We hypothesized that active anodal and cathodal tDCS would, respectively, enhance and diminish overall productivity on tests of verbal fluency. Based on our placement of the active electrode over the left dorsolateral prefrontal cortex, we expected to find more prominent tDCS effects on letter- than category-cued tasks and on measures of controlled (i.e., switching) than automatic (i.e., clustering) word retrieval processes. In a subsample of participants matched for basic demographic characteristics, our results provide partial support for our hypotheses in that anodal tDCS selectively enhanced aspects of verbal fluency while cathodal stimulation inhibited the same processes. However, our predictions regarding the type of fluency task and the qualitative aspects of fluency performance that would be most affected by tDCS were not supported.
In fact, we found that active anodal tDCS affected category-cued fluency productivity but had no discernible effects on letter-cued verbal fluency. Nor did tDCS alter controlled cognitive aspects of word retrieval (i.e., switching), despite our application of stimulation over the left dorsolateral prefrontal cortex, an area often associated with executive functioning and set-shifting. Rather, we found a nearly three-word increase in productivity on category-cued verbal fluency tasks in the anodal stimulation condition relative to the sham condition. Analyses of the qualitative aspects of verbal fluency productions suggest that this enhanced productivity was likely due to the increased clustering seen with anodal stimulation relative to both the sham and cathodal stimulation, and not due to changes in switching. Although more modest in its effect, cathodal stimulation also reduced clustering relative to sham stimulation.
The fact that we found effects of tDCS exclusively for category fluency, and not letter fluency, differs from the two other studies of tDCS and verbal fluency in healthy adults. Iyer et al. (2005
) found facilitative effects of 2
mA of anodal tDCS on overall productivity on a test of letter-cued fluency compared to sham and cathodal conditions. However, they did not find effects of tDCS in their initial experiment which used a lower current intensity (1
mA) and participants in their study did not complete category-cued fluency tasks. Cattaneo et al. (2011
) also used 2
mA of anodal stimulation and found improved productivity for both letter and category-cued fluency relative to sham stimulation. Although group means are not presented, a figural representation of the data suggests a larger magnitude of effect for category-cued relative to letter-cued fluency. Thus, our lack of findings for letter-cued fluency may be due to our decision to use 1
mA rather than 2
mA of current. We chose to use 1
mA because pilot testing revealed that subjects could reliably detect active stimulation at 2
mA whereas they could not at 1
mA. Thus, in our effort to blind our study participants to the stimulation condition, we may have also reduced the effectiveness of the experimental intervention. In addition, we administered sham and active tDCS separated by a 90-min washout during each session. We based this decision on evidence that the cortical excitability effects of short duration tDCS typically return to baseline by 60–90
min after the cessation of stimulation (Nitsche and Paulus, 2001
). However, if active tDCS stimulation combined with directed cognitive activity produces longer-last effects, this could have limited our ability to detect the behavioral effects of active tDCS. Future studies should explore whether increasing administration of a greater current density would produce effects for letter-cued fluency, as well as whether administering stimulation to more posterior regions would produce effects on both types of word fluency tasks.
Another weakness of this study is the heterogeneity of the initial study sample and unbalanced randomization into study groups. Participants were recruited through two methods, flyers placed on the Johns Hopkins University and medical campuses and through Internet ads (i.e., Craigslist). As a result, we recruited a rather homogenous group of young, well-educated participants along with a larger group of individuals having more diverse demographic characteristics. When examining the effects of tDCS on verbal fluency, we found no effects of tDCS within the full sample of participants. One hypothesis for this lack of findings is that the healthy, young, highly educated individuals who were over-represented in the anodal condition were already performing at ceiling and masked the effects of tDCS within the remaining participants. In fact, when the sample was trimmed to form two groups matched for relevant characteristics only then were the effects of tDCS apparent. Future studies should further explore the role of patient characteristics in relation to participant responsiveness to experimental interventions.
A related limitation to the current study is that, due to the small size of the final sample, we were unable to use multivariate ANOVA. Nor did we adjust for multiple comparisons. The latter decision was based on the fact that this was an exploratory study that aimed to determine whether tDCS could selectively alter controlled and automatic aspects of verbal fluency productions in healthy adults. We believe that the present findings, while relatively weak, suggest that tDCS can alter these word retrieval processes, as well as overall productivity on such tasks.
A final weakness is that this study employed a single-blind rather than double-blind experimental design. The tDCS device we used is not programmable in a way that permits one to blind both the experimenter and participant to the experimental condition. We did have one experimenter administer the cognitive testing while another operated the tDCS device, but this did not blind the machine operator to the experimental condition, and the other experimenter usually could discern whether a recipient was receiving active or sham stimulation. A procedural “workaround” for this limitation is possible but cumbersome in practice, and was not used in the present study. Fully programmable tDCS devices that overcome this limitation are recommended for use in future studies.
To our knowledge, this is the first study to investigate the utility of tDCS as a means of altering automatic and controlled aspects of speeded lexical during both letter and category word fluency tasks in neurologically healthy adults. We found that anodal tDCS was associated with an increase in overall productivity during a category-guided verbal fluency task, and that anodal stimulation led to a relative increase in clustering whereas cathodal stimulation had the opposite effect. These findings, although preliminary, suggest that tDCS may be an effective tool in ameliorating language dysfunction in disorders characterized by deficient activation or functioning of the semantic network. Our ongoing work is exploring this issue in such individuals including those with aphasia, autism spectrum disorders, and schizophrenia.