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Background: Driving a car is a complex task requiring coordinated functioning of distributed brain regions. Controlled and safe driving depends on the integrity of the dorsolateral prefrontal cortex (DLPFC), a brain region, which has been shown to mature in late adolescence. Methods: In this study, driving performance of twenty-four male participants was tested in a high- end driving simulator before and after the application of transcranial direct current stimulation (tDCS) for 15 minutes over the left or right DLPFC. Results: We show that external modulation of both, the left and the right, DLPFC directly influences driving behavior. Excitation of the DLPFC (by applying anodal tDCS) leads to a more careful driving style in virtual scenarios without the participants noticing changes in their behavior. Conclusion: This study is one of the first to prove that external stimulation of a specific brain area can influence a multi-part behavior in a very complex and everyday-life situation, therefore breaking new ground for therapy at a neural level. lesions in the DLPFC (especially in the right hemisphere) Background Standardized so-called "gambling tasks" in which partici- show riskier behavior than a healthy control group . By pants can win or loose money by drawing cards from dif- contrast, lesions in the ventro-medial prefrontal cortex ferent decks have become an established tool for the lead to "myopia" for the future, that is, insensitivity for investigation of "risk behavior" in psychological and neu- future consequences of present behavior . Interestingly, rophysiological research [Iowa Gambling Task:. , Cam- recent studies have shown that external stimulation of the bridge Gambling Task: [2,3]]. Typically, riskier behavior DLPFC with Transcranial Magnetic Stimulation (TMS)  in these tasks leads to higher gains but also to higher and with Transcranial Direct Current Stimulation (tDCS) losses. The standardization of such gambling tasks is cru-  can influence risk-taking behavior. cial when considering their clinical application; e.g. in the diagnosis of patients having problems with impulsiveness The DLPFC is a brain region that matures through to late or planning and decision-making. adolescence , and even during the second decade of life . The late myelination of the DLPFC may serve as one At a neural level, risk-taking behavior, decision-making possible explanation why adolescent behavior is often and impulsiveness share similar neural networks in the characterized by motivational difficulties, addiction and dorsolateral prefrontal cortex (DLPFC) . Patients with impulsivity . The fact that driving accidents are the Page 1 of 7 (page number not for citation purposes) Behavioral and Brain Functions 2008, 4:34 http://www.behavioralandbrainfunctions.com/content/4/1/34 main cause of death for adolescents and young adults is a Experimental design problem of paramount importance, also from a political Every subject was tested on two different days within a perspective . Different studies reported that risky driv- week. On the first day, after a theoretical instruction about ing behavior is more prominent among young drivers the driving simulator and the tDCS procedure, all subjects . The frequency of substance abuse and the degree of gave their written informed consent for participation in aggressiveness are (besides gender and social factors) the the experiment and filled in a questionnaire about their main predictors for risky driving . Furthermore, chil- driving behavior (frequency of driving and years in pos- dren diagnosed with ADHD have been shown to have an session of driver's license), education and health. Before elevated risk for driving-related problems in adulthood the actual experiment, participants had the opportunity to . In view of the preceding, we can assume that the drive a sample course ("circuit") in the driving simulator DLPFC is importantly involved in modulating risky driv- in order to get used to the simulation. ing behavior. Results from the standardized "Risk-" and "Gambling-Tasks" are consistent with the findings about For the actual experiment, a course called "Mountain the neurodevelopment of the DLPFC, but the generaliza- Course"  was chosen (see below for details). Every tion of findings to everyday life situations is hampered by participant drove this course once without any tDCS the high specificity of these paradigms. influence. After this "baseline-drive", tDCS was applied over the DLPFC for 15 min (see below for details). In half The aim of this study was to examine the role of the of the subjects stimulation was applied to the right hemi- DLPFC in a situation more closely associated with risk tak- sphere, while in the other half the left hemisphere was ing in everyday life. We hypothesized that excitation of stimulated. After the stimulation, the tDCS equipment the DLPFC causes stronger executive control and less risky was removed and the subjects drove the same course driving behavior. In order to test this hypothesis, we mod- under the after-effect of the stimulation without cables on ulated neural excitability of the participants' DLPFC their heads. This protocol (testing performance after the before measuring their performance in a driving simula- application of tDCS) was used to increase external validity tor. As mentioned above, several studies have reported of the driving situation and relies on the long-lasting after- differential involvement of the right and left DLPFC in the effects of tDCS (on the motor cortex until 90 min) . control of risk behavior . Therefore, we also tested for To our knowledge, there are no studies that investigated such laterality effects expecting stronger effects after mod- after-effects of tDCS on prefrontal cortical areas. There- ulation of the right PFC. fore, we assume similar temporal characteristics as reported for the motor cortex. During the stimulation In contrast to an earlier study on the modulation of risk with tDCS, the participants sat outside the driving simula- behavior by external brain stimulation , we used tDCS tor on a chair and filled in the handedness and health instead of TMS. tDCS has the advantage that the partici- questionnaires . To assess subjective involvement in pants barely notice the stimulation. Furthermore, depend- the virtual environment, an adapted version of the MEC- ing on the direction of the current flow, neural excitability SQ (spatial presence questionnaire)  was filled in by can be either enhanced or decreased. the participants after each driving session. The possible impact of the tDCS stimulation on the emotional state Methods was assessed using the Self-Assessment-Manikin  Subjects before and after stimulation. On the second day, the same Twenty-four male subjects participated in the study. procedure was applied but the stimulation electrodes Twenty-one of them were students. All participants were were switched resulting in a stimulation condition between 20 and 30 years old (mean age: 24.1; SD: 2.7). (anodal or cathodal stimulation) different from that Male subjects were chosen because in pilot experiments applied during the first experimental day. The order of the men were found to have a lower probability of experienc- stimulation conditions was counterbalanced. The ques- ing nausea in the driving simulator. All of the participants tionnaires about health and handedness were not filled in were right-handed, had no history of neurological or psy- on this second day. This difference in procedure on the chiatric diseases and were in the possession of a driver's second day, however, is unproblematic since the condi- license for at least 2 years. The experiment was approved tions were counterbalanced across subjects. by the local ethic committee (ethic committee of the can- ton of Zurich, specialized subcommittee for psychiatry, Driving simulator neurology and neurosurgery, Oetwil am See, Switzer- The driving simulator used in the experiment is an land). upgraded version of the F10PF-Model of the Dr.-Ing. Reiner Foerst GmbH . The virtual environment was projected on three 61" videowalls (RP 61" ES LCD) . The actual test-course, called "Mountain Course", consists Page 2 of 7 (page number not for citation purposes) Behavioral and Brain Functions 2008, 4:34 http://www.behavioralandbrainfunctions.com/content/4/1/34 of a car that can be driven on a road starting outside a Statistical analysis small village, passing through the village with traffic Dependent variables reflecting driving performance under lights, and then following a route through built up areas. the influence of tDCS were compared with the perform- The simulation automatically stopped after a covered dis- ance during the baseline-drive (before tDCS application) tance of 3 km (lasting around 3.5 min depending on driv- using repeated-measures ANOVAs with 'time' (2 levels; ing speed). The scene was identical for each subject. pre- vs. post-simulation) and 'stimulation condition' (2 Traffic, traffic lights, dangerous events (children, animals) levels; anodal vs. cathodal) as within-subject factors and etc. were simulated randomly in order to enhance the real- 'side of stimulation' as between-subject factor. For each ity of the scene. Every 20 ms, about 30 measures with dependent variable ("distance to driver ahead", "driving which to capture driving behavior were registered (e.g. speed", "speed violations" and "revolutions per minute") driving speed, distance to driver ahead, position in the an individual ANOVA model was set up. Post-hoc t-tests course, position of break, accelerator, gear, revolutions (based on the Bonferroni-Holm procedure) were calcu- per minute, lateral distance from road mid-line etc.) lated to further explore the effects of the ANOVA. Transcranial direct current stimulation Results The "DC-Stimulator" distributed by neuroConn  was Prior to the statistical analyses, behavioral data of three used for transcranial direct current stimulation. The con- participants were excluded (right-hemispheric stimula- stant current was applied through two saline-soaked elec- tion group: 1, left-hemispheric stimulation group: 2) trodes with a surface of 35 cm . Based on earlier studies because these subjects demonstrated extremely high or modulating DLPFC excitability , stimulation electrodes low values for the parameter "distance to driver ahead" were placed at the F3 or F4 position (international EEG before tDCS stimulation. The remaining data were sub- 10–20-system), respectively for left and right-hemispheric jected to repeated-measure ANOVAs with 'time' and 'stim- stimulation. For DLPFC excitation, the anode was posi- ulation condition' as within-subject factors and 'side of tioned on F3 (or F4) and the cathode was mounted on the stimulation' as between-subject factor. As displayed in fig- ipsilateral mastoid. For DLPFC inhibition, the two elec- ure 1, the analyses revealed 'time × condition' interactions trodes were switched (cathode over F3/F4, anode over for "distance to driver ahead" [F(1,19) = 4.25, p = 0.05] ipsilateral mastoid). The subjects were randomly divided and "number of speed violations in built-up areas" into two equally sized groups. One group was stimulated [F(1,19) = 5.97, p = 0.02]. The same trend was evident for on the left, the other on the right hemisphere. tDCS was "driving speed" [F(1,32) = 2.83, p = 0.1] and "revolutions applied for 15 minutes with a constant current intensity of per minute" [F(1,32) = 3.21, p = 0.09]. There was no main 1mA. As a precaution measure, the "DC-Stimulator" auto- effect of 'side of stimulation' or an interaction of this matically turns off when electrical resistance is too high. Differen Figure 1 ces between anodal and cathodal tDCS Differences between anodal and cathodal tDCS. Depicted are differences and standard errors (SE) between pre- and post-stimulation driving behavior (POST minus PRE) pooled across the two experimental groups (left DLPFC and right DLPFC stimulation). The p-values indicate the significances of the 'time × condition' interactions for each of the four behavioral varia- bles. Page 3 of 7 (page number not for citation purposes) Behavioral and Brain Functions 2008, 4:34 http://www.behavioralandbrainfunctions.com/content/4/1/34 between-subject factor with the variables of interest (time, Subjects did not indicate different degrees of presence in condition) for any of the four variables. the virtual scene in the different conditions, and there were no differences in emotion either, as reported with Post-hoc paired t-tests revealed that anodal tDCS induced the Self-Assessment Manikin. None of the subjects an increase of the "distance to driver ahead" [right-hemi- reported nausea during driving simulation. The years in sphere tDCS: T(10) = -1.77, p = .05; left-hemisphere tDCS: possession of a driver's license were not associated with T(9) = -1.84, p = .05] and declines in "number of speed different effects of tDCS. violations" [right-hemisphere tDCS: T(10) = 3.26, p = .005; left-hemisphere tDCS: T(9) = 1.54, p = .08], "driving speed" Discussion [right-hemisphere tDCS: T(10) = 1.64, p = .07; left-hemi- The present study aimed to examine effects of tDCS, and sphere tDCS: T(9) = 1.56, p = .08], and "revolutions per hence, of the induced manipulation of DLPFC activity on minute" [right-hemisphere tDCS: T(10) = -1.51, p = .08; left- driving behavior in a customary driving simulator. As a hemisphere tDCS: T(9) = 3.10, p = .006]. All four variables main result, we found that anodal tDCS evoked less risky indicate a more cautious driving behavior when DLPFC driving behavior while cathodal tDCS did not signifi- activity is enhanced. For cathodal tDCS, on the other cantly influence the driving style. With respect to anodal hand, only one trend was registered (decrease of "driving stimulation, behavioral differences were found in four speed" in the left-hemisphere stimulation group; p = .08). variables ("driving speed", "distance to driver ahead", Hence, learning effects induced merely by the repeated "number of speed violations", "revolutions per minute") exposure to the task cannot explain the effects found. measuring different aspects of driving behavior. While the "distance to driver ahead" was larger after anodal tDCS as To compare the two groups, post-stimulation perform- compared to the baseline measurement, the "number of ance was related to the individual pre-stimulation per- speed violations", the "driving speed" and the "revolu- formance for each participant (a posttraining value of tions per minute" were reduced. These strong behavioral 100% means no change from pre- to posttraining). The changes are evident despite the fact that the participants corresponding values are depicted in figure 2. Since, in were not aware of their change in behavior. case of cathodal stimulation, the resulting values did not differ significantly from the reference value (100%), we The crucial association between functions mediated by refrain from comparing between-group differences. With the prefrontal cortex and risk-taking driving behavior respect to anodal tDCS, two-sample t-tests comparing the found in this study is in line with previous findings about performance changes between the two groups resulted in the prefrontal cortex . It is remarkable that a complex p-values > 0.4 for all behavioral variables. behavior such as driving a car can be directly influenced by an external modulation of the cortical excitability. Our main result is consistent with earlier research focusing on Left- vs. right-hem Figure 2 ispheric DLPFC stimulation Left- vs. right-hemispheric DLPFC stimulation. Depicted are performance changes from pre- to post-stimulation meas- urements in percent ((POST*100)/PRE) and standard errors (SE) separately for two experimental groups (left DLPFC and right DLPFC stimulation). Page 4 of 7 (page number not for citation purposes) Behavioral and Brain Functions 2008, 4:34 http://www.behavioralandbrainfunctions.com/content/4/1/34 the external modulation of DLPFC activity and its effects pate increased and not decreased attentional functional- on risk-taking behavior in situations less closely related to ity). It can be further speculated about general effects of risk-taking in everyday life [5,22,23]. Knoch et al., for boredom or tiredness after the stimulation break; how- example, showed that low-frequency rTMS applied over ever, this effect should be the same after anodal and the DLPFC evoked more risky behavioral choices in a cathodal stimulation and can therefore not explain the standard gambling paradigm . The authors did not, observed difference between stimulation conditions. In however, study the effect of DLPFC excitation (as evoked addition, the increased carefulness of driving that we by high-frequency rTMS) in their study, which would have observed following anodal tDCS was not only character- induced similar effects in the stimulated tissue as anodal ized by a generally slower driving speed but also by a tDCS. Furthermore, Fecteau et al. reported a reduction of reduced number of speed violations, by reduced revolu- risk-taking behavior in different task paradigms following tions per minute and by an enlarged distance to the car tDCS applied over the DLPFC [6,24]. In their studies, the driving ahead. In our opinion this combination of effects two electrodes were mounted to overly the left and right points to a more careful driving style rather than to DLPFC areas – an electrode configuration that allowed the enhanced tiredness. simultaneous stimulation of both hemispheres. Depend- ing on the task, behavioral effects were evident only after Cathodal stimulation did not lead to a significant altera- right anodal/left cathodal stimulation  or after both, tion of driving behavior. The reasons for this lacking effect right anodal/left cathodal and left anodal/right cathodal are difficult to explain, thus we can only offer more or less DLPFC stimulation . Using EEG combined with the speculative explanations. Given that functional lateraliza- estimation of intracerebral sources of brain activation, a tion of the DLPFC is an unsolved issue, it may well be that recent study of our group uncovered less activation in the the unilaterally evoked hyperpolarization is simply not right-sided DLPFC during speeded and impulsive driving strong enough to induce a clear behavioral effect. The . This finding is in close correspondence with the hemisphere not stimulated may be equipped to solely study by Clark et al.  reporting the same lateralization prevent the individual from showing more risky behavior effects in patients with brain lesions in the context of risk – a mechanism that would be reasonable from an evolu- behavior and with the later study of Fecteau et al. . The tionary perspective. Alternatively, it may be argued that present study, however, did not replicate this lateraliza- the mere notice of receiving electrical stimulation (per- tion effect and, thus, rather supports the earlier study of ceived as a slight itching at the beginning of the stimula- Fecteau et al. . Considering the data currently available, tion) leads to more careful driving that is independent of we have to conclude that the issue of functional DLPFC the stimulation condition. This effect may have counter- lateralization in the context of risk-taking behavior is not acted a potential enhancement of a risky driving style entirely understood – studies comparing simultaneous induced by cathodal stimulation and on the other hand it stimulation protocols as used by Fecteau et al. with stim- may have facilitated the behavioral effect of anodal tDCS. ulation protocols where the reference electrode is posi- tioned on a functionally ineffective position would There is one methodological limitation of the tDCS tech- contribute to clarify this issue. nique that should be addressed. Given the electrode size of 35 cm , it is obvious that the spatial resolution is low. The propensity of risk-taking behavior has been assumed Furthermore, when using this technique, one has to deal being linked to the openness to drug experiences and the with remote effects. Since the brain is a heavily wired sys- general vulnerability for pathological addictive behavior. tem, current spread from the stimulated region to neigh- Several previous studies demonstrated that noninvasive boring and interconnected regions is most likely. Remote stimulation of the frontal cortex lessens the craving for effects have been proven in studies combining transcra- typical drugs such as nicotine [26,27] or cocaine , nial brain stimulation (TMS, tDCS) with PET or fMRI hence suppressing the need to initiate reward-related [29,30]. With respect to the present study, it may be that behavior. In a broader sense, this effect corresponds to a the stimulation of the DLPFC triggered a co-activation of more deliberate style of behavior and is consistent with other regions in the frontal lobe such as the ventromedial the main result of the present study. or orbitofrontal cortex, which may have influenced task performance after stimulation. Since we do not know the One may argue that the lowering of the driving speed can real extent of the tDCS effect, we cannot disentangle pre- be explained by a stimulation-induced decline of atten- cisely the neurophysiological underpinnings and the asso- tion. However, since anodal tDCS stimulation is known ciated psychological processes. Although several to enhance neural excitability in cortical regions underly- methodological problems of tDCS are unsolved so far, ing the stimulation electrode, it seems unlikely to us that there are several studies available supporting the precision anodal stimulation reduces attentional capacities (if and usability of tDCS [31,32]. Uy and Ridding, for exam- anodal tDCS should modulate attention we would antici- ple, showed a specific increase of cortical excitability for Page 5 of 7 (page number not for citation purposes) Behavioral and Brain Functions 2008, 4:34 http://www.behavioralandbrainfunctions.com/content/4/1/34 7. 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Uy J, Ridding MC: Increased cortical excitability induced by transcranial DC and peripheral nerve stimulation. Journal of neuroscience methods 2003, 127(2):193-197. Publish with Bio Med Central and every scientist can read your work free of charge "BioMed Central will be the most significant development for disseminating the results of biomedical researc h in our lifetime." Sir Paul Nurse, Cancer Research UK Your research papers will be: available free of charge to the entire biomedical community peer reviewed and published immediately upon acceptance cited in PubMed and archived on PubMed Central yours — you keep the copyright BioMedcentral Submit your manuscript here: http://www.biomedcentral.com/info/publishing_adv.asp Page 7 of 7 (page number not for citation purposes)
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