Transcranial direct current stimulation (tDCS) can enhance cognitive control functions including attention and top-down regulation over negative affect and substance craving in both healthy and clinical populations, including early abstinent (∼1. 5 h) smokers. The aim of this study was to assess whether tDCS modulates negative affect, cigarette craving, and attention of overnight abstinent tobacco dependent smokers. In this study, 24 smokers received a real and a sham session of tDCS after overnight abstinence from smoking on two different days. We applied anode to the left dorsolateral prefrontal cortex and cathode to the right supra-orbital area for 20 min with a current of 2. 0 mA. We used self-report questionnaires Profile of Mood States (POMS) to assess negative affect and Urge to Smoke (UTS) Scale to assess craving for cigarette smoking, and a computerized visual target identification task to assess attention immediately before and after each tDCS.
Smokers reported significantly greater reductions in POMS scores of total mood disturbance and scores of tension–anxiety, depression–dejection, and confusion–bewilderment subscales after real relative to sham tDCS. Furthermore, this reduction in negative affect positively correlated with the level of nicotine dependence as assessed by Fagerström scale.
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However, reductions in cigarette craving after real vs. sham tDCS did not differ, nor were there differences in reaction time or hit rate change on the visual task. Smokers did not report significant side effects of tDCS. This study demonstrates the safety of tDCS and its promising effect in ameliorating negative affect in overnight abstinent smokers. Its efficacy in treating tobacco dependence deserves further investigation.
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Keywords: tobacco dependence, transcranial direct current stimulation, smoking abstinence, cigarette craving, negative affect, brain stimulation. Cigarette smoking is the number one cause of preventable death in the United States (1 ). Most tobacco dependent smokers want to stop smoking (2 ). However, they often experience tobacco withdrawal symptoms including craving for smoking, negative affect, and deficits in attention after abstinence from smoking, and thus relapses are common after short durations of abstinence (3 –5 ). Current therapies for tobacco dependence include nicotine replacement therapy, bupropion sustained release formula, and varenicline. These therapies can significantly reduce tobacco withdrawal symptoms and increase abstinence rates, but are not effective in all smokers (6 –9 ). Therefore, new therapies for reducing tobacco withdrawal are needed to help smokers quit.
This study assessed whether transcranial direct current stimulation (tDCS) could modulate mood, attention, and craving for smoking of tobacco dependent smokers who maintain abstinence overnight. Transcranial direct current stimulation is a safe, non-invasive, and inexpensive method for modulating neuronal excitability. It modulates cortical excitability using small direct electrical currents (1 ∼ 2 mA) delivered to the scalp (10 –14 ) via two electrodes with opposite polarities (i. anodal and cathodal) placed on the scalp.
Anodal stimulation increases cortical excitability whereas cathodal stimulation decreases cortical excitability (12. 13. 15. 16 ). These effects can last up to 90 min after a single stimulation session of 13 ∼ 20 min (17 –20 ), and can further increase after repeated stimulation (i. cumulative effects) (21.
22 ). Several studies assessed the effects of tDCS on cue-induced craving for drug use. One study applied anodal stimulation of 2 mA to either the right or left dorsolateral prefrontal cortex (DLPFC) for 20 min. This anodal stimulation reduced cue-induced tobacco craving in early abstinent (∼1.
5 h) smokers (23 ). In another study, daily sessions (20 min) of anodal stimulation to the left DLPFC for 5 days reduced cue-induced tobacco craving and the number of smoked cigarettes during the 5-day period (22 ). This study also observed the cumulative effect of tDCS, i.
cue-induced craving decreased further after each tDCS session. Other studies reported that anodal stimulation of the DLPFC reduced substance craving of alcohol abusers, marijuana users, and healthy participants (22 –28 ). Furthermore, tDCS has been reported to induce beneficial effects on other cognitive domains such as attention, working memory, or response inhibition in healthy participants or patients with stroke, depression, Parkinson’s disease, or alcohol dependence (29 –40 ), and also in affective domains such as mood in patients with depression or tinnitus (36.
41 –45 ). Findings from aforementioned studies indicate that anodal stimulation of the DLPFC may ameliorate tobacco withdrawal by reducing cigarette craving, ameliorating negative affect, and improving cognitive function. However, only two tDCS studies on smokers have been published, and these two studies assessed smokers abstinent from smoking for a short duration (i. ∼1. 5 h). To our knowledge, no published studies assessed the effect of tDCS on longer abstinent smokers (e.
overnight abstinent) and across several measures related to different aspects of tobacco withdrawal. Given the potential clinical significance of assessing longer abstinent smokers and also to collect pilot data for further larger clinical trials, we designed this study to test whether anodal stimulation applied to the left DLPFC in overnight abstinent smokers would modulate their mood, attention, and craving for smoking. Based on the above-reviewed studies, we predicted that abstinent smokers would show reduced craving and negative mood, and improved performance on an attention task, after real relative to sham tDCS. Materials and Methods. This study was approved by the Human Investigation Committee at Yale School of Medicine and was performed in accordance with the Declaration of Helsinki. Potential participants were recruited from communities around Yale University through flyers and ads placed on Craigslist (www.
craigslist. org ). All participants provided written informed consent. The inclusion criteria were good general health, age between 18 and 60 years, more than 10 cigarettes per day for at least 2 years, no current illicit drug use as indicated by negative results on urine drug screens of cocaine, methamphetamine, opiates, or benzodiazepines at all sessions, and ≤10 standard drinks of alcohol per week (one standard drink consists of one 12 oz. beer, 6 oz.
of wine, or one shot (1. 5 oz. ) of hard liquor (80 proof). The exclusion criteria were any current medical conditions, current neuropsychiatric disorders, more than one marijuana cigarette per week, pregnancy as indicated by a positive result on the urine pregnancy test, self-report of learning disability or dyslexia, current use of psychotropic drugs, or self-report of TB or HIV positive.
During a baseline session, carbon monoxide (CO) in expired air was taken as an objective measure of recent smoking (Micro Smokerlyzer II, Bedfont Scientific Instruments), and a level >15 ppm was considered as consistent with recent smoking. Participants also completed the Fagerström Test for Nicotine Dependence (46 ), Urge to Smoke (UTS) Scale (47 ), Profile of Mood States (POMS) (48 ), questionnaires for smoking history and demographic information, and received training in performing a computer task testing attention.
The final sample included 24 smokers (3 females), with a mean age of 45 years (range 28 ∼ 59, standard deviation, SD = 7. 6), smoked an average of 16. 4 cigarettes per day (range 10 ∼ 30, SD = 5. 6), and a mean Fagerström score of 5.
7 (range 1 ∼ 9, SD = 2. 0). Subsequent to baseline assessments, subjects participated in two test sessions, one for real and the other for sham tDCS, on two different days with a minimal interval of 48 h.
This used a single-blind design, i. participants were blind to real vs. sham tDCS. The sequence of the two tDCS sessions was counterbalanced among participants. On each test day smokers reported to the laboratory in the morning around 10 a.
after maintaining abstinence from smoking overnight (>10 h abstinence). They provided a breath sample for CO assay, which should be <10 ppm or half of the baseline measure as a confirmation of overnight abstinence. Otherwise, the study session would be stopped and rescheduled. Smokers also provided a urine sample for drug screen, and would be excluded from further study if the urine sample were positive for any drugs mentioned above.
After confirmation of overnight abstinence and no drug use, participants continued the study session by completing a set of questionnaires including UTS (47 ) and POMS (48 ). Then, they performed a computerized task testing attention. After the task, they watched cigarette smoking-related pictures and video clips to induce craving for smoking for 5 min. While viewing smoking cues, smokers were instructed to put a pack of cigarettes on the desk in front of them, hold a cigarette, and put the cigarette in their mouth, and light a lighter without lighting the cigarette.
Participants received tDCS (either real or sham) after watching the smoking cues. Following the tDCS, they completed the tDCS Adverse Effects Questionnaire, performed the computerized attention task, and completed the UTS and POMS again. Transcranial direct current stimulation. We used a 1 × 1 Low-Intensity DC Stimulator, Model 1224-B (Soterix, LLC, New York, NY, USA), and two sponge electrodes (5 cm × 7 cm) soaked with saline to deliver tDCS.
During each session, the anode was placed over the left DLPFC and the cathode was placed over the contralateral supra-orbital area. The DLPFC was localized using the international 10/20 EEG system (F3) (49 ). In real tDCS session, stimulation was given at 2 mA for 20 min, with gradual ramping up of the current over 30 s. For sham stimulation, current ramped up to 2 mA over the first 30 s and then ramped down to zero during another 30 s, thus giving the same initial sensation of tDCS. This procedure was regularly used to keep participants blind to the real vs.
sham stimulation (23. 50 –52 ). The sham stimulation also lasted for 20 min. The POMS consists of six subscales, collectively including 65 five-point items that describe mood, and these items were used to calculate a score for total mood disturbance. The range of possible scores is −32 to 200 for total mood disturbance, calculated by subtracting the score for the vigor–activity subscale from the sum of scores for the remaining five subscales (5 ). The possible scores for the six subscales are as follows: tension–anxiety (0–36), depression–dejection (0–60), anger–hostility (0–48), vigor–activity (0–32), fatigue–inertia (0–28), and confusion–bewilderment (0–28). For the total mood disturbance and all subscales, except for vigor–activity, a higher score indicates a more negative mood state.
The UTS was used to assess cigarette craving. It consists of following seven-point items: (1) If you could smoke freely, would you like a cigarette at this moment? (2) Do you have an urge for a cigarette right now? (3) Do you miss a cigarette? (4) I crave a cigarette right now, (5) I am going to smoke as soon as possible, (6) All I want right now is a cigarette, (7) I don’t want to smoke now, (8) I have no desire for a cigarette now, (9) Nothing would be better than smoking a cigarette right now, (10) Smoking a cigarette would not be pleasant. The highest possible score is 70, and a higher score indicates greater craving. The tDCS Side Effect Questionnaire was used to assess tDCS side effects including headache, neck pain, scalp pain, scalp burns, tingling, skin redness, sleepiness, trouble concentrating, acute mood change, and other effects (24 ). The severity of each side effect is indexed using a four-point system, i.
1-Absent, 2-Mild, 3-Moderate, and 4-Severe.
The computerized task for testing attention had two load conditions, one for low and the other for high load. It used digits, inclusively between 1 and 9, as stimuli.
The low load condition presented one digit in the center of the screen for each stimulus (Figure (Figure1), 1 ), and the stimulus was a target if the digit was an even number. The high load condition presented five digits simultaneously for each stimulus (Figure (Figure1), 1 ), and the stimulus was a target if three of the five digits were even numbers. The task used block design and each block consisted of 40 trials and one third of them were targets.
Each stimulus was presented for 500 ms with an interstimulus interval of 1000 ms. Our previous studies and others’ indicated that different neural substrates underlay attention at different levels of attentional demand (53.
54 ). Therefore, a task with parametric loads was used to help understand whether tDCS modulates attention at specific task loads. Due to a technical problem, task performance record was not complete for four participants. Given that this missing data can be considered completely at random, the task performances of these 4 participants were excluded from analysis, and the performance data from 20 remaining participants were analyzed.