Transcranial direct current stimulation, implicit alcohol associations and craving
Introduction
Transcranial direct current stimulation (tDCS) is a technique that can influence cortical plasticity and excitability, and it has been used to manipulate cognitive processes. With tDCS two electrodes are placed on top of the skull and a very low electrical current is transmitted through, which increases excitability under the anodal electrode and decreases excitability under the cathodal electrode (Nitsche et al., 2003). By influencing activity in certain cortical areas during relevant cognitive processes, tDCS may have beneficial effects. Anodal stimulation of the dorsolateral prefrontal cortex (DLPFC) increases performance in several cognitive domains, such as working memory (e.g. Fregni et al., 2005, Gladwin et al., 2012a; Ohn et al., 2008) and decision making (e.g. Dockery, Hueckel-Weng, Birbaumer, & Plewnia, 2009; Fecteau et al., 2007). The DLPFC is involved in many processes related to addiction; mainly higher-order cognitive processes such as behaviour monitoring and attentional and memory processes (Goldstein & Volkow, 2011). The lack of control over impulses has also been proposed to constitute an important factor (Goldstein & Volkow, 2011; Jentsch & Taylor, 1999). Therefore, improving the functioning of the DLPFC could have beneficial effects in addiction. Indeed, anodal tDCS of DLPFC has been found to reduce craving for several substances, such as alcohol, cigarettes and food (Boggio et al., 2008, Fregni et al., 2008, Goldman et al., 2011). To the best of our knowledge, effects of stimulation of other brain regions on craving have not yet been tested. Anodal stimulation of the right inferior frontal gyrus (IFG) has been found to increase inhibitory control, measured by a stop-signal task (Ditye et al., 2012, Jacobson et al., 2011). Therefore stimulation of this region may also decrease craving and/or increase control over impulses to use addictive substances.
The current study had two goals. First, we aimed to extend previous results of tDCS on craving. We investigated whether the effects on craving are also present in heavy drinkers and whether the IFG is also an effective target area. Second, we explored the effects of prefrontal stimulation on the ability to change or overcome biases due to automatic processing of alcohol-related information. The reduction of automatic processing biases may be a potential mediating mechanism for effects of tDCS on craving. One potentially important automatic process is the automatic activation of alcohol associations, which can be measured using an implicit association task (IAT). The IAT has been developed to measure associations between two concepts by comparing performance on a classification task when certain response-categories are grouped together (Greenwald, McGhee, & Schwartz, 1998). The grouping is congruent when the response-categories that are grouped together are associated in memory and incongruent when the associated response-categories are mapped to opposite responses. In a standard alcohol IAT, participants categorize alcohol and other beverages together with positive and negative attribute words. If participants have strong positive associations with alcohol they will show improved performance when “alcohol” responses are grouped with “positive” than with “negative” responses. Perhaps unexpectedly, many studies found that both heavy and light drinkers are faster to sort alcohol with negative than with positive attribute words (Meta-analysis, Rooke, Hine, & Thorsteinsson, 2008; Wiers et al., 2002). However, heavy drinkers were found to be somewhat less negative than light drinkers. When positive and negative associations were measured separately, heavy drinkers showed both positive and negative associations with alcohol, with positive and not negative associations correlating with drinking (Houben & Wiers, 2008). Implicit valence and arousal associations with alcohol have also been found to predict drinking prospectively (Wiers et al., 2002). The IAT has also been tested with approach and avoidance attribute words instead of valence or arousal words; alcohol-approach associations correlated with a higher urge to drink (Palfai & Ostafin, 2003), and with alcohol use and problems (Ostafin & Palfai, 2006). Automatic alcohol-related processes, such as those measured by the IAT, play a potentially important role in the development and maintenance of alcohol addiction. It has been demonstrated that changing alcohol-approach tendencies (and related associations) in alcohol-dependent patients helped them to remain abstinent (Eberl et al., 2013, Wiers et al., 2011).
Prefrontal tDCS could be hypothesized to influence the executive processes that allow biases due to automatic associations to be overcome. In line with this hypothesis, an fMRI study found that the DLPFC was more active during incompatible than during compatible trials (Ames et al., 2013). This leads to the possibility that prefrontal stimulation will result in a relatively negative bias, due to a shift from impulsive to reflective evaluation. This would align with findings in the context of attentional biases: several studies reported a fast alcohol-approach attentional bias while using alcohol, followed by a slow disengagement bias when patients were abstinent (Noël et al., 2006, Townshend and Duka, 2007, Vollstädt-Klein et al., 2009).
As yet, little is known of effects of tDCS on IAT performance. A previous study with a classical IAT with insect and flower words showed that tDCS of the DLPFC did not reduce the bias, and actually selectively improved performance within congruent trials (positive-flowers and negative-insects; Gladwin, den Uyl, & Wiers, 2012). One explanation of this is that stimulation of DLPFC facilitates the recall of information but does not affect the processes leading to incongruence costs in the context of an IAT, thus only leading to a beneficial outcome in the congruent condition where the task-related response is in line with the existing bias. However, effects on alcohol-related IATs have not yet been studied. One possibility we explored is that prefrontal tDCS would enhance the ability to overcome biases, in line with previous work on the enhancement of working memory and executive function. Another possibility is that it would actually enhance performance for the congruent response-grouping, as in our previous study. Given the repeated finding that negative alcohol-associations are stronger than positive alcohol associations, tDCS could then make alcohol associations more negative. In either case, if tDCS can affect biases due to alcohol associations, this could provide clues on how tDCS is able to reduce craving.
To these aims, we tested the effects of tDCS on self-reported alcohol craving and on two variants of the IAT, one with positive and negative words (affective IAT) and one with approach/avoidance words (motivation IAT). Based on previous research, the main target area was the left DLPFC. Since addiction is associated with weakened ability to inhibit drinking behaviour (Goldstein & Volkow, 2011), the right IFG was also explored in our setup. We hypothesized that, similar to alcohol-dependent patients, heavy drinkers would also demonstrate reduced craving after receiving DLPFC and possibly also IFG stimulation. As described above, we further explored effects of tDCS on cognitive processes indexed by the IAT.
Section snippets
Participants
Forty-eight students (age: M = 21.7, SD = 2.8; gender: 17M/31F) were included. The study focused on hazardous drinkers (AUDIT > 8 at screening via email). On the testing day six participants scored lower than 8 when retaking the AUDIT, and were excluded from the final sample. One participant did not perform the experiment as required and was also excluded. The final analytical sample therefore consisted of 41 participants (age: M = 21.7; SD = 3.0; gender: 15M/26F). All were right handed and were Dutch
Results
All participants tolerated the stimulation well and none asked for the stimulation to be terminated. Groups did not differ on baseline characteristics (Table 1). The interaction between tDCS and time on Inclined scores was significant (F(2,38) = 4.13, p = 0.024, η2 = 0.18; Fig. 1). Planned contrasts with difference scores (post–pre) showed that craving decreased after DLPFC stimulation compared to sham stimulation (t(38) = −1.88, p (one-sided) = 0.034, d = 0.762). Craving did not change significantly after
Discussion
This study examined the effects of anodal tDCS over the DLPFC and IFG on craving and two implicit association tests. It gives new support for the possibility for tDCS of the DLPFC to also influence mild craving in heavy drinkers, in line with earlier studies indicating reductions in stronger forms of craving in alcohol-dependent patients (Boggio et al., 2008). In the present sample of heavy drinking students, effects were found on a scale that measured inclinations to drink; somewhat weaker
Acknowledgements
This research was supported by N.W.O. (Dutch Science Foundation) Research Talent Grant 406-11-203, and a grant from the European Foundation for Alcohol Research (ERAB, EA 1239).
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2022, Neuroscience LettersCitation Excerpt :Albeit with different protocols, in particular with distinctions among single or multiple sessions [15,42], findings are convergent for different kinds of addiction (see [39,46] for reviews) with anodal stimulation generally administered for about 20 min at 2 mA over the bilateral DLPFC (F3 and F4 sites of the 10/20 systems for the left and right hemisphere respectively; for more details see the comprehensive review by Yadollahpour and Yuan [85]). Similar effects on craving were obtained for alcohol, cocaine and nicotine with the active electrode positioned on the left [30,12,11,19,21,82] as well as on the right hemisphere [30,27,43,7,53,51,60]. However, craving and substance consumptions are not always affected by the tDCS in a similar way: in fact, some studies document a reduction of both craving and consumption [11,27], while others report unaffected craving with reduced consumption [78], as well as a decrease of craving with unaffected substance consumption [51,60].
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