Drug and Alcohol Dependence 115, 240243.CrossRefGoogle ScholarPubMed
Hart, CL, Haney, M, Vosburg, SK, Rubin, E, Foltin, RW (2008). Smoked cocaine self-administration is decreased by modafinil. Neuropsychopharmacology 33, 761768.CrossRefGoogle ScholarPubMed
Hasin, DS, Stinson, FS, Ogburn, E, Grant, BF (2007). Prevalence, correlates, disability, and comorbidity of DSM-IV alcohol abuse and dependence in the United States: results from the National Epidemiologic Survey on Alcohol and Related Conditions. Archives of General Psychiatry 64, 830842.CrossRefGoogle ScholarPubMed
Hoffman, WF, Schwartz, DL, Huckans, MS, McFarland, BH, Meiri, G, Stevens, AA, Mitchell, SH (2008). Cortical activation during delay discounting in abstinent methamphetamine dependent individuals. Psychopharmacology (Berlin) 201, 183193.CrossRefGoogle ScholarPubMed
Hunter, MD, Ganesan, V, Wilkinson, ID, Spence, SA (2006). Impact of modafinil on prefrontal executive function in schizophrenia. American Journal of Psychiatry 163, 21842186.CrossRefGoogle ScholarPubMed
Joos, L, Docx, L, Schmaal, L, Sabbe, BG, Dom, G (2010). Modafinil in psychiatric disorders: the promising state reconsidered. Tijdschrift voor Psychiatry 52, 763773.Google ScholarPubMed
Kable, JW, Glimcher, PW (2007). The neural correlates of subjective value during intertemporal choice. Nature Neuroscience 10, 16251633.CrossRefGoogle ScholarPubMed
Kable, JW, Glimcher, PW (2010). An “as soon as possible” effect in human intertemporal decision making: behavioral evidence and neural mechanisms. Journal of Neurophysiology 103, 25132531.CrossRefGoogle Scholar
Kalechstein, AD, De La Garza, R, Newton, TF (2010). Modafinil administration improves working memory in methamphetamine-dependent individuals who demonstrate baseline impairment. American Journal of Addiction 19, 340344.CrossRefGoogle ScholarPubMed
Kim, C, Chung, C, Kim, J (2012). Conflict adjustment through domain-specific multiple cognitive control mechanisms. Brain Research 1444, 5564.CrossRefGoogle ScholarPubMed
Kirby, KN, Godoy, R, Reyes-Garcia, V, Byron, E, Apaza, L, Leonard, W, Pérez, E, Vadez, V, Wilkie, D (2002). Correlates of delay-discount rates: evidence from Tsimane’ Amerindians of the Bolivian rain forest. Journal of Economic Psychology 23, 291316.CrossRefGoogle Scholar
Liston, C, Watts, R, Tottenham, N, Davidson, MC, Niogi, S, Ulug, AM, Casey, BJ (2006). Frontostriatal microstructure modulates efficient recruitment of cognitive control. Cerebral Cortex 16, 553560.CrossRefGoogle ScholarPubMed
Luppino, G, Rozzi, S, Calzavara, R, Matelli, M (2003). Prefrontal and agranular cingulate projections to the dorsal premotor areas F2 and F7 in the macaque monkey. European Journal of Neuroscience 17, 559578.CrossRefGoogle Scholar
MacKillop, J, Kahler, CW (2009). Delayed reward discounting predicts treatment response for heavy drinkers receiving smoking cessation treatment. Drug and Alcohol Dependence 104, 197203.CrossRefGoogle ScholarPubMed
Marco-Pallares, J, Mohammadi, B, Samii, A, Munte, TF (2010). Brain activations reflect individual discount rates in intertemporal choice. Brain Research 1320, 123129.CrossRefGoogle ScholarPubMed
McClure, SM, Laibson, DI, Loewenstein, G, Cohen, JD (2004). Separate neural systems value immediate and delayed monetary rewards. Science 306, 503507.CrossRefGoogle ScholarPubMed
McLaren, DG, Ries, ML, Xu, G, Johnson, SC (2012). A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. NeuroImage 61, 12771286.CrossRefGoogle ScholarPubMed
Meade, CS, Lowen, SB, MacLean, RR, Key, MD, Lukas, SE (2011). fMRI brain activation during a delay discounting task in HIV-positive adults with and without cocaine dependence. Psychiatry Research 192, 167175.CrossRefGoogle ScholarPubMed
Mehta, MA, Manes, FF, Magnolfi, G, Sahakian, BJ, Robbins, TW (2004). Impaired set-shifting and dissociable effects on tests of spatial working memory following the dopamine D2 receptor antagonist sulpiride in human volunteers. Psychopharmacology (Berlin) 176, 331342.CrossRefGoogle ScholarPubMed
Mitchell, JM, Fields, HL, D'Esposito, M, Boettiger, CA (2005). Impulsive responding in alcoholics. Alcohol: Clinical and Experimental Research 29, 21582169.CrossRefGoogle ScholarPubMed
Mitchell, JP, Schirmer, J, Ames, DL, Gilbert, DT (2011). Medial prefrontal cortex predicts intertemporal choice. Journal of Cognitive Neuroscience 23, 857866.CrossRefGoogle ScholarPubMed
Monterosso, JR, Ainslie, G, Xu, J, Cordova, X, Domier, CP, London, ED (2007). Frontoparietal cortical activity of methamphetamine-dependent and comparison subjects performing a delay discounting task. Human Brain Mapping 28, 383393.CrossRefGoogle ScholarPubMed
Myerson, J, Green, L, Warusawitharana, M (2001). Area under the curve as a measure of discounting. Journal of the Experimental Analysis of Behavior 76, 235243.CrossRefGoogle ScholarPubMed
Nielsen, FA, Hansen, LK (2002). Automatic anatomical labeling of Talairach coordinates and generation of volumes of interest via the BrainMap database. Presented at the 8th International Conference on Functional Mapping of the Human Brain, 2–6 June 2002, Sendai, Japan. (Available on CD-ROM.).Google Scholar
Petry, NM (2001). Delay discounting of money and alcohol in actively using alcoholics, currently abstinent alcoholics, and controls. Psychopharmacology (Berlin) 154, 243250.CrossRefGoogle ScholarPubMed
Reimers, S, Maylor, EA, Stewart, N, Chater, N (2009). Associations between a one-shot delay discounting measure and age, income, education and real-world impulsive behavior. Personality and Individual Differences 47, 973978.CrossRefGoogle Scholar
Robertson, M, Hellriegel, ET (2003). Clinical pharmacokinetic profile of modafinil. Clinical Pharmacokinetics 42, 123137.CrossRefGoogle ScholarPubMed
Sahakian, B, Morein-Zamir, S (2007). Professor's little helper. Nature 450, 11571159.CrossRefGoogle ScholarPubMed
Schmaal, L, Goudriaan, AE, Joos, L, Krüse, AM, Dom, G, Van den Brink, W, Veltman, DJ (2013 a). Modafinil modulates resting state functional network connectivity and cognitive control in alcohol dependent patients. Biological Psychiatry 73, 789795.CrossRefGoogle ScholarPubMed
Schmaal, L, Joos, L, Koeleman, M, Veltman, DJ, Van den Brink, W, Goudriaan, AE (2013 b). Effects of modafinil on neural correlates of response inhibition in alcohol dependent patients. Biological Psychiatry 73, 211218.CrossRefGoogle ScholarPubMed
Schmand, B, Bakker, D, Saan, R, Louman, J (1991). The Dutch Reading Test for Adults: a measure of premorbid intelligence level. Tijdschrift voor Gerontologie en Geriatrie 22, 1519.Google ScholarPubMed
Shearer, J, Darke, S, Rodgers, C, Sladie, T, van Beek, I, Lewis, J, Brady, D, McKetin, R, Mattick, RP, Wodak, A (2009). A double-blind, placebo-controlled trial of modafinil (200 mg/day) for methamphetamine dependence. Addiction 104, 224233.CrossRefGoogle ScholarPubMed
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E, Hergueta, T, Baker, R, 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 (Suppl. 20), 2233.Google ScholarPubMed
Sobell, LC, Sobell, MB (1992). Timeline followback: a technique for assessing self-reported alcohol consumption. In Measuring Alcohol Consumption: Psychosocial and Biological Methods (ed. Litten, R.Z. and Allen, J., editors), pp. 4172. Humana Press: New York.CrossRefGoogle Scholar
Spence, SA, Green, RD, Wilkinson, ID, Hunter, MD (2005). Modafinil modulates anterior cingulate function in chronic schizophrenia. British Journal of Psychiatry 187, 5561.CrossRefGoogle ScholarPubMed
Sripada, CS, Gonzalez, R, Phan, KL, Liberzon, I (2011). The neural correlates of intertemporal decision-making: contributions of subjective value, stimulus type, and trait impulsivity. Human Brain Mapping 32, 16371648.CrossRefGoogle ScholarPubMed
Stanger, C, Ryan, SR, Fu, H, Landes, RD, Jones, BA, Bickel, WK, Budney, AJ (2011). Delay discounting predicts adolescent substance abuse treatment outcome. Experimental and Clinical Psychopharmacology 20, 205212.CrossRefGoogle ScholarPubMed
Sun, H, Cocker, PJ, Zeeb, FD, Winstanley, CA (2012). Chronic atomoxetine treatment during adolescence decreases impulsive choice, but not impulsive action, in adult rats and alters markers of synaptic plasticity in the orbitofrontal cortex. Psychopharmacology (Berlin) 219, 285301.CrossRefGoogle Scholar
Szpunar, KK, Watson, JM, McDermott, KB (2007). Neural substrates of envisioning the future. Proceedings of the National Academy of Sciences USA 104, 642647.CrossRefGoogle ScholarPubMed
Tachibana, Y, Nambu, A, Hatanaka, N, Miyachi, S, Takada, M (2004). Input–output organization of the rostral part of the dorsal premotor cortex, with special reference to its corticostriatal projection. Neuroscience Research 48, 4557.CrossRefGoogle ScholarPubMed
Takahashi, T, Ohmura, Y, Oono, H, Radford, M (2009). Alcohol use and discounting of delayed and probabilistic gain and loss. Neuroendocrinology Letters 30, 749752.Google ScholarPubMed
Touret, M, Sallanon-Moulin, M, Fages, C, Roudier, V, Didier-Bazes, M, Roussel, B, Tardy, M, Jouvet, M (1994). Effects of modafinil-induced wakefulness on glutamine synthetase regulation in the rat brain. Molecular Brain Research 26, 123128.CrossRefGoogle ScholarPubMed
United Nations Educational Scientific and Cultural Organization (1997). International Standard Classification of Education. UNESCO: Geneva.Google Scholar
Wittmann, M, Leland, DS, Paulus, MP (2007). Time and decision making: differential contribution of the posterior insular cortex and the striatum during a delay discounting task. Experimental Brain Research 179, 643653.CrossRefGoogle ScholarPubMed
Wittmann, M, Lovero, KL, Lane, SD, Paulus, MP (2010). Now or later? Striatum and insula activation to immediate versus delayed rewards. Journal of Neuroscience, Psychology and Economics 3, 1526.CrossRefGoogle ScholarPubMed
Wolf, RC, Sambataro, F, Vasic, N, Schonfeldt-Lecuona, C, Ecker, D, Landwehrmeyer, B (2008). Altered frontostriatal coupling in pre-manifest Huntington's disease: effects of increasing cognitive load. European Journal of Neurology 15, 11801190.CrossRefGoogle ScholarPubMed
Worsley, KJ, Marrett, S, Neelin, P, Vandal, AC, Friston, KJ, Evans, AC (1996). A unified statistical approach for determining significant signals in images of cerebral activation. Human Brain Mapping 4, 5873.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
Zack, M, Poulos, CX (2009). Effects of the atypical stimulant modafinil on a brief gambling episode in pathological gamblers with high vs. low impulsivity. Journal of Psychopharmacology 23, 660671.CrossRefGoogle ScholarPubMed
Zago, L, Pesenti, M, Mellet, E, Crivello, F, Mazoyer, B, Tzourio-Mazoyer, N (2001). Neural correlates of simple and complex mental calculation. NeuroImage 13, 314327.CrossRefGoogle ScholarPubMed
Supplementary material: File

Schmaal Supplementary Material

Supplementary Material

Download Schmaal Supplementary Material(File)
File 578 KB