Modulation of executive control in dual tasks with transcranial direct current stimulation (tDCS)
Highlights
• Investigation of causal relation of lPFC activity and dual‐task executive functions.
• Application of anodal and cathodal tDCS in dual‐task situations.
• Improved dual‐task executive functions with anodal tDCS; no effect of cathodal tDCS.
• Evidence for causal involvement of lPFC activity and executive functions.
Introduction
Dual-task performance is characterized by the requirement to coordinate two simultaneous task processing streams. This need to coordinate two tasks is accompanied by impaired performance, such as increased processing time and error rates, compared to the performance in single-task situations (i.e., dual-task costs). Recent studies with functional magnetic resonance imaging (fMRI) have shown that executive control processes are involved in such task coordination and that higher demands on these processes are associated with increased activity in the lateral prefrontal cortex (lPFC; D’Esposito et al., 1995; Koechlin et al., 1999; Schubert and Szameitat, 2003; Stelzel et al., 2008; Szameitat et al., 2006, Szameitat et al., 2011, Szameitat et al., 2002). The areas of increased activity were located in regions surrounding the inferior frontal junction (IFJ), the inferior frontal sulcus (IFS), and in regions of the middle frontal gyrus (MFG).
However, so far, the association between increased demands on dual-task coordination and increased activation of lPFC, as seen on fMRI, remains correlative. This correlative relationship is a result of the basic nature of the fMRI method, reflecting neuronal mass activity with its implications for drawing judicious conclusions that are most frequently ignored (Logothetis, 2008). For instance, rather than showing simple feed-forward integration of cortical input in the lPFC, fMRI signals cannot unambiguously reflect the underlying functional role since these signals are typically a combination of neural mechanisms, such as a local connectivity with strong excitatory and inhibitory recurrence (Douglas and Martin, 2004). Moreover, lPFC activations usually do not occur in isolation but in synchrony with task-specific areas (e.g., Stelzel et al., 2009), rendering conclusions about region-specific effects of these activations difficult. Thus, conclusions on the causal role of lPFC activity and its function-specific processing in executive control in dual tasks based on fMRI signals are unwarranted. We address this open issue by noninvasive brain stimulation, such as transcranial direct current stimulation (tDCS), which modulates lPFC activity in order to test whether the lPFC is causally related to executive functioning in dual tasks.
Executive functions are particularly essential in dual tasks since some task components cannot be processed simultaneously, but instead only sequentially, and thus compete for access to the same capacity-limited processing structure (i.e., a bottleneck). This bottleneck is typically located at the central task processing stage including response selection and has been characterized as structural (i.e., unavoidable; e.g., Pashler, 1994; Pashler and Johnston, 1989) and/or strategic (e.g., Meyer and Kieras, 1997; with the potential of capacity sharing, Tombu and Jolicœur, 2003). The left IFJ has often been linked to this central bottleneck (Dux et al., 2006, Dux et al., 2009, Hesselmann et al., 2011, Ivanoff et al., 2009, Jiang and Kanwisher, 2003). The capacity-limited nature of this bottleneck explains one of the most prominent findings in dual-task research: the effect of the Psychological Refractory Period (PRP) (i.e., PRP effect). This effect is realized in situations in which two tasks are presented with varying stimulus onset asynchronies (SOAs) and processing times for the second of the two tasks (Task 2) increase with decreasing SOA, whereas processing times for the first task (Task 1) are usually unaffected by SOA (Pashler, 1994, Schubert, 1999). In line with other authors, we assume that the coordination of bottleneck access for Task 1 and Task 2 in a PRP situation is not a passive mechanism but involves active control processes (de Jong, 1995, Kamienkowski et al., 2011, Liepelt et al., 2011, Meyer and Kieras, 1997, Sigman and Dehaene, 2006). These processes include the planning of the appropriate sequence of actions and the online control of the serial processing order of tasks.
To provide neuropsychological evidence for the assumption of active task order planning, Szameitat et al. (2002) used a version of the PRP paradigm and compared the fMRI signals between dual-task blocks with different demands on task-order control. In these blocks, a visual and an auditory component task were presented in dual-task blocks with either a random temporal order or in blocks with a fixed order of the two component tasks. In random-order blocks, the task order changed randomly from trial to trial. Accordingly, participants needed to control task processing permanently to perform the tasks in the correct temporal order (i.e., task order control). In fixed-order blocks, however, the task order was constant across all trials and the need for task order control is thus reduced compared to random order blocks (albeit still present due to the involved bottleneck). The increased demands on task order control in random-order vs. fixed-order blocks led to extended fronto-parietal network with activation foci in the left and right lPFC when comparing the BOLD signal changes in random-order in contrast to fixed-order blocks (see also Stelzel et al., 2008).
In addition to a manipulation of the task order in a block design (i.e., random-order vs. fixed-order dual-task blocks; Szameitat et al., 2002), a trial-wise manipulation is essential since a block design is not completely conclusive in its indication of the association between lPFC activity and task control. That is, this block design may have resulted in some further confounding influences, which may hamper the final interpretation of the findings. For example, participants do not know which task is presented first in random-order blocks, while they do know in fixed-order blocks. Accordingly, the demand on divided attention between both tasks and the potential to prepare the task order may have been different in the two types of dual-task blocks. Thus, differences in task-order preparation may have caused the activation difference between random-order and fixed-order blocks. To allow a more elaborate manipulation of dual-task order control, Szameitat et al. (2006) compared (1) same-order vs. (2) different-order trials in the context of random-order blocks. In a same-order trial, the task order is identical to the order in the preceding trial. This order, however, changed in a different-order trial. In same-order trials, in contrast to different-order trials, the authors demonstrated reduced dual-task interference (i.e., dual-task costs in RTs and error rates are reduced in same-order trials). In addition, lPFC activation was reduced in same-order trials and this reduction may have been associated with decreased demand on task-order preparation in this trial type.
To modulate lPFC activation and executive functioning, we applied tDCS in the present study. tDCS is a noninvasive technique for brain stimulation that induces prolonged functional changes in the cerebral cortex (Nitsche and Paulus, 2011). During tDCS, weak electrical currents are applied to the scalp to modulate the excitability of underlying neural populations (Nitsche et al., 2003). Even though the stimulating electrodes are relatively large, high spatial specificity for cognitive tasks has been demonstrated for the combination of localized task-related activity and placement of the electrode (e.g., ventral vs. dorsal inferior frontal gyrus for semantic word generation; Holland et al., 2011; Meinzer et al., 2012). The most consistent beneficial effects on motor and cognitive functions have been reported for anodal stimulation (atDCS; Kuo and Nitsche, 2012) that facilitates firing of task-specific neuronal populations. Among other functions, this induced physiological state supports facilitating working-memory updating (e.g., Andrews et al., 2011; Fregni et al., 2005), and executive control functions of inhibition (Beeli et al., 2008, Jacobson et al., 2011). In contrast, cathodal stimulation (ctDCS) inhibits neuronal firing and generally decreases performance in the task under study (e.g., Nitsche and Paulus, 2000; Utz et al., 2010). Moreover, due to its excellent safety profile and effective placebo (sham tDCS) stimulation scheme (Gandiga et al., 2006), tDCS has become increasingly popular in clinical settings and research (Flöel, 2014, Kuo and Nitsche, 2012).
A recent study (Filmer et al., 2013) investigated the improvement of dual-task performance as an after-effect of tDCS (i.e., offline atDCS, ctDCS, and sham) over the left posterior lPFC. Speeded visual and auditory response-selection tasks were assessed in single tasks and in dual tasks (i.e., simultaneous presentation of both tasks). Immediately after ctDCS, the dual-task performance was improved in contrast to atDCS and sham stimulation while the dual-task performance was improved 20 min after atDCS and ctDCS in contrast to sham. Thus, while this study generally demonstrated the impact of tDCS on dual-task performance, the specific after-effects of atDCS and ctDCS in contrast to sham stimulation were mixed (i.e., atDCS has an effect similar to ctDCS only after a delay of 20 min after stimulation). Furthermore, the comparison of single- vs. dual-task performance yielded only limited information on executive control in dual tasks, since the impact of different SOAs and task orders, as well as the contribution of task-order control processes could not be investigated (e.g., de Jong, 1995; Luria and Meiran, 2003; Sigman and Dehaene, 2006; Szameitat et al., 2002, Szameitat et al., 2006). Moreover, Filmer and colleagues exclusively focused on the (offline) after-effects of tDCS on dual-task performance, leaving the impact of online stimulation an open issue (i.e., concomitant assessment of dual-task performance and tDCS).
The aim of the present study is to test the causal involvement of the lPFC in active task order planning (e.g., task-order preparation, task-order decision) under dual-task conditions. To test this involvement, we investigated whether atDCS-related facilitation, in contrast to sham, enhances performance in complex task situations. These task situations included multiple simultaneous (dual) tasks and executive functions that are required for an efficient control of these tasks (Experiment 1). In contrast, we applied ctDCS to investigate whether this stimulation type also affects the performance in complex task situations including multiple simultaneous (dual) tasks and executive functions that are required for an efficient control of these tasks (Experiment 2); in fact, due to the inhibitory character of ctDCS on neuronal firing, we would expect impaired executive control performance in dual tasks. This enhancement and/or impairment could demonstrate lPFC's excitability/inhibitory and define the function-specific causal role of this area in the context of dual-task executive functions. In the present study, we specifically applied atDCS/ctDCS over the area of the left IFJ, since IFJ activity correlates with executive functioning in dual-task situations (Dux et al., 2006, Dux et al., 2009, Schubert and Szameitat, 2003, Szameitat et al., 2006), as well as alternative situations requiring executive control (e.g., task switching; Brass and von Cramon, 2002, Brass and von Cramon, 2004).
Based on prior work (Stelzel et al., 2008, Szameitat et al., 2002, Szameitat et al., 2006), we manipulated the demand on executive functions in dual-task situations on two levels. First, we assessed the manipulation of the requirement of coordinating the temporal task order and access to a capacity-limited structure in form of dual-task blocks with random task order vs. fixed task order; in addition, we performed single-task blocks with no multiple task coordination requirement. Based on their increased task order processing demands, we hypothesized that atDCS (Experiment 1)/ctDCS (Experiment 2) should particularly affect random-order blocks when the level of activation in the left IFJ is crucial for the performance level of task-order control. Here, atDCS would lead to increased excitability in the IFJ, and subsequently more efficient (e.g., speeded) task-order control processes. In contrast, ctDCS should lead to reduced excitability in the IFJ and less efficient task-order control.
Second, within the context of random-order blocks, the preparation of the task order could be a consequence of the application of task-order information in a previous trial when preparing the task order in a current trial (de Jong, 1995, Luria and Meiran, 2003). This preparation may particularly contribute to the efficiency of task-order decisions under conditions of same-order trials. If atDCS/ctDCS, in contrast to sham, over the left IFJ improves/impairs performance in same-order trials (e.g., reduced/increased RTs), then such a finding would provide evidence for a causal involvement of the IFJ excitability in task-order preparation. We assess both hypotheses (i.e., [1] impact of atDCS/ctDCS on random-order blocks, [2] impact of atDCS/ctDCS on same-order vs. different-order trials) and its relative timing of stimulation when applying this stimulation during random-order blocks (online stimulation) vs. before random-order blocks (offline stimulation in regards to this block type; for details see 2.1 Methods, 3.1 Methods).
Similar to Filmer et al. (2013), we were also interested in the effects of timing of tDCS. So we assessed random-order dual-task blocks during atDCS/ctDCS (online stimulation), as well as after these stimulation types (offline stimulation). Therefore, we are able to analyze dual tasking in random-order blocks and its relative timing of stimulation (Stagg et al., 2011). This issue of timing in behavioral tasks has been investigated most thoroughly in the motor system, but these studies have recently been extended to the cognitive domain, including attention switching (Stone and Tesche, 2009) or language learning (Flöel, 2012, Sparing et al., 2008). For instance, concomitant atDCS and implicit motor learning led to an improvement in the rate of learning (Nitsche et al., 2003), while learning after atDCS was not significantly enhanced (Kuo et al., 2008). A mechanistic explanation for these timing effects of atDCS could be that the changes in cortical perfusion with widespread decreases in cortical perfusion being demonstrated after atDCS compared to the period during stimulation (Stagg et al., 2013). Analogous to findings on implicit motor learning, our hypothesis was that the effect on dual-task performance is increased under concomitant atDCS/ctDCS in contrast to dual-task performance following stimulation.
Section snippets
Experiment 1
In Experiment 1, we realized two component tasks in single tasks, fixed-order dual tasks as well as random-order dual tasks (including same-order and different-order trials), and compared the performance in these situations under conditions of atDCS and sham stimulations.
Experiment 2
In Experiment 2, we investigated an inhibitory impact of ctDCS at the scalp over the left IFJ when contrasted to sham. Furthermore, this experiment controls for the finding of a performance benefit after active stimulation (i.e., long atDCS) vs. passive stimulation (i.e., short sham stimulation) on dual-task performance under random-order block conditions in Experiment 1.
General discussion
The aim of the present study was to investigate the causal relation of activity in the left IFJ on executive functioning in a dual-task context. To approach this question, we applied atDCS (Experiment 1) and ctDCS (Experiment 2) over the scalp of this prefrontal area and compared dual-task and single-task performance under these stimulation conditions with the performance under a placebo condition (i.e., sham). Experiment 1 demonstrated that dual-task performance in random-order blocks
Acknowledgment
The present research was supported by a Grant of the German Research Council to T.S. (last author) and A.F. (Fl 379-8/1, Fl 379-10/1, Fl 379-11/1, and DFG-Exc 257), as well as, to A.F., by the Else-Kröner Fresenius Stiftung (2009-141 and 2011-119), and the Bundesministerium für Bildung und Forschung (FKZ 0315673A, 01EO0801, and 01GY1144).
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