Bachelorthesis
The effect of anodal transcranial direct current stimulation to the
right dorsolateral prefrontal cortex on visual working memory
Name: Peet, B. van der (Bas) Student number: 10381112
Supervisors: Ilja Sligte & Alexander Laufer Date: 29-05-2015
Abstract
Stimulating the DLPFC using tDCS is found to improve VWM. However, there are also studies that provide evidence for a decrease in VWM when the DLPFC is stimulated. The effects of stimulation of DLPFC on visual working memory aren’t clear yet. This study aims to explore whether stimulation of the right DLPFC using tDCS improves the VWM in order to contribute to answer this question. 16 participants took part in two counterbalanced experimental conditions, active tDCS and sham tDCS resulting in a within-subject design. The experiment consisted of three sessions of one hour, performing on a change detection task. 20 minutes of anodal tDCS and sham tDCS was applied to all participants in either session 2 of session 3. There was no significant difference in scores on the change detection task during active tDCS and during sham tDCS. There was found an placebo effect of sham tDCS on task performance. The findings in this study don’t provide evidence that stimulation of the right DLPFC using tDCS improves the visual working memory, nor it provides
Introduction
The role of the dorsolateral prefontal cortex (DLPFC) in visual working memory (VWM) has been a region of interest and controversy for many years. A common accepted definition of visual working memory is Luck & Vogel (2013) definition that visual working memory is the active maintenance of visual information to serve the needs of ongoing tasks. The prefrontal cortex (PFC) seems to act as the most important neural substrate in working memory. First, evidence was found in studies of monkeys where lesions in DLPFC resulted in delay dependent impairments on delayed response tasks (Bauer & Fuster, 1976, cited in Curtis & D’Esposito, 2003). Second, several studies showed with neurophysiological recordings and neuroimaging techniques persistent and sustained neural activity in DLPFC during the retention interval in change detection tasks and delayed response tasks. Courtney,
Ungerleider, Keil & Haxby (1997) for instance used fMRI to show sustained neural activity in several prefrontal areas over a delay period indicating their predominant role in working memory. This sustained activity is considered to be for maintaining internal representations of relevant sensory information that is no longer available in the environment. It is thought to provide a bridge between the stimulus cue and it’s contingent response (Curtis & D’Esposito, 2003). Since previous studies demonstrated a strong link between the prefrontal cortex,
especially DLPFC, and the supporting function of visual working memory, the specific role of DLPFC in visual working memory is getting more and more research question in studies. Whereas lesions in DLPFC lead to impairment of visual working memory it is plausible that stimulation of DLPFC leads to improvement of visual working memory. This raises the question whether visual working memory can be improved or not. A common used method of stimulating the brain is by applying transcranial direct current stimulation (tDCS) over the scalp. It’s a non-invasive brain stimulation technique that induces a constant weak direct electrical current that flows from the anode to the cathode stimulating the cerebral cortex
(Brunoni & Vanderhasselt, 2014). It increases or decreases the cortical excitability through modulating. Hence, it simulates the sustained neural activity that is considered to be
responsible for maintaining the information during the retention interval. TDCS shows promise as a treatment for several working memory deficits and neurological conditions (Floel & Cohen, 2007, cited in Mulquiney et al., 2011). In addition, it’s a low-cost method, the equipment is portable, proven to be extremely safe and easily applied (Coffman, Clark, & Parasuraman, 2014). Fregni,, Boggio, Nitsche, Bermpohl, Anta, Feredoes, ... & Pascual-Leone (2005) demonstrated that anodal transcranial direct stimulation (tDCS) of the left prefrontal cortex increases accuracy performance in a sequential-letter working memory task. These effects weren’t found with inverse polarity, cathodal stimulation of DLPFC. More evidence was suggested in the study of Andrews, Hoy, Enticott, Daskalakis & Fitzgerald (2011) where anodal tDCS during completion of the n-back task resulted in greater improvement in performance on digit span forward. Mulguiney, Hoy, Daskalakis & Fitzgerald (2011) showed an improvement of performance on a WM task while receiving tDCS, providing confirmation of previous findings that anodal tDCS enhances working memory.
However, not all the studies that researched the effects of stimulation of DLPFC on visual working memory point in the same direction. Sligte, Wokke, Tesselaar, Scholte & Lamme (2011) showed that single pulse magnetic stimulation of the right DLPFC decreased performance of visual working memory. In addition, interesting is that they observed that ‘’people with high DLPFC activity had superior working memory capacity compared to people with low DLPFC activity, and only people with high DLPFC activity really showed a reduction in working memory capacity in response to magnetic stimulation’’ (p.1578). Ambrus, Zimmer, Kincses, Harza, Kovacs, Paulus & Antal (2011) support these findings by demonstrating that both anodal and cathodal tDCS to the right as well as to the left DLPFC
result in a significant impairment of the categorization of prototypes compared to the sham condition. Futhermore, most studies focus on the effect of unilateral stimulation of DLPFC on visual working memory. However, it’s possible that stimulating both hemispheres at the same time can cause different effects on visual working memory. Keshvari, Pouretemad & Ekhtiari (2013) proved that bilateral stimulation of the DLPFC didn’t result in significant changes in speed and accuracy of working memory, concluding that bilateral stimulation of the DLPFC isn’t a useful procedure to improve working memory.
The findings in this research field may be helpful to develop appropriate interventions, so called cognitive remediation therapy, aiming at clinical benefits in patients with for
example Parkinson’s disease and schizophrenia. Boggio, Ferrucci, Rigonatti, Covre, Nitsche, Pascual-Leone & Fregni (2006) already demonstrated that tDCS has a beneficial effect on working memory in patients with Parkinson’s disease. The significant improvement was showed in task accuracy after active anodal tDCS of the left DLPFC with 2mA. These results weren’t found in the other conditions, namely sham tDCS, andodal tDCS of LDLPFC with 1 mA and tDCS of M1. As one can see the effects of stimulation of DLPFC on visual working memory aren’t clear. Some studies contradict each other and often it is concluded that more research and replications need to be undertaken to confirm the findings. Previous research makes it really plausible that the prefrontal cortex and especially the DLPFC is involved in VWM. Moreover, it is clear that stimulating prefrontal cortical areas with tDCS affect performance on working memory tasks. However, the specific conditions under which this effect occurs and it’s direction, increasing or decreasing VWM, aren’t obvious. Hence, this study tries to contribute to answering the question whether stimulation of the right DLPFC can improve visual working memory. Based on the amount of studies showing that it is possible to improve VWM by applying tDCS that outweighs the studies that state the opposite, the hypothesis of this study is that tDCS of the right DLPFC improves visual
working memory. Research will be conducted by stimulation the right DLPFC using 1mA tDCS while performing on a change detection task. Thus, in accordance with this hypothesis the performance on a change detection task is expected to increase during active tDCS. The explanatory mechanism underlying this effect is considered to be that more sustained activity in the DLPFC, simulated by tDCS, results in a better maintenance of the sensory information during the retention interval and therefore increases the task performance.
Method
Participants
Twenty participants were recruited for this study. All the participants were students
Psychology at the University of Amsterdam. They were recruited by advertising in university buildings as well as via internet. Participants who had a history with seizures, neurological diseases or other risk factors such as metal implants or pregnancy were excluded from the study. Left-handed people were also excluded due to the fact that cortical areas in the hemisphere responsible for visual working memory are possibly swapped in left-handed people. Ethical approval was granted by the local ethics committee of the department of Psychology of the University of Amsterdam. All participants handed over a written informed consent prior to the experiment. As compensation the participants were awarded 4 participant points.
Design
All participants took part in two counterbalanced experimental conditions: active anodal tDCS and sham tDCS, resulting in a within-subject design. The experiment consisted of three moments of measurement of each 1 hour. The first appointment was just for practicing and to get used with tDCS. The first appointment was a screening as well and therefore lasted 1,5
hour. The study was conducted double blind, neither the participants nor the experimenter knew to which condition the participant was assigned. A change detection task was administered before, during and after stimulation with tDCS to measure any changes in performances on visual working memory. There were at least 72 hours between each measurement to prevent carry over effects and to make sure there weren’t tDCS effects anymore. Preferably all the measurements of individual participants at the same time to control for fatigue.
Materials
Performance on visual working memory is measured by a change detection task, using eight rectangles in 4 different orientations and a maximum of 3 rectangles with the same orientation per trial. A single trials lasts 5.750 seconds and is structured in chronological order as follows: 1 second fixation, 0.5 seconds green fixation cross, 250 ms presenting eight rectangles, 1 second delay and 3 seconds test response. The fixation window consist of a black fixation cross in the middle of the screen against a gray background. One second after onset this fixation cross turns green. Thereafter eight black rectangles in 8 different orientation show up in a circle around the fixation cross, still with a gray background. Since this memory array only lasts 250 ms no saccades can be made. Subsequently a 1 second delay where all the rectangles disappear. Finally, in the last 3 seconds of the trial one randomly chosen rectangle shows up. Figure 1 displays an example trial. During this test response the participant has to make the choice whether the orientation of the displayed test rectangle has changed by 90 degrees (pressing ‘m’ on keyboard, marked by a green label) or not (pressing ‘z’ on keyboard, marked by a red label). If they give the correct answer by pressing the right key they will hear a brief sound (beep). This gives the participant feedback during the experiment which
block the orientation of the rectangle displayed at the test response has changed by 90
degrees. The orientation of the other 50 percent of the trials will therefore be the same. Also,
Figure 1. Trial design. The sequence of the change detection task. Participants had to detect if the orientation of the rectangle in the memory display had changed in the test display. They were required to respond by pressing a key.
each of the eight possible location around the fixation cross will only be used as test response up to 20 times per block resulting in 160 trials per block (20x80). A 90 second break was included every 53 trials. After completing the block the participant got the instructions to wait
for the experimenter for further instructions.
Twenty minutes of 1mA direct current was applied to the scalp using a 3 by 3
centimetre electrode placed over the F4 location, according to the 10-20 international system for EEG electrode placement, and a 5 by 7 centimetre electrode placed over the left
supraorbital location. The tDCS device has two pre-programmed modes, mode A and mode B, that either runs the program for the active tDCS condition or runs the program for sham tDCS condition. The active tDCS program starts with a 60 second ramp up, where the current fades in, is constant for 18 minutes at 1 mA, and then ramps down in 60 seconds where current fades out. During the sham tDCS program the current only ramps up for 60 seconds and then immediately ramps down in 60 seconds, but still occasionally causing an itchy sensation on the scalp in order to give the participant the feeling that he/she is stimulated.
Procedure
When the participant signed up for the experiment they first received an e-mail with the information brochure. They were requested to read this brochure attentively and it was also the first part of the screening. If any of the questions were answered negatively they were excluded from the experiment. Participants were urgently requested not the use drugs of alcohol the day before measurement. When accepted to the experiment three appointments had to be made in advance. When a participant was too late for an appointment they got excluded from the experiment. When a participant didn’t even show up 4 participation points were deducted. Obvious signs of drinking or drug use prior to the experiment resulted in excluding as well. The first appointment started out with a continuation of the screening. When the participant didn’t meet the screening criteria yet they were still excluded from participation and received 1 participation point. After that verbal instructions were given by the experimenter explaining the change detection task. The experiment was now ready to
start. The remaining time was spent practicing and to get used with tDCS. Afterwards the participants had another chance to quit the experiment, for example when tDCS was experienced uncomfortable or any side effects occurred.
Measurement two and three both took 1 hour conducting a change detection task. This hour can be divided in 3 blocks, each lasted 20 minutes including breaks. The first 20 minutes is before stimulation with tDCS, the second 20 minutes is during tDCS or sham tDCS, and the last 20 minutes is after tDCS of sham tDCS. The order of stimulation was counterbalanced across subjects to prevent learning and carry over effects. Each block consist of 160 trails, divided into three equal parts interrupted by 90 second breaks. After each block the participant will be instructed to wait for the experimenter. Total amount of trails per measurement is 480, 3 blocks containing 160 trials.
After each measurement the participant filled out a short questionnaire about his/her experience with tDCS and was advised to remain 1 hour for possible side effects. The
experimenter as well as at least one first aider were present all the time during the experiment. One participant reported a decrease in consciousness during the tDCS program, which could probably be explained by vegetative dystonia that this participant has been diagnosed with. Other reported side effects during the tDCS program were low to moderate varying from slightly uncomfortable (unspecific) to a tingling and itchy sensation on the scalp. In the exit interview at the end of the last session three participants reported that they tended to know in which session they were actively stimulated by tDCS.
Data analysis
The primary outcome measure where scores on the change detection task. Relevant information about the participant and his/her condition, i.e. number, session, age, gender, tDCS mode, date, was saved in a separate file as well as the scores on the task. Each trial can
be done right, resulting in score 1, or wrong resulting in score 0. Missed trials and early responses were written as negative reaction times and were removed from the data set. The percentage correct answered trials is computed for each block using MATLAB and written to a 9x16 matrix. These outcome measures were analysed carrying out a repeated measures ANOVA and multiple paired t-test to assess any effect of condition or time. Tests conducted with clear prior expectations about the results were one-tailed and used an alpha level of .05 to determine significance.
Results
TDCS or sham stimulation of the DLPFC was applied to the participants during a change detection task. Nineteen participants signed up for this study. Three participants didn’t complete the experiment and dropped out early after completing the first session, because of lack of time. The results consist of the data of the sixteen remaining participants. The data of training session 1 block 3 of participant 4 was lost due to a power cut. The remaining data of participant 4 was treated and analysed equally. Almost all participants tolerated the tDCS well without experiencing noteworthy negative side effects. The order of stimulation was
counterbalanced across participants, resulting in an equal number of active and sham tDCS stimulation during session 2 and 3. To verify if this counterbalancing across participants was successful a repeated measures ANOVA was carried out. There was no significant interaction effect of the factors time and condition on the scores on the change detection task; F(2,30 ) = 0.932 , p = .405. This indicates that the order in which the participants passed through the experiment didn’t have any effect on task performance and that the counterbalancing across participants over conditions was therefore successful. Since there were no expectations made for the interaction effect of time and condition on the scores on the change detection task this
In order to verify if there was an effect of tDCS on task performance a paired t-test was conducted to compare difference in performance on the change detection task during active tDCS and during sham tDCS. To do so, the data was sorted by condition, active tDCS and sham tDCS. To control for learning effects the performance on block 2 was normalised by performance on block 1 by subtracting block 1 from block 2 for both active tDCS and sham tDCS,. If tDCS positively affects task performance the t-test should represent a
difference in means in favour of active tDCS. However, there was no significant difference in
Figure 2. Mean scores of all sixteen participants on change detection task sorted by condition represented over time: before, during and after stimulating DLPFC with active and sham tDCS in either session 2 or session 3. Blocks are 20 minutes each. Note that, due to counterbalancing participants across conditions, the order in which the participants were stimulated differs.
scores on the change detection task for active tDCS block 2 (M=.024 SD =.053) and sham tDCS block 2 (M = .048, SD = .075); t(15)=-1.123, p= .279. These results do not correspond to the expectations, since the expectations predicted the scores on the change detection task to be significant higher during active tDCS compared with sham tDCS. Figure 2 displays this difference graphically.
To examine if there was a placebo effect of sham tDCS on task performance an explorative paired t-test was conducted to compare difference in performance of sham tDCS block 1 and block 2. If this t-test would highlight a difference a placebo effect would be confirmed. This t-test yielded a significant result. Performance in sham tDCs block 2 (M = .685 SD = .090) was significant higher than in sham tDCS block 1 (M = .637 SD = .079); t(15)=-2.557, p=.022. Therefore, a placebo effect of sham tDCS on task performance was confirmed. To find out if there were still learning effects after the training session another paired t-test was performed to compare performance of session 2 block 1 with session 3 block 1, unsorted by condition. If there still were learning effects this explorative t-test should represent a significant difference between these two blocks, in benefit of session 3 block 1. This t-test yielded no significant result, t(15)=-1.132, p=.276, indicating there were no more learning effects after session 1.
To verify if there were possibly long term potentiation effects difference in
performance of active tDCS block 1 was compared with active tDCS block 3 by conducting another explorative paired t-test. If this t-test highlights a difference between these blocks in benefit of block 3 this would indicate long term potentiation effects. There was no significant difference in scores on active tDCS block 1 (M = .642 SD = .055) and active tDCS block 3 (M = .672, SD = .096); t(15)=-1.751, p= .100. It is possible that fatigue in the last block leads causes less attention resulting in a decrease of task performance. To examine long term
difference in performance of active tDCS block 3 and sham tDCS block 3. Performance was normalised to control for learning effects as well by subtracting block 2 from block 3 for both active tDCS and sham tDCS. There was no significant difference in scores on active tDCS block 3 (M = -.007 SD = .077) and sham tDCS block 3 (M = .011, SD = .074); t(15)=-0.633, p= .536. These findings don’t provide evidence for long term potentiation effects.
Discussion
Considering the amount of evidence provided by previous studies this study had a slight preference towards to possibly positive effects of tDCS on visual working memory. As stated before the effects aren’t clear yet, but previous research makes it really plausible that the prefrontal cortex and especially the DLPFC is involved in VWM and stimulating prefrontal cortical areas has repeatedly demonstrated to affect performance on working memory tasks. However, the specific conditions under which this effect occurs and it’s direction aren’t obvious.
Based on a conducted paired t-test there is no significant difference in scores on the change detection task during active tDCS and during sham tDCS. These results do not correspond with the expectations prior to this study, since there was expected that the scores on the change detection task would be significant higher during active tDCS compared with sham tDCS. There was found an placebo effect of sham tDCS on task performance, since the performance of sham tDCS block 1 significant differed from sham tDCS block 2 on the change detection task significant. All other explorative test results turned out not to be significant. This is positive with respect to the presence of any learning effects after the training session. Session 2 block 1 didn’t differ from session 3 block 1, excluding learning effects. No evidence was found supporting the theory of long term potentiation. Long term potentiation is the long-lasting increase of synaptic transmission between neurons based on
recent patterns of activity (Nitsche et al.,2003). This theory underlies and explains effect in task performance after a period of stimulation. Since there wasn’t a significant difference between active tDCS block 1 and active tDCS block 3, nor between active tDCS block 3 and sham tDCS block 3 the theory of long term potentiation is not supported in this study.
The predominantly positive findings in previous research of improving the visual working memory by stimulating the DLPFC led to the hypothesis that stimulation of the right DLPFC results in an improvement of the visual working memory. A theoretical explanation for this phenomenon is that more sustained neural activity leads to a better maintenance of the relevant sensory information during the retention interval and therefore increases performance on visual working memory tasks. TDCS is supposed to simulate this sustained neural activity by increasing the cortical excitability through modulating.
Based on the results in this study this hypothesis is not confirmed. As mentioned previously, the effects of stimulation of the DLPFC on visual working memory aren’t clear yet. This study tries to contribute to answering the question whether stimulation of the right DLPFC can improve visual working memory or not. The results in this study don’t provide any evidence that the visual working memory is increased nor decreased by stimulating the right DLPFC using tDCS. A possible explanation for these results is that stimulation of the DLPFC using tDCS with 1mA isn’t enough to accomplish an effect on the visual working memory. Previous research demonstrated an improvement in task accuracy after tDCS of the left DLPFC with 2mA, whereas no significant result was found in the condition stimulating the left DLPFC with 1mA (Boggio et al., 2006). Another possible explanation for these results is that the effect of stimulating the right DLPFC differs from stimulating the left DLPFC with regard to the visual working memory. For example it could be possible that stimulating the left DLPFC leads to an improvement in visual working memory whilst stimulating the right
Although there is strived to conduct this experiment considering all methodological assumptions, this study has some imperfections and limitations. Instead of the target of 20 participants only sixteen participants completed the experiment. If more participants had completed the experiment the statistical power would increase which made it more likely to find an effect if there is one. Therefore, a suggestion for further research is to recruit at least 20 participants. Another limitations that can possibly influence the results negatively is the permanent presence of at least one experimenter in the room where the experiment was conducted. This can possibly distract the participant from performing on the change detection task as accurate as possible, resulting in a lower percentage correct on the trials. An observer-expectancy effect is not likely, since the experiment is carried out double blind. Nor the experimenter nor the participant knew in which session the participant was stimulated with active tDCS or sham tDCS. To exclude risk factors in using tDCS and relevant deficits that can influence the results all participants were screened on exclusion criteria.
Participants were allowed to drink coffee, tea or water during or prior to the
experiment. Caffeine in coffee and tea can influence the results of the experiment, as caffeine is a central nervous system stimulant which produces an increased focus, wakefulness and the feeling of thinking faster and clearer. However, too much caffeine can lead to side effects like anxiety and nervousness which can influence the results as well. To control for these adverse effects it is recommended to avoid caffeine during and prior to the experiment. Another factor that can possibly influence the results is that there we multiple experimenters conducting the experiment and each experimenter developed his/her own way, consciously or unconsciously, to run through the experimental procedure. Before the start of this experiment none of the experimenters had any experience using the tDCS equipment. It is plausible that there is some variation within the experimenters in attaching the electrodes and cap to the head of the participant.
The findings in this study don’t provide evidence that stimulation of the right DLPFC using tDCS improves the visual working memory, nor it provides evidence that it doesn’t. On account of these findings the theoretical explanation that applying tDCS leads to a better maintenance of sensory information caused by an increased cortical excitability isn’t
confirmed as well. This makes it little less likely for that explanation to hold true. This study differs from previous studies examining the visual working memory that visual memory performance was measured before, during and after 20 minutes of active or sham tDCS, whereas other studies often stop measuring after stimulation. Despite the limitations, these findings may contribute to answering the question how stimulation of the DLPFC influences visual working memory. If replicated, the findings in this research field might be helpful to develop appropriate interventions aiming at clinical benefits in patients with neurologic and psychiatric conditions.
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