Top

Published in:

01-10-2016 | Psychiatry and Preclinical Psychiatric Studies - Original Article

Ventral medial prefrontal cortex (vmPFC) as a target of the dorsolateral prefrontal modulation by transcranial direct current stimulation (tDCS) in drug addiction

Authors: Ester Miyuki Nakamura-Palacios, Isabela Bittencourt Coutinho Lopes, Rodolpho Albuquerque Souza, Jaisa Klauss, Edson Kruger Batista, Catarine Lima Conti, Janine Andrade Moscon, Rodrigo Stênio Moll de Souza

Published in: Journal of Neural Transmission | Issue 10/2016

Abstract

Here, we report some electrophysiologic and imaging effects of the transcranial direct current stimulation (tDCS) over the dorsolateral prefrontal cortex (dlPFC) in drug addiction, notably in alcohol and crack-cocaine dependence. The low resolution electromagnetic tomography (LORETA) analysis obtained through event-related potentials (ERPs) under drug-related cues, more specifically in its P3 segment (300–500 ms) in both, alcoholics and crack-cocaine users, showed that the ventral medial prefrontal cortex (vmPFC) was the brain area with the largest change towards increasing activation under drug-related cues in those subjects that kept abstinence during and after the treatment with bilateral tDCS (2 mA, 35 cm², cathodal left and anodal right) over dlPFC, applied repetitively (five daily sessions). In an additional study in crack-cocaine, which showed craving decreases after repetitive bilateral tDCS, we examined data originating from diffusion tensor imaging (DTI), and we found increased DTI parameters in the left connection between vmPFC and nucleus accumbens (NAcc), such as the number of voxels, fractional anisotropy (FA) and apparent diffusion coefficient (ADC), in tDCS-treated crack-cocaine users when compared to the sham-tDCS group. This increasing of DTI parameters was significantly correlated with craving decreasing after the repetitive tDCS. The vmPFC relates to the control of drug seeking, possibly by extinguishing this behavior. In our studies, the bilateral dlPFC tDCS reduced relapses and craving to the drug use, and increased the vmPFC activation under drug cues, which may be of a great importance in the control of drug use in drug addiction.

Anderer P, Saletu B, Pascual-Marqui RD (2000) Effect of the 5-HT(1A) partial agonist buspirone on regional brain electrical activity in man: a functional neuroimaging study using low-resolution electromagnetic tomography (LORETA). Psychiatry Res 100(2):81–96PubMedCrossRef

Assanangkornchai S, Srisurapanont M (2007) The treatment of alcohol dependence. Curr opin psychiatry 20(3):222–227. doi:10.1097/YCO.0b013e3280fa837d PubMedCrossRef

Batista EK, Klauss J, Fregni F, Nitsche MA, Nakamura-Palacios EM (2015) A randomized placebo-controlled trial of targeted prefrontal cortex modulation with bilateral tDCS in patients with crack-cocaine dependence. Int J Neuropsychopharmacol. doi:10.1093/ijnp/pyv066 PubMedPubMedCentral

Berman SM, Whipple SC, Fitch RJ, Noble EP (1993) P3 in young boys as a predictor of adolescent substance use. Alcohol 10(1):69–76PubMedCrossRef

Boggio PS, Zaghi S, Villani AB, Fecteau S, Pascual-Leone A, Fregni F (2010) Modulation of risk-taking in marijuana users by transcranial direct current stimulation (tDCS) of the dorsolateral prefrontal cortex (DLPFC). Drug Alcohol Depend 112(3):220–225. doi:10.1016/j.drugalcdep.2010.06.019 PubMedCrossRef

Bonson KR, Grant SJ, Contoreggi CS, Links JM, Metcalfe J, Weyl HL, Kurian V, Ernst M, London ED (2002) Neural systems and cue-induced cocaine craving. Neuropsychopharmacology 26(3):376–386. doi:10.1016/S0893-133X(01)00371-2 PubMedCrossRef

Brunoni AR, Amadera J, Berbel B, Volz MS, Rizzerio BG, Fregni F (2011a) A systematic review on reporting and assessment of adverse effects associated with transcranial direct current stimulation. Int J Neuropsychopharmacol 14(8):1133–1145. doi:10.1017/S1461145710001690 PubMedCrossRef

Brunoni AR, Valiengo L, Baccaro A, Zanao TA, de Oliveira JF, Vieira GP, Bueno VF, Goulart AC, Boggio PS, Lotufo PA, Bensenor IM, Fregni F (2011b) Sertraline vs. electrical current therapy for treating depression clinical trial–SELECT TDCS: design, rationale and objectives. Contemp Clin Trials 32(1):90–98. doi:10.1016/j.cct.2010.09.007 PubMedCrossRef

Brunoni AR, Nitsche MA, Bolognini N, Bikson M, Wagner T, Merabet L, Edwards DJ, Valero-Cabre A, Rotenberg A, Pascual-Leone A, Ferrucci R, Priori A, Boggio PS, Fregni F (2012) Clinical research with transcranial direct current stimulation (tDCS): challenges and future directions. Brain Stimul 5(3):175–195. doi:10.1016/j.brs.2011.03.002 PubMedCrossRef

Brunoni AR, Schestatsky P, Lotufo PA, Bensenor IM, Fregni F (2014) Comparison of blinding effectiveness between sham tDCS and placebo sertraline in a 6-week major depression randomized clinical trial. Clin Neurophysiol 125(2):298–305. doi:10.1016/j.clinph.2013.07.020 PubMedCrossRef

Bzdok D, Langner R, Schilbach L, Engemann DA, Laird AR, Fox PT, Eickhoff SB (2013) Segregation of the human medial prefrontal cortex in social cognition. Front Hum Neurosci 7:232. doi:10.3389/fnhum.2013.00232 PubMedPubMedCentralCrossRef

Ciesielski KT, Madden JS, Bligh JG, Schopflocher D (1985) Long-term brain impairment in chronic alcoholics: N2-P3 cognitive potentials in a template-matching memory task. Alcohol Alcohol 20(4):403–408PubMed

Constantino JN, Todd RD (2003) Autistic traits in the general population: a twin study. Arch Gen Psychiatry 60(5):524–530. doi:10.1001/archpsyc.60.5.524 PubMedCrossRef

Conti CL, Nakamura-Palacios EM (2014) Bilateral transcranial direct current stimulation over dorsolateral prefrontal cortex changes the drug-cued reactivity in the anterior cingulate cortex of crack-cocaine addicts. Brain Stimul 7(1):130–132. doi:10.1016/j.brs.2013.09.007 PubMedCrossRef

Conti CL, Moscon JA, Fregni F, Nitsche MA, Nakamura-Palacios EM (2014) Cognitive related electrophysiological changes induced by non-invasive cortical electrical stimulation in crack-cocaine addiction. Int J Neuropsychopharmacol 17(9):1465–1475. doi:10.1017/S1461145714000522 PubMedCrossRef

da Silva MC, Conti CL, Klauss J, Alves LG, do Nascimento Cavalcante HM, Fregni F, Nitsche MA, Nakamura-Palacios EM (2013) Behavioral effects of transcranial direct current stimulation (tDCS) induced dorsolateral prefrontal cortex plasticity in alcohol dependence. J Physiol Paris 107(6):493–502. doi:10.1016/j.jphysparis.2013.07.003 PubMedCrossRef

Faber M, Vanneste S, Fregni F, De Ridder D (2012) Top down prefrontal affective modulation of tinnitus with multiple sessions of tDCS of dorsolateral prefrontal cortex. Brain Stimul 5(4):492–498. doi:10.1016/j.brs.2011.09.003 PubMedCrossRef

Feigl GC, Hiergeist W, Fellner C, Schebesch KM, Doenitz C, Finkenzeller T, Brawanski A, Schlaier J (2014) Magnetic resonance imaging diffusion tensor tractography: evaluation of anatomic accuracy of different fiber tracking software packages. World Neurosurg 81(1):144–150. doi:10.1016/j.wneu.2013.01.004 PubMedCrossRef

Fein G, Di Sclafani V, Meyerhoff DJ (2002) Prefrontal cortical volume reduction associated with frontal cortex function deficit in 6-week abstinent crack-cocaine dependent men. Drug Alcohol Depend 68(1):87–93PubMedPubMedCentralCrossRef

Fregni F, Liguori P, Fecteau S, Nitsche MA, Pascual-Leone A, Boggio PS (2008a) Cortical stimulation of the prefrontal cortex with transcranial direct current stimulation reduces cue-provoked smoking craving: a randomized, sham-controlled study. J Clin Psychiatry 69(1):32–40PubMedCrossRef

Fregni F, Orsati F, Pedrosa W, Fecteau S, Tome FA, Nitsche MA, Mecca T, Macedo EC, Pascual-Leone A, Boggio PS (2008b) Transcranial direct current stimulation of the prefrontal cortex modulates the desire for specific foods. Appetite 51(1):34–41. doi:10.1016/j.appet.2007.09.016 PubMedCrossRef

George O, Koob GF (2013) Control of craving by the prefrontal cortex. Proc Natl Acad Sci USA 110(11):4165–4166. doi:10.1073/pnas.1301245110 PubMedPubMedCentralCrossRef

Ghazizadeh A, Ambroggi F, Odean N, Fields HL (2012) Prefrontal cortex mediates extinction of responding by two distinct neural mechanisms in accumbens shell. J Neurosci 32(2):726–737. doi:10.1523/JNEUROSCI.3891-11.2012 PubMedCrossRef

Goldstein RZ, Volkow ND (2002) Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. Am J Psychiatry 159(10):1642–1652PubMedPubMedCentralCrossRef

Goldstein RZ, Volkow ND (2011) Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci 12(11):652–669. doi:10.1038/nrn3119 PubMedPubMedCentralCrossRef

Hare TA, Hakimi S, Rangel A (2014) Activity in dlPFC and its effective connectivity to vmPFC are associated with temporal discounting. Front Neurosci 8:50. doi:10.3389/fnins.2014.00050 PubMedPubMedCentralCrossRef

Hess CW (2013) Modulation of cortical-subcortical networks in Parkinson’s disease by applied field effects. Front Hum Neurosci 7:565. doi:10.3389/fnhum.2013.00565 PubMedPubMedCentralCrossRef

Hyman SE, Malenka RC, Nestler EJ (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29:565–598. doi:10.1146/annurev.neuro.29.051605.113009 PubMedCrossRef

Jansen JM, Daams JG, Koeter MW, Veltman DJ, van den Brink W, Goudriaan AE (2013) Effects of non-invasive neurostimulation on craving: a meta-analysis. Neurosci Biobehav Rev 37(10 Pt 2):2472–2480. doi:10.1016/j.neubiorev.2013.07.009 PubMedCrossRef

Klauss J, Penido Pinheiro LC, Silva Merlo BL, de Almeida Correia Santos G, Fregni F, Nitsche MA, Miyuki Nakamura-Palacios E (2014) A randomized controlled trial of targeted prefrontal cortex modulation with tDCS in patients with alcohol dependence. Int J Neuropsychopharmacol 17(11):1793–1803. doi:10.1017/S1461145714000984 PubMedCrossRef

Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35(1):217–238. doi:10.1038/npp.2009.110 PubMedCrossRef

LaRowe SD, Saladin ME, Carpenter MJ, Upadhyaya HP (2007) Reactivity to nicotine cues over repeated cue reactivity sessions. Addict Behav 32(12):2888–2899. doi:10.1016/j.addbeh.2007.04.025 PubMedPubMedCentralCrossRef

Manuel AL, David AW, Bikson M, Schnider A (2014) Frontal tDCS modulates orbitofrontal reality filtering. Neuroscience 265:21–27. doi:10.1016/j.neuroscience.2014.01.052 PubMedCrossRef

McKay JR, Foltz C, Stephens RC, Leahy PJ, Crowley EM, Kissin W (2005) Predictors of alcohol and crack cocaine use outcomes over a 3-year follow-up in treatment seekers. J Subst Abuse Treat 28(Suppl 1):S73–S82. doi:10.1016/j.jsat.2004.10.010 PubMedCrossRef

Millan EZ, Marchant NJ, McNally GP (2011) Extinction of drug seeking. Behav Brain Res 217(2):454–462. doi:10.1016/j.bbr.2010.10.037 PubMedCrossRef

Miller PM, Book SW, Stewart SH (2011) Medical treatment of alcohol dependence: a systematic review. Int J Psychiatry Med 42(3):227–266PubMedPubMedCentralCrossRef

Monte-Silva K, Kuo MF, Hessenthaler S, Fresnoza S, Liebetanz D, Paulus W, Nitsche MA (2013) Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain Stimul 6(3):424–432. doi:10.1016/j.brs.2012.04.011 PubMedCrossRef

Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45(2):265–269PubMedCrossRef

Moselhy HF, Georgiou G, Kahn A (2001) Frontal lobe changes in alcoholism: a review of the literature. Alcohol Alcohol 36(5):357–368PubMedCrossRef

Nakamura Palacios EM (2011) Working memory and prefrontal cortex and their relation with the brain reward system and drug addiction. In: Levin ES (ed) Working memory: capacity, developments and improvement techniques. Nova Science Publishers, New York

Nakamura-Palacios EM (2011) Working memory and prefrontal cortex and their relation with the brain reward system and drug addiction. In: Levin ES (ed) Working memory: capacity, developments and improvement techniques. Neuroscience research progress. Nova Science Publisher, New York

Nakamura-Palacios EM, de Almeida Benevides MC, da Penha Zago-Gomes M, de Oliveira RW, de Vasconcellos VF, de Castro LN, da Silva MC, Ramos PA, Fregni F (2012) Auditory event-related potentials (P3) and cognitive changes induced by frontal direct current stimulation in alcoholics according to Lesch alcoholism typology. Int J Neuropsychopharmacol 15(5):601–616. doi:10.1017/S1461145711001040 PubMedCrossRef

Nakamura-Palacios EM, Souza RS, Zago-Gomes MP, de Melo AM, Braga FS, Kubo TT, Gasparetto EL (2014) Gray matter volume in left rostral middle frontal and left cerebellar cortices predicts frontal executive performance in alcoholic subjects. Alcohol Clin Exp Res 38(4):1126–1133. doi:10.1111/acer.12308 PubMedCrossRef

Nestler EJ (2004) Molecular mechanisms of drug addiction. Neuropharmacology 47(Suppl 1):24–32. doi:10.1016/j.neuropharm.2004.06.031 PubMedCrossRef

Nitsche MA, Boggio PS, Fregni F, Pascual-Leone A (2009) Treatment of depression with transcranial direct current stimulation (tDCS): a review. Exp Neurol 219(1):14–19. doi:10.1016/j.expneurol.2009.03.038 PubMedCrossRef

Park SQ, Kahnt T, Beck A, Cohen MX, Dolan RJ, Wrase J, Heinz A (2010) Prefrontal cortex fails to learn from reward prediction errors in alcohol dependence. J Neurosci 30(22):7749–7753. doi:10.1523/JNEUROSCI.5587-09.2010 PubMedPubMedCentralCrossRef

Pascual-Marqui RD, Lehmann D, Koenig T, Kochi K, Merlo MC, Hell D, Koukkou M (1999) Low resolution brain electromagnetic tomography (LORETA) functional imaging in acute, neuroleptic-naive, first-episode, productive schizophrenia. Psychiatry Res 90(3):169–179PubMedCrossRef

Pascual-Marqui RD, Esslen M, Kochi K, Lehmann D (2002) Functional imaging with low-resolution brain electromagnetic tomography (LORETA): a review. Methods Find Exp Clin Pharmacol 24:91–95PubMed

Peters J, LaLumiere RT, Kalivas PW (2008) Infralimbic prefrontal cortex is responsible for inhibiting cocaine seeking in extinguished rats. J Neurosci 28(23):6046–6053. doi:10.1523/JNEUROSCI.1045-08.2008 PubMedPubMedCentralCrossRef

Peters J, Kalivas PW, Quirk GJ (2009) Extinction circuits for fear and addiction overlap in prefrontal cortex. Learn Mem 16(5):279–288. doi:10.1101/lm.1041309 PubMedPubMedCentralCrossRef

Potenza MN (2008) Review. The neurobiology of pathological gambling and drug addiction: an overview and new findings. Philos Trans R Soc Lond B Biol Sci 363(1507):3181–3189. doi:10.1098/rstb.2008.0100 PubMedPubMedCentralCrossRef

Prisciandaro JJ, McRae-Clark AL, Myrick H, Henderson S, Brady KT (2014) Brain activation to cocaine cues and motivation/treatment status. Addict Biol 19(2):240–249. doi:10.1111/j.1369-1600.2012.00446.x PubMedCrossRef

Rahman A, Reato D, Arlotti M, Gasca F, Datta A, Parra LC, Bikson M (2013) Cellular effects of acute direct current stimulation: somatic and synaptic terminal effects. J Physiol 591(Pt 10):2563–2578. doi:10.1113/jphysiol.2012.247171 PubMedPubMedCentralCrossRef

Rudorf S, Hare TA (2014) Interactions between dorsolateral and ventromedial prefrontal cortex underlie context-dependent stimulus valuation in goal-directed choice. J Neurosci 34(48):15988–15996. doi:10.1523/JNEUROSCI.3192-14.2014 PubMedCrossRef

Seo D, Lacadie CM, Tuit K, Hong KI, Constable RT, Sinha R (2013) Disrupted ventromedial prefrontal function, alcohol craving, and subsequent relapse risk. JAMA Psychiatry 70(7):727–739. doi:10.1001/jamapsychiatry.2013.762 PubMedPubMedCentralCrossRef

Siegal HA, Li L, Rapp RC (2002) Abstinence trajectories among treated crack cocaine users. Addict Behav 27(3):437–449PubMedCrossRef

Sullivan EV, Deshmukh A, Desmond JE, Lim KO, Pfefferbaum A (2000) Cerebellar volume decline in normal aging, alcoholism, and Korsakoff’s syndrome: relation to ataxia. Neuropsychology 14(3):341–352PubMedCrossRef

Sullivan EV, Harding AJ, Pentney R, Dlugos C, Martin PR, Parks MH, Desmond JE, Chen SH, Pryor MR, De Rosa E, Pfefferbaum A (2003) Disruption of frontocerebellar circuitry and function in alcoholism. Alcohol Clin Exp Res 27(2):301–309. doi:10.1097/01.ALC.0000052584.05305.98 PubMedCrossRef

Suresh S, Porjesz B, Chorlian DB, Choi K, Jones KA, Wang K, Stimus A, Begleiter H (2003) Auditory P3 in female alcoholics. Alcohol Clin Exp Res 27(7):1064–1074. doi:10.1097/01.ALC.0000075549.49800.A0 PubMedCrossRef

Tanaka T, Takano Y, Tanaka S, Hironaka N, Kobayashi K, Hanakawa T, Watanabe K, Honda M (2013) Transcranial direct-current stimulation increases extracellular dopamine levels in the rat striatum. Front Syst Neurosci 7:6. doi:10.3389/fnsys.2013.00006 PubMedPubMedCentralCrossRef

Tzschentke TM (2000) The medial prefrontal cortex as a part of the brain reward system. Amino Acids 19(1):211–219PubMedCrossRef

Tzschentke TM (2001) Pharmacology and behavioral pharmacology of the mesocortical dopamine system. Prog Neurobiol 63(3):241–320PubMedCrossRef

Van den Oever MC, Spijker S, Smit AB, De Vries TJ (2010) Prefrontal cortex plasticity mechanisms in drug seeking and relapse. Neurosci Biobehav Rev 35(2):276–284. doi:10.1016/j.neubiorev.2009.11.016 PubMedCrossRef

Verdejo-Garcia A, Bechara A (2009) A somatic marker theory of addiction. Neuropharmacology 56(Suppl 1):48–62. doi:10.1016/j.neuropharm.2008.07.035 PubMedCrossRef

Volkow ND, Wang GJ, Telang F, Fowler JS, Logan J, Jayne M, Ma Y, Pradhan K, Wong C (2007) Profound decreases in dopamine release in striatum in detoxified alcoholics: possible orbitofrontal involvement. J Neurosci 27(46):12700–12706. doi:10.1523/JNEUROSCI.3371-07.2007 PubMedCrossRef

Volkow ND, Tomasi D, Wang GJ, Fowler JS, Telang F, Goldstein RZ, Alia-Klein N, Wong C (2011a) Reduced metabolism in brain “control networks” following cocaine-cues exposure in female cocaine abusers. PLoS One 6(2):e16573. doi:10.1371/journal.pone.0016573 PubMedPubMedCentralCrossRef

Volkow ND, Wang GJ, Fowler JS, Tomasi D, Telang F (2011b) Addiction: beyond dopamine reward circuitry. Proc Natl Acad Sci USA 108(37):15037–15042. doi:10.1073/pnas.1010654108 PubMedPubMedCentralCrossRef

Wagner T, Fregni F, Fecteau S, Grodzinsky A, Zahn M, Pascual-Leone A (2007) Transcranial direct current stimulation: a computer-based human model study. Neuroimage 35(3):1113–1124. doi:10.1016/j.neuroimage.2007.01.027 PubMedCrossRef

Weiss F (2005) Neurobiology of craving, conditioned reward and relapse. Curr Opin Pharmacol 5(1):9–19. doi:10.1016/j.coph.2004.11.001 PubMedCrossRef

Worrell GA, Lagerlund TD, Sharbrough FW, Brinkmann BH, Busacker NE, Cicora KM, O’Brien TJ (2000) Localization of the epileptic focus by low-resolution electromagnetic tomography in patients with a lesion demonstrated by MRI. Brain Topogr 12(4):273–282PubMedCrossRef

Zago-Gomes Mda P, Nakamura-Palacios EM (2009) Cognitive components of frontal lobe function in alcoholics classified according to Lesch’s typology. Alcohol Alcohol 44(5):449–457. doi:10.1093/alcalc/agp043 PubMedCrossRef

Title: Ventral medial prefrontal cortex (vmPFC) as a target of the dorsolateral prefrontal modulation by transcranial direct current stimulation (tDCS) in drug addiction
Authors: Ester Miyuki Nakamura-Palacios
Isabela Bittencourt Coutinho Lopes
Rodolpho Albuquerque Souza
Jaisa Klauss
Edson Kruger Batista
Catarine Lima Conti
Janine Andrade Moscon
Rodrigo Stênio Moll de Souza
Publication date: 01-10-2016
Publisher: Springer Vienna
Published in: Journal of Neural Transmission / Issue 10/2016
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI: https://doi.org/10.1007/s00702-016-1559-9

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Ventral medial prefrontal cortex (vmPFC) as a target of the dorsolateral prefrontal modulation by transcranial direct current stimulation (tDCS) in drug addiction

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 10/2016

Impaired synaptic plasticity in RASopathies: a mini-review

A proof-of-concept study on the combination of repetitive transcranial magnetic stimulation and relaxation techniques in chronic tinnitus

Effects of theta-rhythm transcranial alternating current stimulation (4.5 Hz-tACS) in patients with clozapine-resistant negative symptoms of schizophrenia: a case series

Transcranial direct current stimulation of the prefrontal cortex increases attention to visual target stimuli

Transcranial direct current stimulation in children and adolescents: a comprehensive review

Preliminary investigation of the effects of γ-tACS on working memory in schizophrenia