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Transcranial direct current stimulation tDCS has been shown to modulate subjective craving ratings in drug dependents by modification of cortical excitability in dorsolateral prefrontal cortex DLPFC. Given the mechanism of craving in methamphetamine meth users, we aimed to test whether tDCS of DLPFC could also alter self-reported craving in abstinent meth users while being exposed to meth cues. In this double-blinded, crossover, sham-controlled study, thirty two right-handed abstinent male meth users were recruited. Our findings showed a state dependent effect of tDCS: while active prefrontal tDCS acutely reduced craving at rest in the abstinent meth users, it increased craving during meth-related cue exposure. These findings reflect the important role of the prefrontal cortex in both cue saliency evaluation and urge to meth consumption. According to the world drug report, after cannabis, amphetamine-type stimulants ATS are the world's most widely used drugs. ATS has become an international public health problem with an estimation of Methamphetamine meth is an extremely potent psycho-stimulant and highly addictive drug, accompanied by cheap price, ease of synthesis and long lasting effects Henry et al. Relapse to drug use is a common phenomenon in the treatment of addiction that can occur after prolonged abstinence, and is often precipitated by the exposure to drug-associated cues that provoke drug craving Pickens et al. Drug craving is one of the most important factors in addiction that can lead to drug-seeking behaviour during abstinence. It represents a complex condition that includes emotional and cognitive aspects along with behavioural and physiological states. Emerging evidence suggests that craving induced by meth cues can be reliably measured in meth-dependent individuals and cue-induced craving is a strong predictor of subsequent meth use Culbertson et al. Accordingly, cue-elicited meth craving should be viewed as a clinically important phenomenon and one of the primary behavioural symptoms of meth dependence. According to several neuroimaging studies, the prefrontal cortex, especially the dorsolateral prefrontal cortex DLPFC , plays an important role in drug craving Brody et al. Additionally, modulation of DLPFC activity using repetitive transcranial magnetic stimulation rTMS , which is a non-invasive brain stimulation technique, has shown significant effects on nicotine Eichhammer et al. Hence, we aimed to test the effects of prefrontal cortex modulation using a technique that has been shown to induce significant behavioural effects and can interact with current neural processes to enhance neuroplasticity — transcranial direct current stimulation tDCS. TDCS is a method of non-invasive brain stimulation which has recently demonstrated promising neuro-rehabilitative effects in different types of neuropsychiatric disorders Demirtas-Tatlidede et al. TDCS delivers a weak and continuous current to the cortex through an electrode connection with the subject's scalp, and either inhibits or enhances neuronal firing in an area related to the location of the electrode. The interesting advantage of tDCS is its interactive effect with the ongoing neural process; thus it is an attractive technique to be used in combination with behavioural stimulation. A main drawback of these studies is the possible confounding effect of bilateral protocols, in the sense that excitatory effects of the anodal electrode are not distinguishable from inhibitory effects of the cathodal electrode. We therefore assessed the effects of unilateral stimulation of the right DLPFC on the immediate and cue-induced craving in abstinent meth-dependent subjects. We used a cue reactivity paradigm, which has been demonstrated to be a validated method for craving induction and thus, given the mechanism of tDCS, appropriate to be combined with tDCS of the prefrontal cortex. We chose the right DLPFC as we hypothesized that increasing ongoing activity of this area, would have an inhibitory effect on craving behaviour. Subjects were recruited from meth-dependent patients who were admitted to Vardij Abstinence-Based Residential Centre which is specialized for ATS dependence. This centre is located at Vardij, a rural area near Tehran, and is a part of the therapeutic network belonging to Rebirth Society Organization RSO , a non-profit charity. The setting was ideal for this study as the population was relatively homogeneous and given the large numbers of meth users in this facility, it also provided an adequate external validity. Thirty two right-handed male subjects were initially enrolled, although only 30 completed the whole procedure of the study. All the subjects had used meth at least 6 d a week in the last month before entering the treatment and the most common route of administration was smoking among all subjects. Subjects were excluded if their self-reported mean craving was below 20 out of We also excluded individuals with any current or past major clinical neurologic disorders, central nervous system-effective medication intake, history of epilepsy, brain surgery, tumor, intracranial metal implantation, clinically significant head trauma, or any major clinical psychiatric disorders in axis I, except substance-related disorders. The experimental protocol was designed and carried out according to the Declaration of Helsinki principle. Since exposing patients to meth cues may increase the possibility of relapse, similarly to studies using cue-reactivity paradigms, we carefully addressed this important ethical concern by using images instead of real substance and paraphernalia and subjects received IEC-approved psychological interventions to manage potential drug craving after being exposed to drug cues. As the subjects were already admitted to a caring facility they were closely monitored through the following week for any sign of relapse. All subjects signed a written informed consent form. This study was a randomized, double-blinded, sham-controlled, crossover study. Participants and the evaluating investigators except the technician that applied tDCS were blinded to the intervention type. The procedure consisted of three separate sessions, a recruitment session followed by two intervention sessions. At the beginning of the recruitment session, all aspects of the experiment were explained completely to each individual, and then, in the case of full consent for participation, each individual was asked to sign the consent form. Basic demographic information, drug abuse and treatment history, and high risk behaviours of each subject were recorded during a structured interview by an expert drug counsellor. The next two intervention sessions consisted of an active and a sham stimulation session, the sequence of which was randomly chosen. All subjects were asked to abstain for cigarettes 1 h prior to intervention sessions to control for potential nicotine effect. At the beginning of the sessions, the subject was seated on a comfortable chair and was asked to complete the Persian version of Positive and Negative Affect Scale PANAS in order to control for his affective status before each session. Eventually, we assessed any possible side effects using a tDCS side-effect checklist at the end of the intervention sessions Fig. Intervention procedure. In both interventional sessions, the exact same procedure was followed, except for the type of the stimulation and task version. The sequence of stimulation and task type was randomized with permuted-block method. The same investigators carried out stimulation sessions, at the same time of the day and the same room. Duration of each trial was 24 s in which a visual cue an image accompanied by a computerized Visual Analog Scale cVAS were shown in a fixed and predefined order on the screen of a 14 in laptop and the subject was asked to rate his cue-induced craving on a scale of 0 to The total duration of the task was exactly 10 min, which contained twenty drug-related and five neutral cues Fig. Every subject completed five blocks of current task containing different stimuli from each cue group with the same sequence of the cues in each block. The task was completed in 10 min during which the craving elicited by each stimulus was rated 0— by the subject using a cVAS located under each image. This task was carried out in two equivalent versions with two different sets of images, CICT1 and CICT2 to avoid memory interference and training effects. Two versions were performed randomly for each subject during two intervention sessions, meaning that if CICT1 had been used in the first session, then CICT2 would be used in the second one and vice versa. The two series of images were counterbalanced for two equivalent versions based on their mean craving induction power, which was assessed in a previous study by Ekhtiari et al. Electrodes were standard carbonic, covered with a normal saline soaked sponge cases. Subjects were randomized to receive sham or anodal tDCS. During anodal tDCS, a 2 mA current was applied for 20 min. For the sham stimulation, the same montage was used, but the stimulator was turned off after gradually ramping up to 2 mA and down to 0 mA which took 1 min. The electrodes were on the scalp for the remaining 19 min and subjects were not informed that the device was turned off. Wash-out period between two sessions of intervention was at least 72 h to avoid any potential carry-over effects. Statistical analysis was performed by R v. Multiple comparison error was corrected by the Bonferroni method. Pearson's correlation coefficient was computed to test for bivariate correlation among potential confounder variables such as age, duration of abstinence, duration of addiction and marital status and explanatory variables. A total of 32 subjects initially entered the study, but two of them withdrew from the study. As this was a cross-over study, statistical analysis was performed on 30 subjects. Demographic and drug-related variables are summarized in Table 1. Baseline variables of age, duration of meth abstinence, duration of meth dependence, and marital status had no significant correlation with tDCS effect on craving. Also the results showed a marginal interaction effect of time and tDCS condition. Percent change in craving for real and sham tDCS are shown in Fig. A comparison between mean self-reported CICT score of each participant in sham vs. For further investigation paired t -test was used to compare variation of induced craving among four groups of stimuli which were presented in both sham and active conditions. Results showed that the drug cues and associated cues induced highest and lowest craving, respectively. Detailed results are presented in Table 2. It appears that some stimuli induced more craving than others; therefore pictures with a median rating of over 30 were grouped as more provocative. As illustrated in Fig. Induced craving ratings for real and sham tDCS with more provocative stimuli. All participants tolerated tDCS without any major complications. According to Fisher's exact test, other side effects including headache, vertigo, drowsiness, dizziness and nausea, were not significantly different between two conditions. The most common side effects were drowsiness, itching and tingling. All side effects were temporary and mostly from mild to moderate in intensity. The purpose of this study was to investigate the effects of anodal stimulation of right DLPFC on the immediate and online cue-induced meth craving. The results showed a clear state dependent effect of tDCS: while active tDCS in comparison with sham stimulation led to a larger decrease of self-reported craving at rest, active stimulation of the right DLPFC compared to sham stimulation induced larger craving ratings during cue exposure. The first important finding to discuss is the decrease of craving at rest after 10 min of anodal stimulation on the right DLPFC of abstinent subjects. This change was observed before exposure to meth-related cues. This result is therefore consistent with previous findings from studies using tDCS to modulate other types of craving. Fregni et al. Furthermore Boggio et al. Finally, this effect was also found for marijuana craving. Boggio et al. Although effects on craving are similar across these studies, mechanisms may not be necessarily the same, as these studies used some variations in the assessments and parameters of stimulation. In spite of no direct measurement of neurophysiological parameters such as cortical excitability, these tDCS studies had targeted the DLPFC area as a common location for stimulation. Furthermore, drug-dependent individuals exhibit lower resting and metabolic activity in the prefrontal cortex Botelho et al. The DLPFC integrates cognitive and motivationally relevant information about decision making, reward, motivation, and internal state and uses this information to regulate drug seeking and drug avoiding behaviours Goldstein and Volkow, ; Bechara, ; McBride et al. According to these findings, and considering mechanisms of anodal tDCS in facilitating spontaneous neuronal activity and reinforcing local plasticity, we conjecture that anodal stimulation enhances DLPFC activity, which may inhibit drug seeking behaviour. The second important finding of our study was the small increase in craving ratings during cue exposure under anodal stimulation compared to sham. To date, few studies have investigated effects of online tDCS on induced craving. In fact, our results are inconsistent with the previous study conducted by Goldman et al. The increased cue-induced craving observed in our study could be due to an increase in the effective processing of drug cue saliency through enhancement of sustained attention under anodal stimulation of DLPFC. Nelson et al. Here, one provocative speculation is that enhancing the processing of a drug-related cue without the reward associated with the drug may in fact decrease the conditioning effect of the drug and result in a late decrease in relapse. Such a hypothesis needs to be tested in future studies. Although we have shown that 10 min of anodal tDCS stimulation on the right DLPFC can acutely reduce the immediate meth craving, the results of this study do not imply necessarily that this type of stimulation can lead to clinical applications for meth abstinence. It should be noted that this reduced craving might be transient. Although it is possible that repeated stimulation could enhance and prolong the effect of tDCS on clinical applications, as shown previously Boggio et al. As there is no clinically approved pharmacologic intervention to reduce meth craving and abstinence, further clinical trials with daily repeated tDCS sessions should be explored. Furthermore, our study was focused on abstinent and treatment-seeking patients, who have different patterns of brain activity from active drug users who do not seek treatment. Therefore single session tDCS studies could target non-treatment seekers, gender effects and other cognitive processing involved in continued drug use, including lack of insight, attentional bias towards drug cues and impaired motor control or even craving self-reports with other possible electrode montages over PFC. Our findings showed that active prefrontal tDCS reduces craving at rest in the abstinent meth users while it may increase craving during cue exposure. This may reflect the role of the prefrontal cortex in both cue saliency evaluation and top-down craving modulation. These results offer preliminary promising data to support further studies investigating tDCS as a clinical application for craving control among meth-dependent subjects. The authors are grateful to the participants for committing the time to this study. Bechara A Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective. Nat Neurosci 8 : — Google Scholar. Drug Alcohol Depend 92 : 55 — Neurosci Lett : 82 — Drug Alcohol Depend : — Neuropsychol Rehabil 21 : — Brain Stimul 5 : — Ann N Y Acad Sci : — Arch Gen Psychiatry 59 : — Biol Psychiatry 62 : — Am J Psychiatry : — Drug Alcohol Depend 86 : 91 — Pharmacol Biochem Behav 96 : — Neuropharmacol 64 : — J Clin Psychiatry 64 : — Ekhtiari H Alam-Mehrjerdi Z George S Mokri A Designing and evaluation of reliability and validity of visual cue-induced craving assessment task for methamphetamine smokers. Basic Clin Neurosci 1 : 33 — Pain : — J Clin Psychiatry 69 : 32 — Garavan H Cue-induced cocaine craving: neuroanatomical specificity for drug users and drug stimuli. Arch Gen Psychiatry 58 : — Appetite 56 : — Goldstein R Volkow N Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. Addict Behav 35 : — Neuroimage 57 : — Ann Phys Rehabil Med 55 : — Brain Stimul 1 : — Biol Psychiatry 73 : — Neuropsychopharmacol 31 : — Brain Stimul 4 : 38 — Neuropsychopharmacol 29 : — Int J Alzheimers Dis : 1 — 5. Neuroimage 85 Pt 3 : — Exp Neurol : 14 — Neuroimage 85 : — Neuropsychopharmacol 26 : 53 — Drug Alcohol Depend 93 : 93 — Trends Neurosci 34 : — Biol Psychiatry 65 : — Drug Alcohol Depend 96 : — New York. Google Preview. Schizophr Res : — Wickham H ggplot2: elegant graphics for data analysis , 1 st edn. New York : Springer. Nat Neurosci 7 : — Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide. Sign In or Create an Account. Sign in through your institution. Advanced Search. Search Menu. Article Navigation. Close mobile search navigation Article Navigation. Volume Article Contents Abstract. Methods and materials. Statement of Interest. Journal Article. State dependent effect of transcranial direct current stimulation tDCS on methamphetamine craving. Alireza Shahbabaie , Alireza Shahbabaie. Oxford Academic. Mehrshad Golesorkhi. Behnam Zamanian. Mitra Ebrahimpoor. Fatemeh Keshvari. Vahid Nejati. Felipe Fregni. Hamed Ekhtiari. Address for correspondence: Dr H. Revision received:. Select Format Select format. Permissions Icon Permissions. Abstract Transcranial direct current stimulation tDCS has been shown to modulate subjective craving ratings in drug dependents by modification of cortical excitability in dorsolateral prefrontal cortex DLPFC. Addiction , cue-induced craving , methamphetamine , non-invasive brain stimulation , transcranial direct current stimulation. Open in new tab Download slide. Table 1 Open in new tab. Demographic and substance abuse characteristics. Descriptive statistics. Table 2 Open in new tab. T p -value. Drug Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective. Google Scholar Crossref. Search ADS. Prefrontal cortex modulation using transcranial DC stimulation reduces alcohol craving: a double-blind, sham-controlled study. Cumulative priming effects of cortical stimulation on smoking cue-induced craving. Non-invasive brain stimulation to assess and modulate neuroplasticity in Alzheimer's disease. Prolonged visual memory enhancement after direct current stimulation in Alzheimer's disease. Examining transcranial direct-current stimulation tDCS as a treatment for hallucinations in schizophrenia. One session of high frequency repetitive transcranial magnetic stimulation rTMS to the right prefrontal cortex transiently reduces cocaine craving. Can noninvasive brain stimulation enhance cognition in neuropsychiatric disorders? Activation in mesolimbic and visuospatial neural circuits elicited by smoking cues: evidence from functional magnetic resonance imaging. High-frequency repetitive transcranial magnetic stimulation decreases cigarette smoking. Designing and evaluation of reliability and validity of visual cue-induced craving assessment task for methamphetamine smokers. A sham-controlled, phase II trial of transcranial direct current stimulation for the treatment of central pain in traumatic spinal cord injury. Cortical stimulation of the prefrontal cortex with transcranial direct current stimulation reduces cue-provoked smoking craving: a randomized, sham-controlled study. Cue-induced cocaine craving: neuroanatomical specificity for drug users and drug stimuli. Activation of prefrontal cortex and anterior thalamus in alcoholic subjects on exposure to alcohol-specific cues. Prefrontal cortex transcranial direct current stimulation tDCS temporarily reduces food cravings and increases the self-reported ability to resist food in adults with frequent food craving. Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. Amplitude low-frequency oscillation abnormalities in the heroin users: a resting state fMRI study. Non-invasive cerebral stimulation for the upper limb rehabilitation after stroke: a review. The use of repetitive transcranial magnetic stimulation rTMS and transcranial direct current stimulation tDCS to relieve pain. Repetitive transcranial magnetic stimulation of the dorsolateral prefrontal cortex reduces nicotine cue craving. Low frequency repetitive transcranial magnetic stimulation of the left dorsolateral prefrontal cortex transiently increases cue-induced craving for methamphetamine: a preliminary study. Effects of expectancy and abstinence on the neural response to smoking cues in cigarette smokers: an fMRI study. Reducing procedural pain and discomfort associated with transcranial direct current stimulation. Differential brain activity in alcoholics and social drinkers to alcohol cues: relationship to craving. Effect of transcranial brain stimulation for the treatment of Alzheimer disease: a review. Enhancing vigilance in operators with prefrontal cortex transcranial direct current stimulation tDCS. Treatment of depression with transcranial direct current stimulation tDCS : a review. Behavioural and functional neuroimaging evidence for prefrontal dysfunction in methamphetamine-dependent subjects. Differences in cortical activity between methamphetamine-dependent and healthy individuals performing a facial affect matching task. Impaired prefrontal cortical function and disrupted adaptive cognitive control in methamphetamine abusers: a functional magnetic resonance imaging study. Randomized, placebo-controlled trial of bupropion for the treatment of methamphetamine dependence. United Nations Office on Drugs and Crime. Transcranial direct current stimulation influences probabilistic association learning in schizophrenia. Neurocognitive deficits are associated with unemployment in chronic methamphetamine users. Issue Section:. Download all slides. Views 4, More metrics information. Total Views 4, Email alerts Article activity alert. Advance article alerts. New issue alert. In progress issue alert. Receive exclusive offers and updates from Oxford Academic. Citing articles via Web of Science Working memory performance predicts, but does not reduce, cocaine- and cannabinoid-seeking in adult male rats. More from Oxford Academic. Science and Mathematics. Authoring Open access Purchasing Institutional account management Rights and permissions. Get help with access Accessibility Contact us Advertising Media enquiries.
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